Aided phytostabilisation of As- and Cu-contaminated soils using white lupin and combined iron and organic amendments

Journal of Environmental Management 205 (2018) 142e150

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Research article

Aided phytostabilisation of As- and Cu-contaminated soils using white lupin and combined iron and organic amendments
nez, Pilar Zornoza, Jesús M. Pen ~ alosa Teresa Fresno*, Eduardo Moreno-Jime Department of Agricultural Chemistry and Food Sciences, Faculty of Sciences, Universidad Autonoma de Madrid, 28049, Madrid, Spain

a r t i c l e i n f o

a b s t r a c t

Article history: Received 23 June 2017 Received in revised form 21 September 2017 Accepted 25 September 2017

An aided phytostabilisation strategy consisting of several composite amendments of iron sulphate and organic materials combined with Lupinus albus L. (white lupin) was evaluated for remediation of an Asand Cu-contaminated soil. Iron sulphate was combined with lime, paper mill sludge (PS), olive mill waste compost (OMWC) or holm oak biochar (BC) and applied to a slightly acidic soil with high concentration of As (~2200 mg kg
1) and Cu (~150 mg kg
1). White lupin was grown for 48 days in pots containing amended and non-amended soils and the effect of soil treatments on soluble and extractable trace elements, soil fertility and plant growth and composition was evaluated. The addition of the amendments raised soil pH and reduced soluble As (50e93%) and extractable As and Cu (50e89%). Despite the reduction of As- and Cu-extractable fractions, plant As and Cu uptake was not greatly affected by the amendments. Variations in soil pH and P-Olsen seemed to have influenced As dynamics in the treated soils, although they did not provoke its mobilisation with respect to the non-amended soil. Our results suggest that the freshly formed iron oxides resulting from addition of iron sulphate controlled As dynamics in the treated soils, avoiding its mobilisation due to application of organic materials. The combination of iron sulphate with OMWC and BC is shown as appropriate for aided phytostabilisation of metal(loid)s contaminated soils, as it improved soil fertility and plant nutrition while reduced As and Cu mobility. © 2017 Elsevier Ltd. All rights reserved.

Keywords: Lupinus albus L. Compost Biochar Iron sulphate Soil fertility

1. Introduction It has been recently estimated that approximately 342,000 sites in Europe are currently contaminated and among the main contamination sources, industrial activities, including mining, represent 33% (Panagos et al., 2013). Soils affected by mining activities are usually characterised by the co-presence of metals and metalloids, whose different chemical behaviour may be a challenge for the selection of an appropriate soil remediation technique. In addition, these soils generally present a loss of their ecosystem functions, which hinders the establishment of a plant cover (Sneath et al., 2013; Burges et al., 2015). Conventional soil cleanup technologies, such as excavation and landfill or vitrification, may abate this problem; however, they are generally costly, very invasive and significantly alter soil functions and biodiversity (Ali et al., 2013). On the other hand, environmental-friendly or gentle remediation options, such as ‘aided phytostabilisation’, follow the conservation

* Corresponding author. E-mail addresses: [email protected], [email protected] (T. Fresno). https://doi.org/10.1016/j.jenvman.2017.09.069 0301-4797/© 2017 Elsevier Ltd. All rights reserved.

or improvement of soil functionality while reduce the mobility and availability of pollutants (Cundy et al., 2013, 2016). The reutilisation of wastes as amendments may imply added economical and agricultural value to a soil remediation strategy, due to the reduction of their final disposal and the recycling of nutrients (Alvarenga et al., 2015; Clemente et al., 2015). For instance, the addition of compost and other carbonaceous materials produced from biomass to polluted soils generally results in an improvement of soil fertility and physical properties and supports

pez et al., 2016; Jones et al., 2016). Other plant growth (Alvarez-L o residual materials with considerable amounts of organic matter, such as paper mill sludge, sewage sludge or sugar beet lime, have been also proposed as suitable amendments for the remediation of
n et al., 2006; Alvarenga et al., metal(loid)s-polluted soils (Madejo 2009; Rodríguez et al., 2016). However, the addition or organic materials to As-contaminated soils have often resulted in As mobilisation provoked by competition between arsenate and dissolved organic matter for the same sorption sites or due to the usually alkaline nature of these materials (Bauer and Blodau, 2006; Beesley et al., 2013; Galende et al., 2014). Therefore, As-scavengers

T. Fresno et al. / Journal of Environmental Management 205 (2018) 142e150

such as iron oxides or their precursors can be co-applied to avoid this undesirable effect (Sneath et al., 2013; Fresno et al., 2016). When aided phytostabilisation is implemented, the success in the establishment of a plant cover is essential, as plants can minimize the dispersion of contaminants (Wong, 2003). Thus, the evaluation of soil fertility and plant nutritive status may provide further information about the effectiveness of a given strategy. Lupinus albus L. has been proposed as a good plant for phytostabilisation due to its metal-excluding behaviour and its tolerance to different environmental constraints (Castaldi et al., 2005; Vazquez
et al., 2009). In addition, the use of et al., 2006; Martínez-Alcala legumes for crop rotation may enhance the soil remediation process by increasing soil fertility due to their N2-fixing capacity (Reichman, 2007; Fumagalli et al., 2014). The objective of this work was to evaluate the effectiveness of several soil amendments combining iron sulphate and organic materials in aided phytostabilisation of As- and Cu-contaminated soils. The influence of the amendments on As and Cu geochemistry and the improvement of soil fertility and Lupinus albus L. growth were assessed.

2. Materials and methods 2.1. Soil and amendments A contaminated material was collected from the spoil heaps of an old smelting factory located in Guadalix de la Sierra, in the north of Madrid (Spain). The waste material was rich in arsenopyrite and scorodite and had high concentration of As and Cu. An uncontaminated soil was collected from a nearby area, sieved at <4 mm, and mixed with the contaminated material (<2 mm) in a ratio 95:5 (w:w) to obtain a composite soil, henceforth referred to as soil. The following materials were used as soil amendments: (1) iron sulphate (FeSO4$7H2O, PRS grade) and CaCO3 (PRS grade), both purchased from Panreac (Barcelona, Spain); (2) paper mill sludge (PS), obtained from the company Holmen Paper S.L. (Madrid, Spain); (3) olive mill waste compost (OMWC), prepared from solid olive mill waste (alperujo) and cow manure at CEBAS-CSIC (Murcia, Spain); (4) holm oak biochar (BC), produced by the pyrolysis of holm oak
nez et al., 2016). All the woodchips at 600  C (Moreno-Jime amendments were air dried, sieved to <2 mm and characterised. Some characteristics of the composite contaminated soil and the organic materials are shown in Table 1.

143

2.2. Experimental design The soil and the corresponding amount of amendments (calculated on a soil dry weight basis) were manually mixed and homogenised to obtain the following treatments: (1) FeSO4 (1%) þ CaCO3 (0.37%) (Fe þ lime); (2) FeSO4 (1%) þ paper mill sludge (1%) (Fe þ PS); (3) FeSO4 (1%) þ CaCO3 (0.29%) þ olive mill waste compost (3%) (Fe þ OMWC); (4) FeSO4 (1%) þ CaCO3 (0.15%) þ holm oak biochar (3%) (Fe þ BC). A control, consisting of the nonamended soil, was established. In order to obtain similar soil pH to that obtained with treatment Fe þ PS in previous studies, the amount of CaCO3 applied in treatments (1), (3) and (4) was adjusted to the content of carbonates added when applying 1% of PS in treatment (2). Carbonates content of OMWC and BC was accounted for adjustment in treatments (3) and (4). The mixtures were gently homogenised and 3.5 kg were placed in pots (four replicates per treatment). One rhizon sampler (Rhizosphere Research Products, Wageningen, The Netherlands) was inserted in each pot at an angle of 45 . The mixtures were left to equilibrate for 2 weeks and then a one-week-old Lupinus albus L. seedling previously grown in peat was transplanted to each pot. Plants were cultivated for 48 days in a growth chamber with controlled conditions (day/night: 13/11 h, 40/60% RH and a photon flux density of 520 mmol m
2 s
1). All soils were kept at 70% WHC during the experiment by weighing and adding water losses every two days. Porewater was extracted 14, 28, 42 and 48 days after transplanting and the pH was immediately measured. Porewater samples were filtered through 0.45-mm syringe filters and stored at 4  C until their analysis. After 48 days of plant growth, white lupin plants were harvested and separated into shoots (aboveground biomass) and roots and fresh weights were recorded. All plants presented nodules in their roots, so they were separated from the root system, counted and weighed in order to evaluate a possible relationship between their characteristics and plant growth and N content. Roots were washed with tap and distilled water and sonicated for 3 min to remove soil particles. Plant material was dried at 65  C for 3 days for its analysis. 2.3. Plant and soil analyses For plant analyses, ground biomass (0.2 g) was digested with 4 mL of HNO3 (65% v/v, PA, Sigma-Aldrich) and 1 mL of H2O2 (30% v/ v, PA, Fluka) under a pressure of 1.5 kg cm
2 for 30 min (modified from Lozano-Rodríguez et al., 1995). The concentration of As and Cu in plant digests was analysed by ICP-MS (Elan 9000 DRCe,

Table 1 Main characteristics of the (composite) soil (contaminated soil:uncontaminated material 95:5 w:w) and the amendments used in this experiment. Data are mean (n ¼ 4) ± standard error (SE). PS paper mill sludge; OMWC olive mill waste compost; BC biochar EC electric conductivity; OMLOI organic matter measured by loss on ignition.

pH EC (dS m
1) Clay (%) Silt (%) Sand (%) OMLOI (%) Carbonates (%) Pseudo-total element (mg kg
1) As Cu Zn Fe Mn K Na Ca Mg

Soil

PS

OMWC

BC (from holm oak)

5.4 ± 0.1 1.85 ± 0.04 14.4 22.6 63 2.35 ± 0.01 e

8.69 ± 0.04 0.54 ± 0.02 e e e 31.9 ± 0.1 37 ± 6

9.39 ± 0.01 6.98 ± 0.11 e e e 71 ± 2 2.7 ± 0.6

9.8 ± 0.1 2.4 ± 0.2 e e e 75 ± 4 7.4 ± 0.6

2258 ± 625 157 ± 33 73 ± 11 17058 ± 1380 83 ± 19 e e e e

0.0095 ± 0.0004 125.5 ± 2.3 46.7 ± 0.7 717 ± 23 62 ± 2 46 ± 3 57 ± 1 15406 ± 279 256 ± 8

0.0071 ± 0.0007 24.8 ± 0.7 128 ± 5 820 ± 8 66 ± 3 2099 ± 14 234 ± 3 2945 ± 75 492 ± 20

0.0010 ± 0.0001 12.4 ± 0.3 32.6 ± 2.1 1014 ± 53 726 ± 35 521 ± 15
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PerkinElmer). Ca, Mg, K and P concentrations were measured by ICP-OES (ICAP 6500 DUO, Thermo Scientific). The total content of nitrogen (TN) was directly analysed in the shoots with a LECH CHNS-932 Analyser. The concentration of As, Cu, Fe and P in soil porewater samples was analysed by ICP-MS and dissolved organic carbon (DOC) was measured using a TOC analyser (Shimadzu TOCV CSH). Soil pH was measured in soil:water extracts (1:2.5 v:v). The labile element fraction in soils was determined by extraction with 0.1 M (NH4)2SO4 (1:10 w:v, shaken at 140 rpm for 4 h). Arsenic was analysed in the extracts by hydride generation-atomic fluorescence spectroscopy (HG-AFS, PS Analytical 10.055 Millenium Excalibur) and Cu and Fe by atomic absorption spectroscopy (AAS, Analyst 800, Perkin Elmer). P-Olsen was measured in 1:20 (w:v) NaHCO3extracts by ICP-OES. Exchangeable K, Ca, Mg and Na were extracted with 1 M ammonium acetate (pH 7); the concentration of Ca and Mg in the extracts was measured by AAS and K and Na by atomic emission spectroscopy (AES). TOC and TN contents were measured in HCl-pretreated soil samples with a LECH CHNS-932 Analyser. 2.4. Data analysis The statistical analysis of data was performed using IBM SPSS Statistics 21. Data were checked for normality (Shapiro-Wilk test) and homoscedasticity; logarithmic transformations were applied when necessary. Differences among treatments were evaluated by analysis of variance (one-way ANOVA) followed by Tukey's HSD test (homoscedastic data) or by Games-Howell test (heteroscedastic data). Bivariate correlations (Pearson's coefficient) and multiple linear regression analyses (stepwise, backward and forward methods) were carried out to assess the relationship between several variables. Prediction of metal speciation was carried out with the software Visual Minteq v. 3.1 (2013).

of DOC concentration in porewater (Fig. 1). In this treatment, DOC varied between 93.6 and 108.6 mg L
1 along the experiment, while in the other treatments and the control it varied between 27.4 and 50.1 mg L
1. DOC concentration remained constant along the experiment in all treatments. 3.1.2. Soil pH and extractable elements All treatments significantly reduced (P < 0.05) the (NH4)2SO4extractable As at the end of the experiment (Fig. 2). Arsenic concentration in the (NH4)2SO4-extracts of Fe þ lime-, Fe þ PS-, Fe þ OMWC- and Fe þ BC-treated soils was 89%, 81%, 74% and 79% lower than that in the control. Between treatments, the concentration of extractable As was significantly higher (P < 0.05) in Fe þ OMWC and Fe þ BC than in Fe þ lime, whereas no differences were found between Fe þ lime and Fe þ PS. The concentration of (NH4)2SO4-extractable Cu was significantly higher (P < 0.05) in the control than in the treated soils and was reduced by 72% by Fe þ lime, 46% by Fe þ PS, 35% by Fe þ OMWC and 56% by Fe þ BC (Fig. 2). Between treatments, extractable Cu was significantly higher (P < 0.05) in Fe þ PS and Fe þ OMWC than in Fe þ lime. The addition of Fe þ PS, Fe þ OMWC and Fe þ BC resulted in a significant increase (P < 0.05) in soil pH, which was 0.8, 0.9 and 1.3 pH units higher in Fe þ PS, Fe þ OMWC and Fe þ BC, respectively, than in the control. However, no significant differences were found between Fe þ lime and the control (Fig. 2). Between the treated soils, significant differences (P < 0.05) were found between Fe þ lime, Fe þ PS, Fe þ OMWC and Fe þ BC; in these soils the pH varied in the order: Fe þ BC > Fe þ OMWC > Fe þ PS > Fe þ lime. P-Olsen was significantly higher (P < 0.05) in Fe þ OMWC and Fe þ BC than in the control, Fe þ lime and Fe þ PS (Fig. 2). The increase in Fe þ OMWC and Fe þ BC with respect to the control was by 2.8 and 1.9 times. No differences were found between the control, Fe þ lime and Fe þ PS.

3. Results 3.1. Soil chemistry 3.1.1. Soil porewater The treatments resulted in a significant decrease (P < 0.05) in the concentration of As in soil porewater with respect to the control at all sampling times (Fig. 1). At the last sampling time (day 48), the reduction in soluble As in Fe þ lime, Fe þ PS, Fe þ OMWC and Fe þ BC accounted for 93%, 62%, 69% and 50% of the control, respectively. The concentration of As in the porewater significantly increased (P < 0.05) throughout the experiment in most of the treatments. At day 48, As concentration in porewater of the control, Fe þ PS, Fe þ OMWC and Fe þ BC soils was ~24%, ~77%, ~63% and ~89% higher, respectively, than that at day 14. However, in Fe þ lime As concentration was >3-fold lower at day 48 than at day 14 (Fig. 1). After 14 days of lupin growth, the treatments significantly reduced (P < 0.05) the concentration of soluble Cu with respect to the control (Fig. 1). The decrease of soluble Cu in treated soils accounted for >50% and was the largest in Fe þ BC. In the control, Fe þ lime and Fe þ PS, soluble Cu significantly decreased (P < 0.05) throughout the experiment, whereas in Fe þ OMWC and Fe þ BC, Cu concentration in porewater remained constant at all sampling times (Fig. 1). All treatments provoked a significant increase (P < 0.05) in soil porewater pH compared to the control; it was 1.4, 1.7, 2.0 and  2.2 pH units higher in Fe þ lime, Fe þ PS, Fe þ OMWC and Fe þ BC than in the control, respectively (Fig. 1). Porewater pH remained constant throughout the experiment in all cases. Most of the treatments had little effect on DOC concentration, except Fe þ OMWC, that resulted in a significant increase (P < 0.05)

3.1.3. Soil nutrients As expected due to the addition of CaCO3 in the composite amendments, the concentration of ammonium acetate-extractable Ca significantly increased (P < 0.05) in all the treated soils (Table 2). Exchangeable K significantly increased in the Fe þ OMWC- and Fe þ BC-treated soils, and it was more than 15 and 3 times higher, respectively, than in the control soil. The concentration of exchangeable Mg increased by 2.2-fold in Fe þ OMWC and by 1.5fold in Fe þ BC, with respect to the control soil. The treatments Fe þ OMWC and Fe þ BC also resulted in a significant increase (P < 0.05) in TOC and TN contents in soil. 3.2. Plant growth and As, Cu and nutrients uptake Treatments Fe þ OMWC and Fe þ BC slightly increased lupin shoots biomass, although not significant differences were found between them and the control (Fig. 3). No differences were found between Fe þ lime, Fe þ PS and the control either. None of the treatments significantly increased root biomass. The treatments Fe þ OMWC and Fe þ BC resulted in a significant reduction (P < 0.05) in the concentration of As in lupin shoots (Fig. 4), whereas no differences were found between Fe þ lime, Fe þ PS and the control plants. Nevertheless, a slight decrease in shoots As concentration was observed in all treated plants; compared to the control plants, As concentration was 1.2-fold, 1.2fold, 2.3-fold and 2.0-fold lower in shoots from Fe þ lime, Fe þ PS, Fe þ OMWC and Fe þ BC treatments. The amendments did not greatly affect the concentration of As in roots, although it was slightly but not significantly lower in roots from Fe þ OMWC and Fe þ BC-treated soils (Fig. 4). In any case, the total amount of As

T. Fresno et al. / Journal of Environmental Management 205 (2018) 142e150

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Fig. 1. Concentration of As, Cu and DOC and pH measured in soil porewater collected 15, 28, 42 and 48 days after white lupin transplanting. Data are mean (n ¼ 4) ± SE. PS paper mill sludge; OMWC olive mill waste compost; BC biochar.

accumulated in the plants (in mg As plant
1) did not differ among treatments (not shown). There were neither statistical differences in Cu concentration in white lupin shoots nor in roots (Fig. 4), likely due to the high variability (standard error) of the data. However, an increase was observed in the concentration of Cu in shoots from Fe þ lime and Fe þ PS with respect to the control plants, which accounted for 75% and 78%, respectively. A slight increase was observed in the Cu concentration in roots of plants from all treated soils, especially Fe þ BC. Despite the increase in the exchangeable Ca, its concentration in lupin shoots was significantly lower (P < 0.05) in plants from all treated soils than in those grown in the control (Table 3). All the treatments provoked an increase, to a greater or lesser extent, in the K concentration in shoots, but Fe þ OMWC and Fe þ BC were those which significantly affected (P < 0.05) K uptake by white lupin. Similarly, P accumulation in shoots was significantly higher (P < 0.05) in Fe þ OMWC and Fe þ BC-treated plants. Magnesium concentration was significantly higher (P < 0.05) in plants grown in Fe þ BC-treated soil than in those from the control and the other treatments, whereas no statistical differences were found between Fe þ lime, Fe þ PS, Fe þ OMWC and the control. Phosphorous concentration, although remained low, was significantly enhanced (P < 0.05) by the addition of Fe þ OMWC, with respect to the control. Although no statistical differences were found in N concentration, a slight increase was observed in plants grown in Fe þ OMWC- and Fe þ BC-treated soils (Table 3).

The number of nodules found in the roots of each treatment and the average dry weight per nodule are shown in Table 4. The nodules seemed to be active because of their light red colour (indicating presence of leg-haemoglobin). The number of nodules in Fe þ BC-treated roots was significantly higher (P < 0.05) than in the control and Fe þ lime, whereas no differences were found between the control and Fe þ lime, Fe þ PS and Fe þ OMWC treatments. However, the Fe þ PS- and Fe þ OMWC-treated plants had on average 11 and 13 more nodules, respectively, than in the control. The average dry weight of each nodule was significantly higher (P < 0.05) in the control than in the treated roots, although no statistical differences were found in the total fresh weight of nodules in each root. 4. Discussion 4.1. Influence of soil amendments on As and Cu mobility All treatments effectively reduced As mobility with respect to the control, since their application resulted in a significant decrease in the concentration of As in soil porewater (Fig. 1) and in the concentration of (NH4)2SO4-extractable As (Fig. 2). Iron sulphate has been proven to be a good immobiliser of As, as its application to soils results in the rapid formation of fresh iron (hydr)oxides (such as ferrihydrite, goethite or hematite) in situ that adsorb As and stabilise it in the long term (Cutler et al., 2014; Katsoyiannis and Zouboulis, 2002; Miretzky and Fernandez

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T. Fresno et al. / Journal of Environmental Management 205 (2018) 142e150

Fig. 2. Soil pH, concentration of (NH4)2SO4-extractable As and Cu and P-Olsen in the control and the treated soils at the end of the experiment. Data are mean (n ¼ 4) ± SE. Different letters indicate significant differences among treatments (P < 0.05). PS paper mill sludge; OMWC olive mill waste compost; BC biochar.

Table 2 Concentration of ammonium acetate-extractable Ca, K, Mg and Na (mg kg
1), total organic carbon (TOC) and total nitrogen (TN) (g kg
1). Data are mean (n ¼ 4) ± SE. Different letters in the same column indicate significant differences among treatments (P < 0.05). Treatment

Ca

Control Fe þ lime Fe þ PS Fe þ OMWC Fe þ BC

1295 1992 1828 2560 2618

± ± ± ± ±

19 a 119 b 69 b 98 c 33 c

K

Mg

Na

47.5 ± 1.9 a 47.5 ± 2.8 a 53.7 ± 1.4 a 738.2 ± 33.8 c 161.1 ± 4.3 b

62.9 ± 3.7 a 58.2 ± 5.0 a 64.0 ± 2.7 a 141.2 ± 9.1 b 96.3 ± 1.3 c

11.2 11.6 13.6 79.5 13.3

Cirelli, 2010). Besides, As may be sequestered by its incorporation into iron minerals such as jarosite and scorodite (Savage et al., 2005). Contrary to that, As mobilisation upon addition of organic amendments, such as compost or biochar, has been previously reported (Clemente et al., 2010; Beesley et al., 2013). Since As mobility generally increases with increasing soil pH (Fitz and Wenzel, 2002), some authors highlight that enhancement in As mobility occurs due to the increase in soil pH, as organic materials usually present an alkaline character (Beesley et al., 2010). However, competition between dissolved organic matter (DOM) and arsenate for soil surface binding sites may also occur and would result in As release into the soil solution (Bauer and Blodau, 2006; Arco-L
azaro et al., 2016). Furthermore, the formation of soluble complexes between DOM and As with iron as a bridge cation can result in As

± ± ± ± ±

1.9 2.0 0.4 7.6 0.3

a a a b a

TOC

TN

7.5 ± 0.6 a 7.5 ± 0.4 a 7.1 ± 0.7 a 14.4 ± 1.9 b 19.2 ± 1.1 c

0.24 0.28 0.30 0.97 0.73

± ± ± ± ±

0.04 0.03 0.05 0.12 0.08

a a a b b

mobilisation (Ritter et al., 2006; Sharma et al., 2010; Mikutta and Kretzschmar, 2011). However, in this experiment the coapplication of iron sulphate led to a decrease in As mobility, contrary to the expected As mobilisation due to the addition of soluble OM. Even though the addition of Fe þ OMWC resulted in significantly higher DOC concentration in soil porewater, this did not provoke an increase in soluble As (Fig. 1). Results of predicted metal speciation (Table 5) showed that, being Fe3þ as the main iron species in the soil porewater, iron (III) hydroxides would predominate in soil solution of treatment Fe þ OMWC (the one with the highest DOC concentration). Furthermore, there was no correlation between As and DOC concentration in the porewater at any sampling time (data not shown), suggesting that the formation of soluble As-Fe-DOM complexes was unlikely to play a significant role

T. Fresno et al. / Journal of Environmental Management 205 (2018) 142e150

Fig. 3. Dry weight of white lupin shoots and roots after 48 days of cultivation in the control and the treated soils. Data are mean (n ¼ 4) ± SE. Different letters above bars indicate significant differences (P < 0.05) in shoots and roots weights among treatments. PS paper mill sludge; OMWC olive mill waste compost; BC biochar.

on As solubility, in agreement with Neubauer et al. (2013), who observed that As transport in a boreal watercourse was mainly associated to large iron (hydr)oxides colloids or aggregates (size

147

>0.2 mm) rather than by DOM, at pH > 4.5. As observed by Fresno et al. (2016), who assessed As partitioning between soil fractions, the addition of materials rich in organic matter (PS, OMWC and pine biochar) to an As-contaminated soil, applied together with iron sulphate, did not interfere with the ability of the newly formed iron (oxy)hydroxides to sequester As. In addition, in this work we found that the increase in soil pH provoked by the treatments did not lead to an increase in soluble and extractable As fractions (Figs. 1 and 2). Our results suggest that the co-addition of iron sulphate increased the As sorption capacity of the soil, thus mitigating the effects of pH and DOC. However, it is important to note that differences among treatments, both concerning soluble (Fig. 1) and extractable As (Fig. 2), were found. When comparing Fe þ lime, Fe þ PS, Fe þ OMWC and Fe þ BC in the last porewater sampling, As concentration was slightly (but not significantly) lower in Fe þ lime than in the other treatments and showed a decreasing tendency that was not observed in Fe þ PS, Fe þ OMWC and Fe þ BC (Fig. 1). This effect seemed to be related with the differences in soil porewater pH among treatments: when considering the treated soils only (i.e. without considering the control), we found a significant positive correlation between As concentration and porewater pH in the last time point (day 48: r ¼ 0.611, P < 0.05). Extractable As was also significantly higher in Fe þ OMWC and Fe þ BC (and slightly higher in Fe þ PS) than in Fe þ lime (Fig. 2); in this case the enhanced extractable As was affected by the higher P-Olsen concentration in

Fig. 4. Concentration of As and Cu in white lupin shoots and roots at harvest. Data are mean (n ¼ 4) ± SE. Different letters above bars indicate significant differences among treatments (P < 0.05). Where there are no letters, no statistical differences were found. PS paper mill sludge; OMWC olive mill waste compost; BC biochar.

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T. Fresno et al. / Journal of Environmental Management 205 (2018) 142e150

Table 3 Nutrients concentration in white lupin shoots (g kg
1 DW) after 48 days of plant growth. Mean (n ¼ 4) ± SE. Different letters in the same column indicate significant differences among treatments (P < 0.05). Treatment

Ca

Control Fe þ lime Fe þ PS Fe þ OMWC Fe þ BC

6.82 4.86 4.54 3.00 3.09

± ± ± ± ±

0.45 0.37 0.16 0.07 0.25

c b b a a

K

Mg

8.33 ± 1.36 a 16.67 ± 0.76 bc 14.14 ± 0.71 b 25.91 ± 0.41 d 19.06 ± 0.41 c

1.33 1.37 1.38 1.36 1.89

P ± ± ± ± ±

0.11 0.11 0.11 0.06 0.14

a a a a b

0.54 0.60 0.61 0.66 0.59

N ± ± ± ± ±

0.03 0.02 0.03 0.01 0.04

a

35.7 37.7 36.7 35.6 36.8

ab ab b ab

± ± ± ± ±

2.6 1.5 2.1 0.7 1.6

a a a a a

Table 4 Number of nodules per plant, fresh weight of all nodules in each plant and average fresh weight per nodule, calculated by dividing total fresh weight by the number of nodules. Mean (n ¼ 4) ± SE. Different letters indicate significant differences among treatments (P < 0.05). Treatment

Nodules fresh weight (g root
1)

Number of nodules

Control Fe þ lime Fe þ PS Fe þ OMWC Fe þ BC

21 28 32 34 60

± ± ± ± ±

a

0.43 0.19 0.30 0.28 0.34

2 2a 9 ab 10 ab 7b

± ± ± ± ±

0.04 0.04 0.08 0.07 0.09

Average fresh weight per nodule (mg)

a

21.1 ± 2.0 b 6.5 ± 0.7 a 9.5 ± 1.0 a 9.2 ± 1.3 a 5.4 ± 1.0 a

a a a a

Table 5 Predicted speciation of Cu, As and Fe (% of the total species) in soil porewater at the last sampling time (day 48). Calculations were made using Visual Minteq 3.1. Cu

Control Fe þ lime Fe þ PS Fe þ OMWC Fe þ BC

As 2þ

Cu-DOM

Cu

HAsO24

95.7 99.3 99.8 99.96 99.9

4.3 0.7 0.2 0.03 0.1

0.3 6.1 39.6 45.2 56.7

Fe H2AsO
4

H3AsO4

Fe-DOM

FeOH2þ

Fe(OH)þ 2

Fe(OH)3(aq)

99.1 93.8 60.4 54.8 43.3

<0.1 e e e e

87.3 11.9 0.8 1.5 0.3

1.9 0.8 <0.1 <0.1 <0.1

10.8 87.3 98.8 97.9 98.8

e e 0.4 0.4 0.7

Fe þ OMWC and Fe þ BC (r ¼ 0.858; P < 0.001). In order to clarify the factors most affecting As mobility within the treated soils, multiple linear regression was performed for porewater and extractable As. For soluble As ([As]PW), we used total As in soil, porewater pH and the concentration of P and DOC in the porewater as independent variables. For extractable As ([As]ext), the independent variables considered were total As, DOC concentration, P-Olsen and the pH of soil-water extracts. Equations (1) and (2) show the generated relationships concerning porewater and extractable As. [As]PW ¼
454 þ 90.9 pHPW R2 ¼ 0.374; F1,15 ¼ 8.36; P < 0.05 (1) [As]ext ¼ 0.297 þ 0.087 [P-Olsen] R2 ¼ 0.737; F1,15 ¼ 39.1; P < 0.001

(2)

Equation (1) shows that, within the treatments, As solubility was mainly affected by porewater pH, which means that an increase in soil pH resulted in As desorption from iron (hydr)oxides and thus an increase in As concentration in the soil solution. Equation (2) confirms that only P-Olsen had a significant effect on extractable As. Due to the fact that phosphate and arsenate behave chemically similarly in soils (Adriano, 2001), competition between these anions for mineral sorption sites can be expected, resulting in As mobilisation from less labile soil fractions (not readily soluble) and an increase in its availability, as already reported by other au
nez et al., 2013; Beesley thors (Clemente et al., 2012; Moreno-Jime et al., 2014). In any case, the increase in the P-Olsen provoked by Fe þ OWMC and Fe þ BC did not result in an increase in extractable As with respect to the control, which suggests again that As mobility in the treated soils was governed by its sorption onto iron oxides.

The reduction of soluble Cu provoked by the treatments at the beginning of the experiment (Fig. 1) was likely related to the increase in porewater pH, as also indicated by the significant negative correlation between these two variables (day 14: r ¼
0.884, P < 0.001; day 28: r ¼
0.690, P < 0.001). In Fe þ BC, retention of Cu by biochar through physical adsorption or complexation by functional groups could also have affected its immobilisation (Uchimiya et al., 2011), as very low concentration of Cu (<5 mg L
1) was found in the soil porewater of this treatment throughout the experiment. Copper speciation modelling showed that in all cases >99% of Cu in porewater was complexed by DOM (Table 5). Therefore, concentration of DOC would have been a major factor controlling Cu mobility between the treated soils. This would explain the higher Cu concentration in porewater of Fe þ OMWC and the positive correlation between Cu and DOC in this treatment (day 42: r ¼ 0.675, P < 0.01; day 48: r ¼ 0.707, P < 0.01), which showed the highest DOC concentration along the experiment (Fig. 1).

4.2. Effect of amendments on As and Cu uptake by Lupinus albus plants Despite the great reduction of extractable As provoked by the treatments, this decrease was not reflected on plant As uptake in all treatments. Although significant differences were observed between As concentration in shoots of the control and treatments Fe þ OMWC and Fe þ BC (Fig. 4), these differences could be a consequence of a slight increase in biomass production, i.e. due to a dilution effect (Fig. 3), as no significant differences were found in As accumulation in shoots (calculated by multiplying As concentration by shoots dry weight; data not shown). This could be related to recent observations by Fresno et al. (2017), who found As solubilisation in the rhizosphere of white lupin grown in iron-treated

T. Fresno et al. / Journal of Environmental Management 205 (2018) 142e150

soils, despite it was stabilised in the bulk soil, which was ascribed to As mobilisation triggered by root exudates. Similarly, plant Cu uptake did not correlate with chemical extractions data. Despite the lower extractable Cu in the treated soils than in the control (Fig. 2), no differences were found in Cu concentration in plant tissues (Fig. 4); this could be also related to rootinduced mobilisation of Cu in the rhizosphere. In any case, Cu concentration in shoots of any treatment cannot be considered as
nchez-Pardo and Zornoza, toxic for this plant (Marschner, 2012; Sa 2014).

149

and surface area of maize roots and the production of fine roots, so the same could be true in our study, resulting in higher surface to infect by the bacteria. However, the differences found in the size and number of nodules did not seem to affect N uptake, since statistical differences in the N content in shoots were not found. Although N content was slightly higher in Fe þ OMWC- and Fe þ BC-treated plants (Table 3), whether this was directly related with root nodulation or was due to the N supplied by these treatments should be further studied. 5. Conclusions

4.3. Effects on soil fertility and plant growth, mineral nutrition and nodulation Although iron-based amendments are generally efficient in stabilise As and metals in soils, their single application barely improve soil functions and plant growth and thus co-application of fertilizers or organic amendments are generally necessary (Bes and Mench, 2008; Hartley and Lepp, 2008). The treatments Fe þ OMWC and Fe þ BC were those that most affected available or total nutrients concentration in the soil, as both significantly increased the concentration of extractable Ca, K, Mg, TN, TOC (Table 2) and P-Olsen (Fig. 2). The great effect of OMWC addition on available K and Mg is not surprising taking into account the high total content of these nutrients in this material (Table 1). Similarly, BC supplied a high amount of Mg, which was reflected in an increase in its exchangeable fraction. OMWC has been proposed as a useful amendment to improve plant growth in aided phytostabilisation strategies as it provides nutrients and enhances soil health (Pardo et al., 2014a; Walker and Bernal, 2008). The mechanisms affecting nutrients availability by biochar can be also related with its large surface area and its high cation exchange capacity, which can reduce nutrients leaching (Laird et al., 2010). It should be noted that the biochar used in this study was relatively rich in some nutrients (Table 1). Our results were generally in agreement with other authors, who have reported that the use of biochar as a soil amendment had in general significant positive effects on several soil physico-chemical parameters (Biederman and Stanley Harpole, 2013; Bruun et al., 2014; Yue et al., 2017). White lupin growth was little affected by the treatments (Fig. 3), although Fe þ OMWC and Fe þ BC slightly increased shoots biomass; this was likely related with the higher P, K and Mg concentration in shoot tissues (Table 3). In fact, the addition of OMWC and BC has been shown to positively affect plant growth in previous studies (Pardo et al., 2014b; Brennan et al., 2014). Root nodules are formed due to the symbiotic relationship between leguminous plants and N2-fixing soil rhizobium bacteria, and can be negatively affected by high concentration of trace elements (Pajuelo et al., 2008), although different strains of rhizobium have been found in soils with high levels of As (Carrasco et al., 2005). In this work, the formation of nodules was not inhibited by the presence of As, since plants from all soils, including the control, presented active nodules in their roots and the total weight of nodules in each plant was similar in all cases (Table 4). On the contrary we found less but larger nodules in plants grown in the control soil, with the highest As availability. Reichman (2007) also observed a decrease in the number of nodules in soybean as the concentration of As in the nutrient solution increased and suggested that this would be related to the decrease in number of root hairs, and thus a reduction in the infection site, rather than due to As toxicity. Likewise, the largest number of nodules in Fe þ BC-roots of this work may be also explained by changes in root morphology provoked by biochar. Brennan et al. (2014) observed that biochar addition to an As- and Cu-contaminated soil enhanced the length

The treatments Fe þ lime, Fe þ PS, Fe þ OMWC and Fe þ BC effectively reduced As and Cu mobility in the contaminated soil. The in situ formed iron (hydr)oxides controlled As dynamics, thus mitigating the effect of pH and DOM. Despite this, differences in porewater pH and available P among the treated soils also affected As mobility. The application of iron sulphate plus OMWC (Fe þ OMWC) or BC (Fe þ BC) generally improved soil nutrients availability and nutrients content in white lupin tissues, compared to the sole application of iron sulphate and lime (Fe þ lime). Fe þ PS had little effect on soil fertility and plant nutrition despite its relatively high organic matter content. Longer term experiments should be carried out to evaluate if these effects on soil quality are stable over time. Acknowledgements This work has been financed by the Spanish Ministry of Economy and Competitiveness (project CTM2013-48697-C2-2-R/
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