Strategies for the use of plant biomass obtained in the phytostabilisation of trace-element-contaminated soils

Biomass and Bioenergy 126 (2019) 220–230

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Research paper

Strategies for the use of plant biomass obtained in the phytostabilisation of trace-element-contaminated soils

T

Maria Pilar Bernala,∗, Xiomar Gómezb, Ruixue Changc, Elena Arco-Lázaroa, Rafael Clementea a

Centro de Edafología y Biología Aplicada del Segura, CSIC, Campus Universitario de Espinardo, 30100, Murcia, Spain Chemical and Environmental Bioprocess Engineering Group, Natural Resources Institute (IRENA), Universidad de León, Av. de Portugal 41, 24009, León, Spain c College of Resources and Environmental Science, China Agricultural University, Beijing, China b

A R T I C LE I N FO

A B S T R A C T

Keywords: Phytoremediation Composting Anaerobic digestion Energy crops Thermal energy

The recycling options of the plant biomass produced during the phytoremediation of contaminated soils include the production of renewable energy (such as biogas or thermal energy) and also of useful products such as compost. The presence of trace elements (TEs) and the nature of the organic matter can affect the biodegradability of the biomass. The biomass of four plant species, Silybum marianum, Piptatherum miliaceum, Nicotiana glauca and Helianthus annuus, grown in a pot experiment for the phytostabilisation of a TEs contaminated soil was studied for biodegradability by biological aerobic and anaerobic transformation and for thermal energy production by thermal analysis and differential scanning calorimetry. According to the aerobic degradation results, all these plant materials are adequate for recycling by composting, with S. marianum being the least recommended due to the lowest potentially-mineralisable carbon. However, S. marianum was suitable for biogas production through anaerobic digestion, as together with P. miliaceum it showed the best results for biogas production potential, whereas, N. glauca gave low biogas production, related to its high Pb, lignin and VS concentrations and C/N ratio. The species most suitable for thermal energy purposes were again S. marianum and P. miliaceum, since both exhibited high energy release in the high-temperature regions of the thermal profile. Contrastingly, H. annuus and N. glauca produced high losses of mass at temperatures below 200 °C, which may indicate flammability risks during handling and storage.

1. Introduction In Europe, around 1,170,000 potentially contaminated soils have been identified [1]. The main contaminant categories are heavy metals and mineral oil, which contribute jointly to around 60% of soil contamination. Only around 58,000 of the contaminated soils have already been remediated, with an estimated total cost per project ranging from 50,000–500,000 € [1]. Remediation of polluted soils is essential, according to FAO [2], and novel, science-based biological remediation technologies must be developed and implemented to replace expensive physico-chemical methods. Phytoremediation of contaminated soils is based on the use of plants, soil amendments and agronomic practices to eliminate, retain or reduce the toxicity of soil contaminants. It is considered a gentle, sustainable remediation option, which can provide added-value through the compliance with conservation objectives and environmental protection, increased food safety, the replenishment of soil C reserves and the improvement of soil health. In the case of phytostabilisation of soils

∗

contaminated by trace elements (TEs), plants that do not accumulate the TEs in their aerial parts (excluders) are used, so the revegetation of the soil together with the use of amendments can guarantee the immobilisation of the contaminants. The commercial success of phytoremediation technologies depends on the generation of valuable biomass on contaminated soils. In this regard, the use of energy crops in the phytostabilisation of contaminated soils has recently received increasing attention [3–6], since value could be added to the plant biomass in the form of bioenergy [7]. In addition, the use of contaminated soils to produce energy crops may help to avoid competition with food production [5], and the use of native species as bioenergy crops would limit the introduction of nonnative species into the soil ecosystem to be remediated. The plant biomass produced during phytoremediation depends ultimately on the species used: populus and willow in short rotation coppice were found to produce 6–10 t dry matter ha−1, while high yield annual crops such as Nicotiana tabacum, sunflower, switchgrass and miscanthus can produce 5 to 9 t dm ha−1 [8,9]. The total biomass

Corresponding author. E-mail address: [email protected] (M.P. Bernal).

https://doi.org/10.1016/j.biombioe.2019.05.017 Received 26 October 2018; Received in revised form 29 April 2019; Accepted 20 May 2019 Available online 29 May 2019 0961-9534/ © 2019 Elsevier Ltd. All rights reserved.

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originating from the phytostabilisation of a TEs contaminated soil for compost, biogas or thermal energy production. With this aim, the influence of the presence of TEs and the nature of the organic matter on the biodegradability of the biomass under aerobic and anaerobic conditions, as well as on the potential thermal use of the biomass, was determined. Composting and anaerobic digestion are microbiallymediated biological decomposition processes, in which different microorganisms are involved, and therefore the study of both processes will allow the identification of the influence of TEs on the activity of the different microbial populations. Also, both processes are considered recovery operations for the recycling of organic wastes/byproducts into valuable products (compost and biogas).

production of several maize cultivars can account for about 13 t dm ha−1 (6 t dm ha−1 without considering seeds) under low fertilisation conditions [4]. The issue of pollution transfer and the presence of TEs in the plants is a major challenge regarding the use of their biomass for bioenergy [6,7,10]. However, the transfer of TEs to the aerial parts is limited in excluder species used for phytostabilisation, and then the plant biomass obtained has low TEs concentrations, which makes the recycling of this biomass possible, with low environmental concern. Domínguez et al. [3] studied the calorific value of some native Mediterranean species used for revegetation of TEs contaminated soils and concluded that Silybum marianum and Dittrichia viscosa are promising species as bioenergy crops. The same plant species were tested for decomposition by pyrolysis [11] showing equally promising results. Meers et al. [4] developed a field phytoattenuation experiment in a soil contaminated with TEs using several cultivars of maize as energy crops, in which the energy production was estimated in terms of biogas production through anaerobic digestion and annual productions per hectare of electricity (15,000–21,000 kW h) and thermal energy (18,000–25,000 kW h) calculated. However, the presence of certain TEs in the plant biomass, even at low concentrations, may affect the biological degradation processes of the plant biomass. The presence of different TEs in the input material for anaerobic digestion can affect positively (stimulating) or negatively (inhibiting) the process, depending on the element (if essential or not) and its concentration and chemical speciation [12,13]. Most research concerning the effect of TEs (or heavy metals) on anaerobic digestion has focused on sewage sludge [14,15] and pig slurry [16]. Aerobic degradation is another option for the recycling of plant biomass through the production of compost. The high C/N ratio and the physico-chemical properties of plant materials make them adequate for the composting with N-rich wastes (such as animal manures or sewage sludge), to adjust the C/N ratio and improve aeration and therefore aerobic decomposition [17,18]. However, heavy metals can affect microbe reproduction and further affect the biodegradation of organic wastes [19], although the microorganisms responsible for the aerobic transformation of these materials during composting have generally high tolerance to TEs [20,21]. Therefore, the presence of TEs in certain wastes (mainly municipal solid wastes, sewage sludge or animal manures) may not delay or inhibit the composting process but can lead to low-quality composts with high TEs contents and restricted use in agriculture [18]. Thermal analysis and differential scanning calorimetry (DSC) have been demonstrated to be useful techniques for the evaluation of the thermal characteristics of different organic materials, either for establishing their most-suitable/profitable degradation process or for the estimation of the benefits deriving from their use as a source of energy [22–24]. Thermogravimetric analysis (TGA) and derivative thermogravimetric (DTG) curves are useful tools for the evaluation of the behaviour of a material when it is submitted to temperature changes under a certain atmosphere (combustion or pyrolysis) [11]. In the present research, it is hypothesised that the remediation of TEs-contaminated soils through phytostabilisation can be enhanced by adding value to the biomass produced through composting, biogas generation or combustion as an alternative to biomass/energy crops, and that the moderate concentrations of TEs in their aerial parts will not limit their biological (aerobic and anaerobic) or thermal transformation. Although the potential for methane production of different (energy) crops has been extensively evaluated [25,26], mainly regarding their content of lignin, cellulose and secondary metabolites, the potential of native species used in the remediation of TEs-contaminated sites needs to be further studied and compared with those of energy crops. The objective of this study was therefore to evaluate the potential use of plant biomass (from two native species from mine-affected sites, a woody plant and an agricultural crop considered as a bioenergy crop)

2. Material and methods 2.1. Experimental procedure A pot experiment was carried out under glasshouse conditions using a soil from the margin of the Portmán gully, within the Sierra Minera of La Unión-Cartagena, which connects directly with old run-off channels and mine-spoil accumulation ponds [27]. The soil was completely bare of vegetation and had a sandy texture, an acid pH (4.2), low levels of organic matter (OM; 0.5%), total organic carbon (2.7 g kg−1) and total N (1.0 g kg−1) and high concentrations of TEs (Cu 230, Pb 19129, Zn 2257 and As 1976, μg g−1) and Fe (215 mg g−1). The soil was treated with an organic amendment (the solid fraction of pig slurry (SF), at 67 g fresh SF kg−1 soil), to provide nutrients and OM, and with two different inorganic amendments (paper mill sludge (PS) from paper mill wastewater treatment, 4.1 g kg−1; pH 8.87, electrical conductivity (EC) 4.40 dS m−1, acid-neutralising capacity 36.7% of CaO, provided by Holmen Paper, Madrid, Spain; and a commercial ‘red mud’ (alumina refinery residue) derivative (RM), 2.2 g kg−1; pH 10.9, EC 0.14 dS m−1, acid-neutralising capacity 68.8% of CaO, provided by Sinergias S.L., Cartagena (Murcia), Spain) to increase soil pH to 5.5 and allow plant growth [28]. Control pots with unamended soil were also run. Seeds of Silybum marianum (L.) Gaertner, Piptatherum miliaceum (L.) Coss and Nicotiana glauca R.C. Graham, collected from the contaminated area, and seeds of Helianthus annuus L., acquired commercially (RAGT Ibérica, Palencia, Spain), were sown in the pots (4.5-L pots with four replicates per species and treatment for S. marianum and P. miliaceum; and 1.5-L pots, in duplicate, for N. glauca and H. annuus) and cultivated for 102 days. The plants were harvested at flowering stage (before seed production), weighed, washed, dried at 60 °C for 48 h, weighed (dry) and ground to a fine powder for analysis (Table 1) and for the different determinations. For N. glauca and H. annuus, leaves were separated from stems and both were studied individually for thermal analysis, while the whole aerial parts of the other plant species were studied since the leaves grow from a crown at ground level. None of these plants were able to grow in the control treatment without any amendment; therefore, the studies were only performed for the plant biomass obtained from the amended soils (2 replicated pots per treatment). 2.2. Aerobic degradation The aerobic biodegradability of the plants was assayed by a respiration test, determining the CO2 emitted during aerobic incubation. Briefly, 5 g of plant dry matter (DM) were incubated in hermetic 500mL glass vessels, the moisture content was adjusted to 70% with deionised water and the CO2 produced was trapped in a NaOH solution contained in small vials placed inside the hermetic vessels. Empty vessels were used as blanks. The different samples and the blank were replicated three times. The experiment was carried out in the dark under controlled conditions, in an incubator at 26 °C. In order to avoid anaerobic conditions and allow the air exchange, the vessels were opened and the small vials changed, after 1, 3, 5, 7, 10 and 14 days and 221

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Table 1 Concentration of trace elements (μg g−1 DM) and C/N ratio in the plants grown in TEs contaminated soil amended with the solid fraction of pig slurry in combination with either a commercial ‘red mud’ derivative (RM) or paper mill sludge (PS) (mean ± se; n = 4). Treatment

As

Cd

Cr

Cu

Pb

Zna

Mn

1.28cd 2.13cd

7.3 ± 1.20 ab 8.4 ± 2.45a

0.05 ± 0.10d 0.03 ± 0.02d

63.6 ± 9.5 ab 25.1 ± 4.4b

20.0 ± 1.0b 19.0 ± 1.2b

91 ± 3.0bc 114 ± 24.5bc

124 ± 2.5cd 99 ± 0.1d

211 ± 8.0d 168 ± 10.0cd

0.52cd 1.37d

2.5 ± 0.60abc 3.2 ± 0.90abc

1.95 ± 0.15a 2.50 ± 0.50a

73.5 ± 8.5 ab 123.0 ± 40a

21.3 ± 0.8b 27.8 ± 0.6a

118 ± 18.5bc 183 ± 10.5 ab

293 ± 17.0b 407 ± 12.5a

639 ± 4.0a 577 ± 6.5b

4.17 ab 0.14bc

0.6 ± 0.52c 1.2 ± 0.15bc

0.45 ± 0.05cd 0.59 ± 0.05bcd

12.4 ± 0.91b 24.7 ± 5.20b

6.3 ± 0.4d 7.9 ± 1.5d

87 ± 10.0c 161 ± 5.5abc

100 ± 7.0d 145 ± 6.9c

229 ± 22.5c 239 ± 8.0c

1.93b 9.67a

2.6 ± 1.76abc 1.6 ± 0.37bc

1.50 ± 0.06abc 1.59 ± 0.36 ab

21.8 ± 2.48b 18.1 ± 1.87b

10.0 ± 1.1c 10.1 ± 0.9c

225 ± 6.5a 231 ± 26a

137 ± 9.5c 137 ± 3.0c

72.5 ± 12.0e 78.0 ± 5.0e

n.s. *** n.s.

n.s. *** n.s.

n.s. *** *

** *** **

** *** n.s.

n.s. *** **

** *** **

C/N

Piptatherum miliaceum RM 18.2 ± PS 15.3 ± Silybum marianum RM 13.8 ± PS 11.1 ± Helianthus annuus RM 32.0 ± PS 22.7 ± Nicotiana glauca RM 30.2 ± PS 40.8 ± ANOVA Treatment ** Plant *** TxP ***

a Log transformed data for statistical analysis. *, **, ***: P < 0.05, 0.01 and 0.001, respectively; n.s.: not significant (P > 0.05). Values followed by the same letter for each parameter were not significantly different according to Tukey's test at P < 0.05.

which a sudden decrease in weight loss is registered in the DTG curve) were determined. The Tp is considered to be a measurement of combustibility, whereas the value of the maximum rate of weight loss represents the reactivity of the biomass. The Ti is calculated as the intersection between the tangent line at the point where the thermal degradation is initiated and the tangent line at the maximum weight loss rate [31].

then weekly until 35 days. The amount of CO2 produced was quantified by titrating the unreacted NaOH with HCl, after precipitation of the carbonates with an excess of saturated BaCl2 solution [29]. The results were expressed as cumulative CO2–C (mg CO2–C g−1 dry weight). 2.3. Anaerobic degradation The anaerobic degradation test was performed in an ANKOMRF Gas Production System of 310-mL-capacity vessels, which automatically recorded pressure changes. The pressure increase provoked by the gas generated in the absence of oxygen was used to calculate the volume of biogas produced [30]. The anaerobic inoculum was obtained from a wastewater treatment plant under mesophilic conditions (urban wastewater, with a reactor capacity of 7612 m3 and a hydraulic retention time of 29.7 days), pre-incubated at 35 °C for 24 h. The characteristics of the inoculum were (mean ± sd): pH 7.37 ± 0.03, EC 14.78 ± 3.58 dS m−1, total solids (TS) 21.67 ± 4.13 g L−1 and volatile solids (VS) 14.02 ± 2.12 g L−1 (the full characterisation is included as supplementary information). Plant samples (0.5 g) were mixed with 150 mL of pre-incubated inoculum in each vessel (VS ratio 1:4.5 substrate:inoculum) and the mixtures were incubated under anaerobic conditions at 35 °C in an incubator for 9 days, with continuous agitation; a control without plant material and a positive control with cellulose were run simultaneously. The proportion substrate:inoculum was fixed in a preliminary experiment, using different weights of plant material, from 0.25 to 2 g, in 150 ml of inoculum. The head space of the vessels was flushed with a N2/CO2 (80/20 vol) mixture before running the system, to ensure anaerobic conditions. The results were expressed as volume of biogas per unit of plant dry weight.

2.5. Analytical methods The inoculum was analysed for pH and EC directly in the fresh sample, TS by drying at 105 °C and VS by ashing at 550 °C. The plant material was analysed for TE concentrations by inductively coupled plasma-optical emission spectroscopy (ICP-OES; ICAP 6500 DUO + ONE FAST, Thermo Scientific) after microwave (ETHOS1, Milestone) assisted digestion with H2O2 and HNO3 (1:4 v/v). The analytical accuracy was checked with a certified reference material (NCS DC 73349). The lignin concentration was determined by the American National Standard method [32]. The elemental analysis for N, C, S and H was carried out using a LECO CHNS-932 analyser. All the analyses were performed in duplicate. The high heating values (HHV; MJ kg−1) of the plant biomass were calculated using the correlation proposed by Sheng and Azevedo [33], with the composition obtained from the elemental analysis: HHV = −1.3675 + 0.3137 × %C + 0.7009 × %H + 0.0318 × %O (Eq. 1)

2.6. Data evaluation and statistical analysis Both CO2–C produced from the aerobic biodegradation test and biogas production from the anaerobic incubation fitted a first-order kinetic model [29,34]: For the aerobic biodegradation

2.4. Thermal analysis The TGA and DSC were performed in an oxidising atmosphere, on plant samples from the pots with amended soil; for N. glauca and H. annuus, leaves and stems were analysed separately. Thermogravimetric analysis was performed using TA Instruments (model Q600, TA Instruments, New Castle, DE, USA) equipment. Aliquots of 5 mg of sample were used in each analysis. The analyses were carried out with an air flow of 100 mL min−1, at a heating rate of 10 °C min−1 from room temperature to 750 °C. Derivative curves of mass loss (DTG) and differential scanning calorimetry (DSC, heat flow) were represented as a function of temperature. For the evaluation of the thermal characteristics, the peak temperature (Tp, the temperature at the maximum rate of weight loss) and the ignition temperature (Ti, the temperature at

Cm = C0 × (1-e-k×t);

(Eq. 2)

For the anaerobic incubation: Bm = B0 × (1-e-kd×t);

(Eq. 3)

where Cm and Bm are the production of CO2–C (mineralised-C; mg g−1) and biogas (mL g−1) at time t, respectively, C0 and B0 indicate the potentially-mineralisable-C under aerobic conditions (mg g−1) and the ultimate biogas production potential under anaerobic conditions (mL 222

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g−1), respectively, k is the aerobic degradation rate constant and kd the anaerobic degradation rate constant. The experimental results were fitted to the model by the non-linear least-square technique (Marquardt-Levenberg algorithm), using the SigmaPlot v. 11.0 computer programme (SPSS Inc.). The statistical significance of the curvefitting, residual mean square (RMS) and F value of the ANOVA were also calculated. The effect of the treatments and plant species on the plant composition and on the values of the parameters measured following aerobic and anaerobic degradation was determined by a two-way ANOVA (using soil treatment and plant species as independent factors). Differences between means were determined using Tukey's test. Before the statistical analysis, the data were tested for normality using the Kolmogorov–Smirnov test; when necessary, they were log-transformed to accomplish normality before the ANOVA and Tukey's test. Pearson's correlation coefficients between the degradation parameters and the TE concentrations in the plants were also determined (IBM SPSS Statistics 22.0 software).

(Table 3), without significant differences among the other plant samples or between the soil treatments. However, the rate constant did not differ significantly among the four different plant species or the soil treatments. The differences found in the aerobic degradation of different plant species can be expected to be a consequence of the differing composition of the plants, mainly regarding their content of lignin, the fraction most resistant to microbial degradation. However, the concentration of lignin was low in S. marianum (Table 2); therefore, the aerobic degradation for this species was lower than expected. Considering the results obtained for the four species studied, significant positive correlations between the concentration of lignin and Cm (P < 0.01) or C0 (P < 0.05) were found (Table 4). But significant negative correlations occurred between Cm and C0 and the concentrations of Cd, Mn and Zn in the plants (Table 4). This indicates that the presence of these elements in the plants affected negatively the aerobic degradation of the plant material. In agreement with this, the highest concentrations of Mn and Zn were found in S. marianum, which also showed the lowest Cm and C0 values. A different situation occurred in the anaerobic degradation (Fig. 2; Table 3), the biogas production being the lowest for N. glauca, especially in treatment RM, with less than half the production of P. miliaceum, although without significant differences among the rest of the plant species or between soil treatments. The biogas production potential (B0) for individual species fitted a first-order kinetic model at a highly-significant level (P < 0.001; Table 3), and only the results of S. marianum deviated from the model during the initial stage of the digestion (i.e., during the first 24 h of the experiment; Fig. 2). The highest B0 values (nearly 350 mL g−1) were obtained for P. miliaceum plants from PS treatment. However, the highest rate constant was found for N. glauca, indicating that the maximum biogas production is reached earlier than for the other plant species independently of the total amount of biogas produced at the end of the incubation. Significant negative correlations were found between the concentrations of Pb in the plants and Bm and B0 (Table 4), which indicates that a toxic effect of Pb on the microbial processes was influencing the biogas production. Contrastingly, significant and positive correlations were found between Bm and B0 and the As and N concentrations, as well as with the C/N ratio of the plants (Table 4). Expressing the biogas production potential (B0) per unit of VS, the values decreased in the order (mL g−1 VS): P. miliaceum (311–399) > S. marianum (269–295) > H. annuus (212–235) > N. glauca (141–154).

3. Results 3.1. Plant composition The highest concentrations of Cd, Cr, Mn and Zn occurred in S. marianum, while N. glauca showed the greatest Pb concentrations and P. miliaceum those of As (Table 1). The concentration of lignin was lowest in S. marianum, followed by H. annuus and N. glauca (leaves), and was highest in P. miliaceum (Table 2). All plants had high VS and the main difference in the elemental composition of the plants occurred for the nitrogen concentration, with the lowest values in the stems of N. glauca and H. annuus. 3.2. Aerobic and anaerobic biodegradation After 35 days of aerobic degradation, the lowest mineralised-C (Cm) values were found for S. marianum (Fig. 1; Table 3), while no significant differences were found between plants of the same species from different treatments. The biodegradation profile in the S. marianum samples differed with respect to those of the other plants, showing a 4-day latency period with scarce degradation (Fig. 1). When expressed as a percentage of the TOC of the plant material, S. marianum also showed the lowest values (average values 25.7 and 29.3% of TOC in treatments RM and PS, respectively), while the rest of the plant species had similar values: P. miliaceum 34.0 and 40.1%, H. annuus 32.9 and 36.2% and N. glauca 34.8 and 38.8%, in treatments RM and PS, respectively (average values). All data of the biodegradation test fitted a first-order kinetic model at a high significance level (P < 0.001 for all curves), according to the RMS and F values of the ANOVA (data not shown). The values of potentially-mineralisable-C (C0) were again lowest for S. marianum

3.3. Thermogravimetry The concentration of VS, elemental composition and HHV of the plants did not differ between soil treatments, so Table 2 shows the average results for each plant species. The lowest concentration of VS was obtained for S. marianum, and similar values were found for the leaves of N. glauca (Table 2). However, for thermal use, the high value

Table 2 Lignin and volatile solids (VS) concentration, elemental composition and higher heating values of the plants (mean ± se; n = 2) grown in TEs contaminated soil amended with the solid fraction of pig slurry in combination with either a commercial ‘red mud’ derivative (RM) or paper mill sludge (PS). The results shown are the mean values of the plants from both soil treatments (RM and PS) as no significant differences were found between them (P > 0.05). Plants

Lignin (%)

VS (%)

C (%)

N (%)

S (%)

H (%)

HHV (MJ kg−1)

P. miliaceum S. marianum H. annuus Leaves Stems N. glauca Leaves Stems ANOVA

26.7 ± 0.95a 9.4 ± 0.21c

87.2 ± 0.10b 77.7 ± 0.40d

39.55 ± 0.067 ab 34.27 ± 0.081c

2.17 ± 0.106b 2.25 ± 0.051b

0.44 ± 0.002a 0.27 ± 0.070b

5.77 ± 0.100b 5.03 ± 0.019c

16.73 ± 0.07a 14.76 ± 0.35b

13.1 ± 0.70b 14.4 ± 0.72b

83.3 ± 1.18c 82.2 ± 0.64c

38.95 ± 0.125b 41.07 ± 0.015a

3.24 ± 0.034a 0.31 ± 0.005d

0.28 ± 0.018b 0.17 ± 0.011c

5.76 ± 0.025b 6.02 ± 0.018 ab

16.53 ± 0.02a 17.40 ± 0.01a

12.4 ± 1.30b 16.9 ± 0.34 ab ***

78.1 ± 0.50d 93.9 ± 0.65a ***

39.52 ± 0.016 ab 41.15 ± 0.020a ***

2.17 ± 0.027b 0.82 ± 0.017c ***

0.22 ± 0.015bc 0.13 ± 0.002c **

5.92 ± 0.065 ab 6.09 ± 0.077a ***

16.84 ± 0.01a 17.45 ± 0.07a ***

**, ***: P < 0.01 and 0.001, respectively. Values followed by the same letter for each parameter are not statistically different according to Tukey's test at P < 0.05. 223

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Fig. 1. Cumulative CO2–C production from the plants during the aerobic degradation process. The plants were grown in a TEs contaminated soil amended with the solid fraction of pig slurry in combination with either a commercial ‘red mud’ derivative (RM) or paper mill sludge (PS). The symbols are the experimental data (n = 3, ± se) and the lines the degradation predicted by a first-order kinetic model for each sample. The numbers in the legend indicate the soil treatment replicate.

of VS in the stems of the latter would mean an increase in the VS content of the plant as a whole, thus resulting in a similar VS content for N. glauca plants to that of P. miliaceum and H. annuus. All the samples had similar HHV (Table 2), except for S. marianum, which showed the lowest value, in agreement with its higher ash (lowest VS) content. The thermal degradation characteristics of the different biomasses were evaluated in terms of their reactivity in an oxidising atmosphere. Two main devolatilisation and combustion stages of the materials were found (Table 5); the peak temperature for these two temperature ranges and the percentage mass change of the samples were calculated. These parameters indicate that the main transformation of biomass took place at low temperatures (150–350 °C), when the highest values of mass change were obtained. The lowest values were found for S. marianum, but all the samples had similar values of peak temperature for this first range. Likewise, all the samples showed similar values for the maximum rate of weight loss (% mass change). Regarding the second temperature range, the peak temperature showed more variability among the different samples analysed, the lowest value being obtained for the stems of H. annuus with the PS

Table 4 Pearson's correlation coefficients between the concentrations of trace elements, total N, and lignin and the C/N ratio of the plants and the parameters of the aerobic and anaerobic degradation processes (n = 16).

As Cd Cr Cu Pb Zn Mn Lignin N C/N

Cm

C0

k

Bm

B0

kb

0.339 −0.636** −0.654** −0.447 0.031 −0.773*** −0.833*** 0.678** −0.384 0.381

0.364 −0.680** −0.619* −0.419 −0.045 −0.755*** −0.785*** 0.647** −0.317 0.331

−0.093 0.498 0.326 0.359 0.178 0.419 0.415 −0.148 0.178 −0.181

0.672** −0.458 0.219 0.454 −0.726** 0.026 0.282 0.425 0.630** −0.672**

0.679** −0.449 0.181 0.467 −0.653** 0.013 0.253 0.431 0.636** −0.651**

−0.424 0.257 −0.355 −0.526* 0.573* −0.218 −0.478 −0.177 −0.676** 0.726**

*, **, ***: P < 0.05, 0.01 and 0.001, respectively.

Table 3 Results of the aerobic and anaerobic degradation of the plants from different soil treatments and the parameters of the first-order kinetic model (mean ± se; n = 2). The plants were grown in a TEs contaminated soil amended with the solid fraction of pig slurry in combination with either a commercial ‘red mud’ derivative (RM) or paper mill sludge (PS). Cm: aerobic C mineralised at 35 days; C0: potentially-mineralisable C; k: rate constant of the aerobic process; Bm: experimental results of biogas production; B0: biogas production potential; and kb: rate constant of the anaerobic process. All fitted models were significant at P < 0.001 (n = 2). Plants

Treat.

Cm (mg g−1 DM)

C0 (mg g−1 DM)

k (d−1)

P. miliaceum

RM PS RM PS RM PS RM PS T P TxP

139.8 ± 2.38a 165.1 ± 5.48a 94.0 ± 5.88b 105.6 ± 0.94b 133.1 ± 11.55a 140.8 ± 15.12a 143.9 ± 0.10a 145.6 ± 13.10a n.s. ** n.s.

147.8 ± 1.91 ab 188.7 ± 12.28a 93.8 ± 3.02b 112.6 ± 8.39b 149.3 ± 8.62a 154.2 ± 16.47a 149.3 ± 0.33a 155.4 ± 17.63a * ** n.s.

0.097 0.068 0.125 0.094 0.066 0.072 0.093 0.099 n.s. n.s. n.s.

S. marianum H. annuus N. glauca ANOVA

± ± ± ± ± ± ± ±

0.0057 0.0074 0.0244 0.0224 0.0060 0.0009 0.0039 0.0207

Bm (mL g−1 DM)

B0 (mL g−1 DM)

kb (h−1)

235 270 202 219 218 198 141 129 n.s. *** n.s.

271 348 210 228 221 196 134 146 n.s. *** *

0.015 0.011 0.022 0.022 0.024 0.026 0.035 0.032 n.s. ** n.s.

± ± ± ± ± ± ± ±

42.2a 31.3a 5.5a 2.9a 7.9a 15.6a 8.98b 23.0b

± ± ± ± ± ± ± ±

56.5b 24.8a 1.11bc 2.20b 13.0b 19.1bcd 8.77d 5.65cd

± ± ± ± ± ± ± ±

0.006b 0.001b 0.001b 0.001b 0.005b 0.003b 0.001a 0.008a

*, **, ***: P < 0.05, 0.01 and 0.001, respectively; n.s.: not significant P > 0.05. Values followed by the same letter for each parameter are not statistically different according to Tukey's test at P < 0.05. 224

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Fig. 2. Biogas production from the plants under anaerobic degradation conditions. The plants were grown in a TEs contaminated soil amended with the solid fraction of pig slurry in combination with either a commercial ‘red mud’ derivative (RM) or paper mill sludge (PS). The symbols are the experimental data and the lines the degradation predicted by a first-order kinetic model for each sample. The numbers in the legend indicate the soil treatment replicate.

miliaceum samples are shown in Fig. 3. The DTG profiles are characterised by three main peaks (Fig. 3 a,c): the release of water contained in the sample took place around 100 °C, while the other two peaks were related to the thermal decomposition of its organic content (mass loss; Table 5). The devolatilisation and further ignition of

treatment (Table 5). Although the oxidation of the material in this second region was lower than that in the first (lower mass loss), the greatest energy release occurred in this temperature zone, the leaves of H. annuus showing the highest peak values of heat flow. The thermal analyses performed for the S. marianum and P.

Table 5 TGA (Tp, Mass change), DTG (Ti) and DSC (Maximum heat flow) characteristics for the combustion process of the plant biomass from different soil treatments. The plants were grown in a TEs contaminated soil amended with the solid fraction of pig slurry in combination with either a commercial ‘red mud’ derivative (RM) or paper mill sludge (PS). Plants/treatments

P. miliaceum PS RM S. marianum PS RM H. annuus leaves PS RM H. annuus stems PS RM N. glauca leaves PS RM N. glauca stems PS RM

Maximum heat flow (W g−1)

Residue at 750 °C (%)

Ti (⁰C)

25.2 24.4

17.7 14.2

10.1 11.1

238.7 235.8

440.0 459.0

27.4 28.5

23.9 17.2

19.2 17.5

230.4 232.3

48.0 54.2

451.6 455.3

22.8 23.5

29.8 34.2

16.7 10.8

221.8 215.5

284.3 294.7

64.7 66.7

419.3 439.5

21.0 19.7

29.7 19.6

5.3 3.5

232.1 226.6

282.0 289.5

48.6 49.2

455.5 455.8

25.7 26.6

17.5 20.8

12.2 12.2

226.8 233.0

276.8 278.5

58.8 61.0

431.1 436.6

26.6 24.8

22.9 23.5

5.1 5.3

223.5 224.3

First peak (150–350 °C)

Second peak (350–520 °C)

Tp (⁰C)

Mass change (%)

Tp (⁰C)

Mass change (%)

287.6 292.8

57.4 58.1

470.2 466.6

281.8 283.2

42.6 43.0

276.7 289.0

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Fig. 3. Results of DTG analysis and heat flow (DSC) for S. marianum (a, b) and P. miliaceum (c, d). The plants were grown in a TEs contaminated soil amended with the solid fraction of pig slurry in combination with either a commercial ‘red mud’ derivative (RM) or paper mill sludge (PS).

4. Discussion

cellulose-type materials took place in the temperature range of 250–350 °C. The species S. marianum had a maximum mass loss rate (dw/dt) of 0.07% s−1 at 294 °C, while this value was much higher for P. miliaceum (0.11% s−1) at 287 °C. The overlapping with the third peak was associated with pyrolysis reactions, leading to char formation and posterior combustion [35], as lignin-type materials are reported to exhibit a characteristic mass loss at 400–500 °C [36]. The mineral residue remaining at the end of the analysis (750 °C; Table 5) was calculated from the TG curves. These values were the greatest for S. marianum, being almost twice that of P. miliaceum, with no significant differences between the soil treatments. However, the mineral residue differed significantly between the leaves and stems for both H. annuus and N. glauca. The degradation of OM is associated with a release of energy, which was clearly observed in the DSC curves (heat flow) for S. marianum and P. miliaceum (Fig. 3b,d), with the maximum occurring at about 450 °C for S. marianum and at ≈470 °C in the case of P. miliaceum. The thermal behaviour of the latter species did not differ significantly between the PS and RM treatments, while for S. marianum the mass loss, and therefore the energy release registered in the DTG and DSC curves for the high-temperature region, revealed lower values for the RM treatment. The thermal behaviour of H. annuus and N. glauca was quite different for leaves and stems (Fig. 4). The devolatilisation in the lowtemperature region was characterised by a shoulder in the DTG curves at around 200 °C (Fig. 4 a,c), which may be associated with lipid components and carbohydrates. This mass loss was not accompanied by a release of energy in the DSC (heat flow) curves (Fig. 4 b,d), which may be indicative of devolatilisation of the lipid fraction [31,37], while combustion of the remaining material took place at higher temperatures, with a peak mass loss at around 280 °C and a second mass loss associated with lignin-type materials in the range 400–500 °C. The shift registered for this peak in the DTG and DSC curves, when leaf and stem samples of H. annuus are compared, may be associated with their differing mineral and, especially, N concentrations (Table 2).

4.1. Aerobic biodegradation and thermogravimetric properties of the plants The aerobic biodegradability of the plants (aerobic respiration), measured as O2 consumption or CO2 production, has been used as an indicator of the degradability of a material, which indicates its feasibility for composting and, also, the stability and maturation index for compost [17,18,38,39]. The values for aerobic biodegradation found in the present experiment can be considered high, if compared with the results found for prunings of different shrubs/trees from public gardens (C-mineralisation 1–5% of TOC after 56 days) [40], due to their high lignin content (> 35%), in comparison with the plant species studied here (Table 2). The aerobic degradation results agree with the thermal behaviour of the samples. Silybum marianum presented a lower change in the mass loss signal (42.8%) than P. miliaceum (57.7%) in the temperature range of 150–350 °C (Table 5), where labile materials are oxidised. This indicates that the latter species would be more prone to degradation and explains the lowest biodegradation of S. marianum. The H. annuus and N. glauca samples exhibited similar thermal oxidation in the low-temperature range (150–350 °C), with the stem fraction undergoing higher mass loss in this range (65.7% for H. annuus and 59.9% for N. glauca), than for the leaves (51.1% and 48.9% for H. annuus and N. glauca, respectively). This fact agrees with the aerobic degradation of whole plants (stems + leaves), which showed similar potential biodegradability (C0 values) for P. miliaceum, H. annuus and N. glauca (Table 3). The fact that S. marianum had the lowest proportion of degradable-C and a 4-day latency period for microbial degradation may retard the temperature increase during composting and is indicative of the presence of toxic compounds readily available to the microorganisms. The elevated concentrations of Cd, Mn and Zn in S. marianum reduced its aerobic degradation, as shown by the significant negative correlations found among these parameters (Table 4), as well as by the fact that this species had the lowest Cm and C0 values and the greatest mineral content remaining at the end of the TG analysis (at 750 °C). However, the concentrations of Cr, Cu, Pb and Zn in the plant materials studied

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Fig. 4. Results of DTG analysis and heat flow (DSC) for leaves and stems of H. annuus (a, b) and N. glauca (c, d). The plants were grown in a TEs contaminated soil amended with the solid fraction of pig slurry in combination with either a commercial ‘red mud’ derivative (RM) or paper mill sludge (PS).

marianum, the anaerobic process did not show a lag-phase, unlike the aerobic degradation, and the amount of biogas produced was not significantly different from that of P. miliaceum or H. annuus. However, the significant correlations found between Bm and B0 and data from the plant analysis indicate that other factors different from lignin affected the anaerobic degradation, such as the N concentration of the plants (this had a positive correlation with Bm and B0, which showed in turn a negative correlation with the C/N ratio), indicating the relevance of protein-type compounds in anaerobic degradation for biogas production [45]. In fact, P. miliaceum showed the greatest biogas production potential, linked to its high N concentration and low C/N ratio. Gunasselan [34] proposed models for the prediction of methane yields from fruit and vegetable wastes, based on their chemical constituents, concluding that B0 can be predicted from total soluble carbohydrate, acid-detergent fibre (ADF), N and ash concentrations and lignin/ADF ratio. Labile compounds, which show high devolatilisation and thermal degradation in the low-temperature range of thermal analysis, are prone to biological transformation. Therefore, S. marianum, which underwent a high mass loss in the low-temperature range, was also characterised in the biogas curve by a steep slope during the initial days of the biological conversion, once the brief adaptation period had ended (Fig. 2). Piptatherum miliaceum, which showed a high mass loss in the same temperature range (150–350 °C), presented a higher biogas yield but a less-pronounced slope (the majority of its biogas had been produced after approximately 80 h), while in the case of S. marianum 80% of the total biogas had already been produced after 50 h. The lower slope value obtained for P. miliaceum during the 20–70 h period of the biogas test and the k value for the model (Table 3) are indicative of the limitations found for the hydrolysis stage due to the difficulties in degrading the lignocellulosic matrix [46]. A similar situation can be described for H. annuus and N. glauca, the former showing higher biogas

here cannot be expected to completely inhibit the aerobic degradation of the plant biomass, as they were lower than the maximum tolerance values reported by Heck et al. [20] for bacteria from compost, and also by Keeling and Cater [41] for free living diazotrops isolated from compost. The concentrations of Cd and Pb in N. glauca and S. marianum (and of Pb in H. annuus under the PS treatment) were above the limits allowed in composts, according to the End-Of-Waste criteria (Pb < 120 mg kg−1 and Cd < 1.5 mg kg−1) [42]. This is a serious limitation for the production of compost, as the concentration of TEs usually increases during composting due to the net loss of dry mass as CO2 during oxidation of OM [18], and implies the need to co-compost these plant biomasses with materials having low TEs concentrations.

4.2. Anaerobic degradation, thermal analysis and energy release of the plants The values of biogas production and biogas production potential obtained under anaerobic conditions were generally low for all the plant species tested in comparison with those reported for energy crops such as maize or other cereals (up to 50% of methane in the biogas), and also when compared to other herbaceous species such as nettle, ryegrass or clover [25,26]. In fact, only the values for P. miliaceum were close to those of cereal crops [25,26]. Different results have been previously reported for sunflower, due to differences in the oil concentration and the composition of the seeds among different varieties of sunflower [43] - up to 454 mL g−1 VS of biogas for the whole plant [43], and 107 mL g−1 VS (of CH4) for de-oiled cake [26]. The wide range of biogas production potential (or biochemical methane potential) of crops may be due to differences in their lignin content [34,44] and physiological status of the plants at harvest, the biogas (and methane) yield decreasing at late harvest times [25]. In the case of S. 227

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glauca, negatively affected the anaerobic degradation of the plant material, leading to the lowest biogas production for N. glauca. Although the total Pb concentration of the mixture with the inoculum did not reach toxic levels, the concentration in the solid particles of the plant material to be degraded could have limited the activity of the microorganisms involved in OM degradation under anaerobic conditions. No other elements showed significant correlations with the anaerobic digestion parameters. Only Zn concentration in S. marianum could pose a risk of toxicity for the anaerobic degradation of its biomass, but this species had the highest results of biogas production and just showed a small initial delay (Fig. 2). The HHV results obtained in the present experiment were close to those found by Domínguez et al. [3] for S. marianum, Carduus tenuiflorus and Scolymus maculatus grown in soils heavily or moderately contaminated by TEs, in a field experiment (15–16.8 MJ kg−1), but were lower than values reported for forest biomass (19–21 MJ kg−1) [50]. The thermal analysis of the different plants indicates that, in an oxidising atmosphere, although P. miliaceum and S. marianum had ignition temperatures similar to those of the other biomasses, these two species could be considered the best option for thermal use due to their high release of energy in the high-temperature range (350–520 °C). As Domínguez et al. [11] reported, the soil TEs did not have major effects on the TGA curves of the plant species. However, in the case of S. marianum, care should be taken regarding its high mineral content, which resulted in the high ash values obtained in the proximate analysis and, therefore, in lower HHV for this species. This high ash content may also represent a potential problem of fouling and slagging in combustion equipment. Piptatherum miliaceum showed a thermal behaviour similar to that of S. marianum, but was characterised by higher HHV and a lower ash content (Table 2), and the energy released in the hightemperature range was only slightly lower in P. miliaceum than in S. marianum (Fig. 3b,d). This species seems, therefore, to represent the best candidate for thermal use among the different plants evaluated. The comparison of the energy produced by combustion (according to HHV) and the energy produced by anaerobic digestion through biogas production (considering a minimum of 50% CH4 in the biogas and 39.8 MJ m−3 of CH4) revealed the most profitable procedure for each biomass (Fig. 5). The biomass of N. glauca showed clear advantages for energy production by combustion, while for P. miliaceum biogas production was found to be the most convenient option. The devolatilisation and combustion of labile materials started at a similar temperature (similar Ti values; Table 5) in all the samples, this being related to the amount of cellulose and hemicellulosic compounds. But the samples having an early loss of material (as occurred for the stems of N. glauca and H. annuus; Table 5) may present a high risk of auto-ignition during handling and storage when used as biomass for energy production. These two species were characterised by a mass loss that started at around 200 °C in the DTG profile (Fig. 4a,c), although their peak temperatures were similar to those of S. marianum and P. miliaceum, in the range of 150–350 °C (Table 5). The high release of energy in the high temperature range for S. marianum (Fig. 3a) could influence the design of combustion chambers based on the fact that, when burning solid fuels, a sequence of stages must be achieved: an initial drying of the material followed by volatilisation, pyrolysis, the subsequent combustion of volatiles previously generated and the final oxidation of char. When co-combustion of biomass is performed, separation between the temperature ranges at which these processes take place for the burning species may cause an extension of the volume needed, also causing the displacement of the main zone of heat release in the combustion chamber.

Fig. 5. Potential energy production by combustion (according to HHV) and by anaerobic digestion through biogas production of the different plant biomasses (mean ± se).

yields than the latter. The highest k values obtained for the degradation of N. glauca could be related to the early devolatilisation obtained in the DTG profiles (Fig. 4). In any case, fast degradation was observed for both species, which indicates the presence of readily-available organic compounds in their tissues. The different values obtained for k in the digestion tests of the different plant materials are indicative of the complexity of their OM [47], although in the present experiment other factors, such as the TEs content, may also account for the extension of the adaptation phase and the elevated degradation rate found. The main release of energy observed in the DSC curves was associated with the high-temperature region (Fig. 3b,d; 4b,d), where the lignin matrix of the samples oxidises. This high release of energy was found even for the samples presenting the greatest mass loss at lower temperatures (N. glauca and P. miliaceum). The oxidation of labile compounds has been associated in DSC curves with low energy releases due to the low energy needed for the devolatilisation and pyrolysis reactions that take place even in oxidising atmospheres [35]. Whereas, the high-temperature region is related to char combustion and the presence of lignin-type components, as previously stated. Therefore, the amount of energy released in this region serves as an indication of the amount of complex material present in the lignocellulosic matrix. The sample of S. marianum, which showed a great difference in the DSC curves for the two temperature regions (Fig. 3b), was the organic material with the poorest degradation under aerobic and anaerobic conditions, indicating the complexity of the organic compounds present in the biomass of this species. Heavy metals can either stimulate or inhibit the anaerobic process, according to their concentrations and chemical speciation. Some of these elements (Cr, Co, Cu, Mn, Mo, Ni, Se, W, Zn) are considered essential to the activity of enzymes involved in the anaerobic process [13,26,48]. But, at certain concentrations they become toxic or inhibitory [49], the lowest limits of reported negative effects on anaerobic digestion being (mg L−1): Cd 20, Cr 100, Cu 40, Ni 10, Pb 340 and Zn 150 [48]. Considering the plants with the highest heavy metal concentrations (S. marianum and N. glauca; Table 1), the maximum amount of each element provided by the plants in the anaerobic digestion (plant material mixed with inoculum) was (mg L−1): Cd 0.010, Cu 0.092, Pb 0.770 and Zn 1.356. Therefore, these plants provided significant amounts only of Pb and Zn, sufficient to increase the values in the mixture for anaerobic digestion (inoculum + plant) only to 1.22 and 20 mg L−1, respectively (see analysis of the inoculum in the supporting information, Table S1), which are well below the lowest limits for negative effects [48]. However, the significant correlations found between Pb concentration in the plant material and the biogas production parameters indicated that the accumulation of Pb, mainly by N.

5. Conclusions The results of potentially-mineralisable-C and biogas production potential indicated that the species P. miliaceum and H. annuus can be easily degraded by aerobic and anaerobic processes, being composting 228

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and biogas production suitable recycling options for their biomass. However, in the case of H. annuus, co-composting with materials low in TEs is encouraged to prevent excessive Pb concentrations (especially when PS is used as a soil amendment) and ensure compost quality. The aerobic biodegradability of N. glauca indicates its usefulness for composting, but its high concentrations of heavy metals (Cd and Pb) can also reduce the quality of the compost and therefore its commercialisation, and co-composting with materials low in TEs is again recommended. Also, the concentration of Pb in its biomass could limit the anaerobic digestion for biogas production. Both N. glauca and H. annuus underwent a relevant loss of mass during the early volatilisation stage and showed low ignition temperatures, which may provoke auto-ignition and limit their thermal use. The lag-phase during the aerobic degradation of S. marianum may retard the development of the composting process, but this species had high biogas production potential. The implication of the nature of the organic compounds in the delay of the aerobic degradation, the low potentially-mineralisable-C and the slow anaerobic digestion (low kd) may need further studies. Piptatherum miliaceum and S. marianum possessed appropriate characteristics for thermal energy production (like elevated mass change at high temperature and high ignition temperature) and the presence of TEs in the soil and plant tissues did not affect the potential thermal use of the species studied. However, the high mineral and ash contents of S. marianum may cause problems of fouling and slagging in combustion equipment, which should be taken into consideration for the practical application. So, the results found here open new perspectives for the implementation of phytostabilisation for TEs contaminated soils, with possible economic benefits from the use of the biomass for bio-energy production. Future work should involve long-term validation experiments for an economic evaluation of the technology and the cost savings provided by renewable energy production. Also, the provision of other valuable products, such as biochar from biomass pyrolysis, could be addressed in future studies. E-supplementary data of this work can be found in online version of the paper.

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Declarations of interest None' Acknowledgements The authors thank the Spanish Ministry of Economy and Competitiveness and EU FEDER Funds (ref.: CTM2013-48697-C2-1-R) and Fundación Séneca (Murcia Region, ref. 19460/PI/14) for financial support and Dr. D.J. Walker for the English revision of the manuscript. The stay of Ms. Chang in CEBAS-CSIC was supported by the AgriPlatform Intelligence Exchange (2015–2016) for Organic Wastes Resources Utilization and Greenhouse Gas Emission Reduction, Ministry of Sciences and Technology of China. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.biombioe.2019.05.017. References [1] P. Panagos, M. Van Liedekerke, Y. Yigini, L. Montanarella, Contaminated sites in Europe: review of the current situation based on data collected through a European Network, J. Environ. Public Health 2013 (2018) 11 158764 https://doi.org/10. 1155/2013/158764. [2] N. Rodríguez-Eugenio, M. McLaughlin, D. Pennock, Soil Pollution: a Hidden Reality, FAO, Rome, 2018, p. 142. [3] M.T. Domínguez, M.M. Montiel-Rozas, P. Madejón, M.J. Díaz, E. Madejón, The potential of native species as bioenergy crops on trace-element contaminated

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