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Please cite this article as: Saida Tayibi, Journal of Environmental Management, https://doi.org/10.1016/j.jenvman.2020.111632

0301-4797/© 2020 Elsevier Ltd. All rights reserved.

Research article

Coupling anaerobic digestion and pyrolysis processes for maximizing energy recovery and soil preservation according to the circular economy concept

Saida Tayibi a,b,c,d, Florian Monlau c,*, Frederic Marias e, Guillaume Cazaudehore c, Nour-Elhouda Fayoud a,b, Abdallah Oukarroum b, Youssef Zeroual f, Abdellatif Barakat a

a IATE, Montpellier University, INRAE, Agro Institut, 34060, Montpellier, France b Mohammed VI Polytechnic University (UM6P), Ben Guerir, Morocco c APESA, Pole Valorisation, Cap Ecologia, Lescar, France d LIMAT, Faculte des Sciences Ben M’Sik, Universite Hassan II de Casablanca, Morocco e Laboratoire de Thermique Energetique et Procedes – IPRA, EA1932, Universite de Pau et des Pays de l’Adour/E2S, UPPA, 64000, Pau, France f Situation Innovation, OCP Group, Complexe industriel Jorf Lasfar, El Jadida, Morocco

A R T I C L E I N F O

Keywords: Biochar Bio-oil Digestate Nutrient leaching test Plant growth Syngas

A B S T R A C T

After press separation of the liquid and solid digestate from an agricultural biogas plant, pyrolysis of solid anaerobic digestate was carried out (i.e., at 500 ◦C, 1h, and 10 ◦C/min) to produce biochar (37.6 wt%), bio-oil (33.7 wt%) and syngas (29.3 wt%). The organic phase of bio-oil and syngas exhibited high and low heating values of 28.4 MJ/kg and 12.9 MJ/Nm3, respectively. Then, the synergy of coupling biochar with liquid digestate for agronomic purposes was investigated by leaching experiment and growth plant tests on wheat. Leaching experiments using combination of liquid digestate (170 kg N/ha) and biochar demonstrated that biochar addi-tion increases the cumulative leaching of all nutrients, except nitrate, that have a significant decrease of 82% and 91%, respectively at 50 and 100 t/ha, compared to soil treated only with liquid digestate. The co-application of biochar with liquid digestate on growth wheat plant tests demonstrated that biochar application at 50 t/ha did not exhibit a negative impact on the relative seed germination and improved aerial dry biomass production (up to 27.5%) compared to soil with only liquid digestate addition.

1. Introduction

Anaerobic digestion (AD) is a robust process that has been in use for many decades for organic wastes treatment (municipal, agricultural and agro-industrial wastes) (Sawatdeenarunat et al., 2016; Surra et al., 2019). The AD process involves biological degradation, during which organic matter is transformed in anaerobic conditions into biogas (a mixture of CH4 and CO2) and an un-degraded residue (i.e., digestate) (Monlau et al., 2015a). At industrial scale, the digestate is generally separated into a liquid fraction (rich in nutrients, especially nitrogen and potassium) and a solid fraction rich in phosphorous and fibers generally separated by screw press, filter press, vibrating sieve or centrifugal systems (Monlau et al., 2015a). The solid digestate still contains a sig-nificant amount of organic matter, since fiber-recalcitrant (i.e., lignin, crystalline cellulose, etc.) is slowly or un-degraded by microorganisms

during the AD process (Santi et al., 2015). Over the last decade, the “cascading” biomass valorization approach,

where the output of one process becomes the input of the following one (thus, also targeting the ‘‘zero-waste” goal), has attracted attention (Gonzalez-Arias et al., 2019; Lam et al., 2018). Moreover, one original cascaded approach allowing to transform a large part of the organic matter present in wastes can be implemented by coupling AD and py-rolysis (Py) (Gonzalez-Arias et al., 2019; Pecchi and Baratieri, 2019; Song et al., 2017). Py is a thermochemical process that converts organic matter (including solid digestate from AD) into three main products: syngas (mainly CO2, H2 and CO), bio-oil (composed of an organic and aqueous phases) and biochar (Neumann et al., 2015). Despite to its low calorific value, the syngas still represents an additional source of energy that can be further converted into heat or heat/electricity alone or mixed with biogas in boilers and engines (Seyedi et al., 2019). In parallel, the organic phase of bio-oil can be combusted in a boiler, diesel engine, and

* Corresponding author. E-mail address: florian.monlau@apesa.fr (F. Monlau).

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https://doi.org/10.1016/j.jenvman.2020.111632 Received 10 April 2020; Received in revised form 30 July 2020; Accepted 11 October 2020

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combustion turbine for producing electricity or heat, or it could be upgraded to petroleum products or steam reformed for producing hydrogen fuel (Sarkar and Kumar, 2010; Zhang et al., 2007). In a recent study, it was clearly demonstrated that the integrated AD + Py approach led to a net 42% increase in electricity production compared to AD stand-alone and that the excess heat produce during the AD process was enough to supplement the drying energy requirement of the solid digestate prior to Py process (Monlau et al., 2015b). Furthermore, Righi et al. (2016) have demonstrated through a Life Cycle Assessment study that during the dual AD-Py concept, greenhouse gas emissions were strongly reduced without worsening the abiotic resources depletion.

In parallel, biochar produced from the Py process can be used for several applications, such as bioremediation, gas purification but also for agronomic issues (Lam et al., 2018; Nanda et al., 2016; Opatokun et al., 2017). Indeed, biochar addition in soil has demonstrated several physico-chemical benefits, such as improving water retention of soil, pH, cation exchange capacity and nutrients retention (Liu et al., 2012).

Recently, there has been increased research on the agronomic asso-ciation of biochar with different fertilizers (organic, minerals) (Dunsin et al., 2018). Nonetheless, few studies have investigated the agronomic potential of combining biochar and digestate from the AD process (Elbashier et al., 2018; Udall et al., 2017) and among them, few reports have extended the implementation to growth plant tests (Glaser et al., 2015; Kizito et al., 2019). For instance, Kizito et al. (2019) have eval-uated the addition of digestate-enriched biochar as soil amendment during maize growth in greenhouse. Their results demonstrated that the addition of digestate-enriched biochars improved soil quality and maize yield better results, as it provided higher soil organic matter (from 232% to 514%), macronutrient content (from 110% to 230%) and showed a significant increase of above ground biomass of maize compared to non-enriched biochar treatments (Kizito et al., 2019).

However, the use of biochar in combination with digestate does not always give positive results (Elbashier et al., 2018; Greenberg et al., 2019; Udall et al., 2017). For instance, Udall et al. (2017) have applied biochar (20 t/ha) combined with digestate (250 kg N/ha) for wheat production in real field experiments and no significant effect was noticed on above ground biomass (18.7 t/ha ) compared to digestate alone (19.2 t/ha) (Udall et al., 2017). Furthermore, most of these studies have focused on the association of whole digestate with biochar and further studies are needed in order to clarify the positive effect on the association of biochar produced from solid digestate Py with liquid digestate fraction richer in nutrients.

The present research evaluated the following objectives: (1) the Py yield products (biochar, bio-oil and syngas) produced from solid diges-tate (i.e., 500 ◦C, 1h, and 10 ◦C/min); (2) the characterization of syngas, bio-oil and biochar (evaluation of the content of inorganic elements contained in the biochar with the range suggested by the International

Biochar Initiative (IBI) and the European Biochar Certificate (EBC)); (3) the effect of co-applications of biochar (50 and 100 t/ha) and liquid fraction of digestate (170 kg N/ha) on soil gravimetric water retention, nutrient leaching in columns and growth plant tests on wheat seeds.

2. Methodology

2.1. Digestate origin and soil sampling

The whole digestate was obtained from an agricultural biogas plant located in the South of France (X: 43◦ 16’ 0.01′′ Y: 0◦ 43’ 0.01′′). The AD plant was fed with 26 t fresh matter/d containing 63% of cattle manure, 2% of duck slurry, 23% agro-industrial wastes and 12% agricultural by- products. The main operational conditions and parameters were an organic loading rate of 2.4 kg VS/m3 d, a hydraulic residence time of 26 days and temperature ranged between 40 and 45 ◦C. The performances of this agricultural biogas plant were estimated as biogas production on site of 1699 m3/d with a methane yield of 58% corresponding to a total energy of 9803 kWh/d (1 Nm3 CH4 = 9.8 kWh). Moreover, biogas was valorized into heat and electricity through a Cogeneration Heat and Power (CHP) system.

After sampling of the whole digestate, a liquid-solid separation of digestate was performed in laboratory using a wine press with a 500 μm mesh. The solid digestate was dried at 60 ◦C until it reached a constant weight and the liquid digestate (LD) was stored at − 17 ◦C until its use for agronomic trials. The main characterizations of LD were as follows: 0.50 ± 0.14 wt% of dry matter, 1.2 ± 0.3 wt% of volatile matter, 0.16 ± 0.04 wt% of TN, 0.37 ± 0.1 wt% of potassium (K2O), and 0.02 ± 0.01 wt% of phosphorus (P2O5).

Surface soil (0–25 cm) was collected from the southwest of France. The soil was air-dried and passed through a 2 mm sieve to remove large fragments. The main soil characteristics were as follows (per thousand): 219 of clays (<2 μm), 352 of fine silt (2–20 μm), 237 of coarse silt (20–50 μm), 113 of fine sand (50–200 μm) and 80 of coarse sands (200–2000 μm). The soil was classified as a clay loamy soil. Other characteristics were 6.4 of pH (water), 2.3 ± 0.2% of organic matter, C/ N ratio of 9.9, total nitrogen (TN) of 0.1 wt%, <30 g/kg of phosphorus (P2O5), and 7.1 ± 0.8 cmol (+)/kg cation exchange capacity (CEC).

2.2. The pyrolysis process

The dried solid digestate sample (about 300 g) has been subjected to the Py process in a steel reactor. Before Py, the basket of feedstock and the furnace were purged with N2 for 30 min to ensure an oxygen free environment. Then, the experiments were carried out in duplicate at 500 ◦C with a heating rate of 10 ◦C/min, for 1 h at high temperature. The collected Py products were biochar, bio-oil (condensable gas) and syn-gas (non-condensable gas). The furnace was then cooled to 25 ◦C under nitrogen flow and the biochar and bio-oil were collected and weighed. The syngas (hydrogen, oxygen, nitrogen, carbon monoxide and dioxide, methane, ethane, and ethylene) was quantified using a micro- chromatography device (Varian CP-4900, Agilent, Germany). The first column (CP-Sil CB) was operated at 37 ◦C to separate H2 and O2, while the second column (Molsieve 5 Å PLO) was operated at 37 ◦C to separate N2, CO and CH4 and the third column (HayeSep A) was operated at 35 ◦C to separate CO2, C2H2, C2H4, and C2H6. The detection of gaseous com-pounds was done by using a thermal conductivity detector. The injector and detector temperatures were 50 ◦C and 55 ◦C, respectively. The an-alyses of syngas were carried out every 5 min during Py reaction using the micro-GC. The mass of the produced syngas MSyngas (g) was deter-mined by the difference between the output and input gas flow during Py process by the use of an acquisition system linked to two flowmeters, measuring input (flowmeter BROOKS) and output (flowmeter M.M.T). equation (1) was used to calculate the mass of syngas as described below:

Abbreviations

AD Anaerobic Digestion B50 biochar application of 50 t/ha B100 biochar application of 100 t/ha ECB European Biochar Certificate FC Fixed Carbon GWR Gravimetric Water Retention H-NMR Proton Nuclear Magnetic Resonance HHV High Heating Value IBI International Biochar Initiative LHV Low Heating Value LD Liquid Digestate Py Pyrolysis VM Volatile Matter

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MSyngas(g)=∑

(output flow (g /min) − input flow (g /min))/

122 (1)

where 122 is the number of acquisitions per min. Biochar, bio-oil and syngas products yields percentages were calcu-

lated as follows:

Biochar (wt%) =MBiochar(g)/MSolid digestate (g) × 100 (2)

Bio − oil (wt%)=MBio− oil(g)/MSolid digestate(g) × 100 (3)

Syngas (wt%) =MSyngas(g)/MSolid digestate(g) × 100 (4)

where MBiochar, MBio-oil, MSyngas represent the produced biochar, bio-oil and syngas during Py and Msolid digestate represents the mass of solid digestate.

The losses during Py (around 6%) were considered as the bio-oil trapped in the walls of the cooling system and were assumed in the bio-oil calculation.

The bio-oil obtained in this work was separated into two different phases: an organic phase and an aqueous phase obtained by decantation using dichloromethane (99.8% from Sigma Aldrich®) as the organic solvent. The weight and yield were measured after decantation. The anhydrous Na2SO4 was added into the solvent mixture/organic phase to remove residual water. Then, the solvent was evaporated using a rotary evaporator, the organic phase of bio-oil was weighed, and its yield was measured.

The average low heating value (LHV) of syngas was calculated based on Eq. (5) (Lv et al., 2004), considering that N2 was separated from produced syngas. The predictive higher heating value (HHV) (MJ/kg) of organic phase of bio-oil was calculated using ultimate analysis in Eq. (6) (Troy et al., 2013) as follows:

2.3. Physico-chemical and biochemical analyses

Total solid (TS) and volatile matter (VM) contents in soil and liquid digestate (LD) were determined according to the protocol outlined by the American Public Health Association (APHA, 2005). Briefly, the TS was determined by drying the sample at 105 ◦C for 24 h, whereas vol-atile matter was determined by heating the dried sample at 500 ◦C under oxygen medium during 12 h. Thermogravimetric analyzer (TGA 2-LF, Mettler Toledo®, Switzerland) was used to illustrate the thermal degradation of solid digestate and the stability of its biochar, as well as to determine moisture, volatile matter, fixed carbon, and ash contents according to the protocol reported in Tayibi et al. (2020). Total Kjeldahl Nitrogen (TKN) of soil and LD was determined according to the Kjeldahl method (Kjeldahl, 1883), by using a mineralizator (BUCHI digestion unit K 438) and a BUCHI 370-K distillator/titrator. Moreover, N–NH4

+

content of the liquid digestate was determined by the titrimetric method after distillation using a BUCHI 370-K distillatory (Rodier, 1975). The fibers (cellulose, hemicelluloses) and the Klason lignin content of the dry solid digestate were determined using the NREL protocol (Sluiter et al., 2008). Briefly, the Klason lignin content was determined as the weight of the residues retained on the sintered glass crucible filter (Ø = 25 mm), and the soluble fractions were analyzed by high-pressure liquid chro-matography (HPLC) to quantify the monosaccharides content (i.e., glucose, xylose, and arabinose). The HPLC (Alliance® system, Waters,

USA) analysis was performed using a column (Aminex® HPX-87H, BioRad, France) at 40 ◦C and 0.3 mL/min of 0.005 M H2SO4. All the measurements were performed in triplicate. The cellulose and hemi-celluloses percentages were determined by equations (7) and (8), respectively.

Cellulose(%)= [(Glucose(g /L)×Vtot) /Mini] × 100 / 1.11 (7)

Hemicelluloses(%)=[(Xylose(g/L)+Arabinose(g/L)×Vtot)/Mini]×100/1.13(8)

where Vtot and Mini represent the total volume of the hydrolysis medium (0.025 L) and the initial mass of sample in grams, respectively, while 1.11 represents the conversion factor between glucose and cellulose and 1.13 represents the conversion factor between monomers (xylose and arabinose) and hemicelluloses (Barakat et al., 2015). The chemical composition of the organic phase of bio-oil was determined using gas chromatography-mass spectrometry (GC-MS, Thermo scientific ISQ single quadrupole). By comparing the recorded mass spectra of com-pounds with those given in the NIST2008 c2.0/Xcalibur data system library provided by the instrument software, compound identification was performed. Bio-oil were separated by silica capillary column, using helium as the carrier gas (1.2 mL/min). The injection volume was 1 μL using a 20:1 split ratio and an injector temperature of 260 ◦C. The GC temperature sequence was as follows: 70 ◦C start, hold 2 min, ramp at 10 ◦C/min to 300 ◦C and hold at 300 ◦C for 5 min. Moreover, 1H NMR (Proton Nuclear Magnetic Resonance) spectra of organic phase were recorded at 298K in deuterium chloroform (CDCl3, 98.9%) on a Bruker Avance III 600 MHz spectrometer equipped with helium cryoprobe operating at 600 MHz. 1H sequence was used with spectral width of 10000 Hz and 16 scans with a relaxation delay of 1.5s. Spectra were processed and visualized with Topspin 3.5 (Bruker Topspin, Germany).

Nutrients content (P, K, Mg, S, Ca and Na) and minor metallic con-tent (Pb, Cd, Cu, Ni, Hg, Zn, Cr and As) were determined by the Inductively Coupled Plasma Mass Spectrometry (ThermoFisher Scien-tific, XSeries 2 ICP-MS) equipped with a cooled spray chamber, a quadruple mass spectrometer and a collision cell. The ICP-MS settings were as follows: Nebulizer flow of 0.82 L/min, auxiliary flow of 0.80 L/ min, cool flow of 13 L/min, forward power 1400 Watts, cell gas flow He/ H of 0.0045 L/min. For this purpose, a microwave-assisted mineraliza-tion of the solid digestate and its biochar was performed after the addition of nitric acid (65%) and hydrogen peroxide (30%). The reaction was conducted for 30 min at room temperature, and then the mixtures were placed in the microwave reactor (Flexiwave, Milestone, USA) and heated for 20 min to reach 210 ◦C, which was maintained for 20 min and then cooled for 25 min. The obtained solutions were filtered using 0.2 μm filters then analyzed with ICP-MS. The ultimate analysis (C, H, N, O, and S) of dry solid digestate and its biochar were analyzed in duplicate using an elemental analyzer (varioMicro V4.0.2, Elementar®, Ger-many). The surface morphology of solid digestate and its biochar were investigated using a tabletop scanning electron microscope-SEM (5th generation-Phenom ProX, Phenom-World®, Netherlands) using a backscattered electron detector and the following parameters: acceler-ation voltage of 10 kV and imaging mode.

LHV(MJ

/Nm3)= [30× v / v% CO+ 25.7× v / v% H2 + 85.4 × v / v% CH4 + 151.3× v / v% (C2H4 +C2H6)

]× 0.42

](5)

HHV (MJ / kg)=[3.55×C2 − 232×C − 2230×H+ 51.2×(C×H)+ 131×N + 20, 600

] /1000 (6)

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2.4. Agronomic tests

Biochar application at 50 t/ha and 100 t/ha was chosen for per-forming the various agronomic trials (i.e., gravimetric water retention, nutrients leaching and growth plant tests). The choice of application at 50 t/ha was based on protocols outlined in previous studies (Glaser et al., 2015; Greenberg et al., 2019). In addition, application at 100 t/ha was chosen to assess the effect of excessive application of biochar on agronomic parameters (including water retention, relative seed germi-nation and leaching experience).

The effects of biochar application (50 t/ha and 100 t/ha) on the gravimetric water retention of soil (GWR) were determined using a modified protocol described in Tayibi et al. (2020). The soil was dried at 70 ◦C for 24 h. The different samples, including soil (S), soil + biochar (50 t/ha) (S + B50) and soil + biochar (100 t/ha) (S + B100), were placed into plastic tubes cut at the bottom and connected by a 50 μm mesh. Water was then added gradually, until the first drop of water appeared. The total volume (L/kg of soil) of water added represents the GWR of the different samples.

A leaching experiment was performed using a modified protocol described by Liu et al. (2017). The leaching columns were designed using a 50 mL plastic medical syringe (with the plunger removed) as described in Fig. 1. Briefly, a filter paper (glass microfiber filter GF/F, diameter 25 mm) was placed first in each syringe and then 15 g of quartz sand were added. Subsequently, 20 g of each soil sample with or without biochar/LD was introduced. Finally, 20 g of quartz sand was used to fill the syringe to prevent potential soil disturbance during leaching (Fig. 1). Subsequently, LD was applied at a rate of 170 kg N/ha of soil to approach the application of nitrogen at field scale and according to the EU Nitrate Directive (EU.C, 1991). Accordingly, four different treat-ments were tested: soil (S, as control), soil + liquid digestate (S + LD), soil + liquid digestate + biochar (50 t/ha) (S + LD + B50) and soil +liquid digestate + biochar (100 t/ha) (S + LD + B100), and each treatment was performed in two replicates. At the starting of the experiment, deionized water was added to the soil columns for each condition to obtain 60% of GWR; then, the columns were incubated at room temperature. After 48 h of incubation, 20 mL of deionized water

was added to the top of columns as the first leaching and the leachate volume was collected at the bottom of each syringe until it had totally leached out (approximately 7 h), and then, the leachate volume was recorded. The duration of the experiment was 30 days and the leaching processes were realized under this period. The leachate was filtered using 0.2 μm filters. The cations (NH4

+, K+, and Na+), anions (NO3− , PO4

3) and total mineral nitrogen (TMN) concentrations in the leachate were measured using an ion chromatography system (ICS-3000, Dionex, USA). This system, consisting of a dual pump module, eluent generator module, detector/chromatography module (single temperature zone configuration) and autosampler, was used to collect the data presented in this method. A 4-mm IonPac AS20 guard and analytical column set was used in the first dimension and a 2-mm IonPac AS16 guard and analytical column set was used in the second dimension. Both column sets were kept in a thermally controlled column compartment, which was operated at 30 ◦C.

The agronomic value of coupling biochar with LD was evaluated by determining the growth parameters (relative seed germination and aerial dry biomass) using wheat as the plant model. Plants trials with seeds of wheat were performed in small pots with a volume of 0.5 L, placed in a growth chamber (Fitotron, Weiss Gallenkamp, UK) according to the OECD 208 guidelines (2006) under controlled conditions. During the trial, the environmental conditions were as follows: 16 h of light at 25 ◦C, 8 h of darkness at 18 ◦C, with 60% relative humidity for the pe-riods of light and 80% during periods of darkness. Moreover, four con-ditions were tested in soil (S, as control); soil + liquid digestate (S + LD); soil + liquid digestate + biochar (50 t/ha) (S + LD + B50); soil + liquid digestate + biochar (100 t/ha) (S + LD + B100). The LD dose was the same as used in the previous experiment. The mixture of each condition was prepared at 70% of the water retention of soil. Ten seeds were planted in each pot, using four replicates for each condition. Each pot was manually watered every 48 h by adding water to reach the initial weight. After 70% germination on the control, five wheat seeds were kept for the growing period. After 21 days, the plants were harvested by cutting them at ground level and then dried in the oven at 70 ◦C for 24 h. For each condition, relative seed germination expressed in % according to equation (9) and the aerial dry biomass expressed in (g TS/100 plants)

Fig. 1. Experiment scheme of leaching columns for different conditions: Soil (S); soil + liquid digestate (S + LD); soil + liquid digestate + biochar (50 t/ha) (S + LD + B50); soil + liquid digestate + biochar (100 t/ha) (S + LD + B100).

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was determined according to equation (10). Generally, a relative seed germination above 70% indicates low phytotoxicity.

Aerial dry biomass (g TS / 100 plants)=(

Mdry (70◦C)/

5)× 100 (10)

where Mdry (70◦C) represents the mean of the aerial dry biomass (g TS) for each condition and 5 is the number of plants in each pot at harvesting time.

3. Results & discussions

3.1. Pyrolysis of solid digestate

The main chemical properties of the solid digestate are listed in Table 1. Low hemicellulose content was detected in the digestate. In contrast, a relatively high lignin content and cellulose were observed in the solid digestate which was in agreement with previous studies that reported 16.1 wt% of lignin and 17 wt% of cellulose on solid anaerobic digestate (Monlau et al., 2016). In addition, Santi et al. (2015) have found higher contents of fibers from corn-silage solid digestate, as their values for cellulose, hemicelluloses and lignin were higher by 15.8 wt%, 19 wt% and 7.8 wt%, respectively, in comparison to our study. These

discrepancies could be explained by the feeding difference on the agri-cultural biogas plants investigated (Santi et al., 2015).

The experimental results regarding Py product yields distribution were as follows: 37.6 ± 1.8 wt% of biochar, 33.7 ± 1.9 wt% of bio-oil and 29.3 ± 2.5 wt% of syngas (data not shown). In comparison, Wei et al. (2018) reported a products distribution of 41.7 wt% for biochar, 23.5 wt% for bio-oil and 32 wt % for syngas after Py at 500 ◦C of digestate. The yield of biochar is in agreement with previous results demonstrated by Opatokun et al. (2017), which found 38 wt% in biochar produced from food waste digestate pyrolyzed at 500 ◦C. Finally, the results of our study differed slightly compared to results demonstrated by Monlau et al. (2015b), which determined 32.5 wt% after Py at 500 ◦C on a full-scale biogas digestate (mixture of chicken manure, groats, olive oil cake and triticale).

The syngas produced during Py was analyzed and its compounds distribution is presented in Fig. 2. According to our results, the LHV of syngas was 12.9 MJ/N m3, in contrast to 15.7 MJ/N m3 reported by Monlau et al. (2015b). Similarly, Cen et al. (2019) reported value of LHV of syngas of 11.3 MJ/N m3 after Py of rice straw at 550 ◦C. Neumann et al. (2015) reported a lower heating value of the syngas of 13.1 MJ/kg after Py at 750 ◦C of digestate from agricultural biogas plant. The syngas mainly consisted of CO2, CH4, CO and H2 with small amounts of C2H4, C2H6 and C2H2, which corresponds to the results reported by Opatokun et al. (2015). Similarly, Cen et al. (2019) reported that the gaseous

Relative Seed Germination (%)= (Mean of germinated seed / Initial number of seeds) × 100 (9)

Table 1 Physico-chemical properties of solid digestate and produced biochar compared to IBI (International Biochar Initiative) and EBC (European Biochar Certificate) recommendations.

Parameter (Units) Solid digestate Biochar IBI standards V2.0

EBC standards V4.8

Cellulose (wt%) 19.6 ± 1.1 – – – Hemicelluloses (wt%) 5.6 ± 0.7 – – – Lignin (wt%) 17.9 ± 0.7 – – – Proteins (wt%) 9.1 ± 1.9 – – – Ash (wt%) 5.9 ± 1.9 23.4 ± 8.3 Required Required C (wt%) 38.6 ± 0.1 45.3 ± 0.2 10 wt% Minimum

Class 1: ≥60 wt% Class 2: ≥30 wt% and ≤60 wt%. Class 3: ≥10 wt% and ≤30 wt%.

Biochar ≥50 wt% Bio Carbon Minerals (BMC) < 50 wt%

H (wt%) 5.0 ± 0.2 1.8 ± 0.0 – – N (wt%) 1.5 ± 0.3 1,3 ± 0,1 – – S (wt%) 0.4 ± 0.1 0.3 ± 0.3 – – P (wt%) 1.09 1.89 – – K (wt%) 2.97 2.62 – – O (wt%)a 48.6 ± 0.5 27.9 ± 0.2 – – Mg (wt%) 0.7 1.24 – – Fe (wt%) 0.28 0.32 – – Ca (wt%) 2.25 4.14 – – Na (wt%) 0.21 0.57 – – H/C 0.1 0.04 – – O/C 1.3 0.6 – – Moisture (wt%) 11.5 ± 1.2 8.5 ± 0.6 – – Volatile matter (wt%) 68.8 ± 3.7 24.9 ± 4.6 Optional Required Fixed carbon (wt%) 13.8 ± 2.9 43.2 ± 3.1 – – Minor metallic elements (mg/kg TS) Pb <2 3 70–500 <150 Cd 0.30 0.7 1.4–39 <1.5 Cu 26 64 63–1500 <100 Ni 96 14 47–600 <50 Hg <0.05 <0.05 1–17 <1 Zn 124 352 200–7000 <400 Cr 133 15 64–1200 <90 As 0.90 1.0 12–100 –

a Determined by O% = 100%-C%-H%-N%-S%-Ash%.

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products from Py of rice straw at 550 ◦C were mainly CO, CO2, CH4, and H2, accompanied with small amounts of C2+ gases. Specifically, CO2 and CO mostly derived from decarboxylation and decarbonylation reactions (Jeczmionek and Porzycka-Semczuk, 2014). Moreover, a large portion of CO2 produced resulted from the cracking of remaining fibers like cellulose and hemicellulose in digestate (Liu et al., 2011). The content of (H2 + CO) was determined to be 46.4%(v/vsyngas) and the ratio H2/CO was found to be 0.3, which is in agreement with results obtained in previous studies (Monlau et al., 2015b).

The bio-oil was obtained from Py of dry solid digestate, including organics and aqueous phase at a ratio of 42.8 wt%, and 57.2 wt%, respectively. Similarly, Cen et al. (2019) reported a distribution of 49.4 wt% and 50.6 wt% of aqueous phase and organic phase respectively after Py of rice straw at 550 ◦C. On the contrary, Neumann et al. (2015)

have found 71 wt% of organic phase versus 29 wt% of aqueous phase from the bio-oil produced from pre-conditioned digestate from an anaerobic digestion plant. The distribution of aqueous and organic phase of bio-oil mainly depends on the nature of initial material and the Py condition (Zhang et al., 2007). Generally, the aqueous phase of bio-oil is mainly composed of water originating from the initial moisture content and from the product of dehydration and the secondary cracking reaction (Wei et al., 2018; Zhang et al., 2007). Table 2 summarizes the properties of the organic phase of bio-oil. The organic phase of bio-oil presented a high carbon content (64.5 wt%) and low oxygen content (21.4 wt%), which is required for bio-oil fuel application.

The high heating value (HHV) of organic phase of bio-oil (Table 2) was estimated as 28.4 MJ/kg. These values are in the same range as those reported by Monlau et al. (2015b) after carrying out Py at 500 ◦C of solid digestate from an agricultural biogas plant with an HHV of 23.5 MJ/kg. Similarly, Neumann et al. (2015) reported Py at 750 ◦C of digestate from an agricultural biogas plant, resulting in a bio-oil with a slightly higher HHV of 33.9 MJ/kg. These values are also in agreement with results obtained by Zhang et al. (2007), which mentioned HHV of bio-oil ranging from 20 to 41 MJ/kg. Nonetheless, Opatokun et al. (2015) reported a lower value of 13.5 MJ/kg from food waste digestate pyrolyzed at 500 ◦C, which could be explained by the difference of feedstock origin.

After comparing our results with the NIST library data, it was determined that all compounds of the organic phase of bio-oil with more than 1% of the total area (defined by the percentage of the compound’s

Fig. 2. Syngas distribution and composition during the Py process.

Table 2 Properties of organic phase of bio-oil at 500 ◦C.

Parameters Values

C (wt%) 64.5 ± 0.8 H (wt%) 6.7 ± 0.2 N (wt%) 6.5 ± 1.7 Oa (wt%) 21.4 ± 2.7 Empirical Formula CH2.28O0.52N0.024

Density (kg/L) 1.12 HHVb (MJ/kg) 28.4

a Defined by difference. b High heating value.

Fig. 3. GC-MS chromatogram of the organic phase of bio-oil, with numbered compound names representing each peak.

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chromatographic area out of the total area) were identified. The GC-MS chromatogram of detected peaks and their area percentages are pre-sented in Fig. 3 and Table S1 (supplementary material), respectively.

As indicated in Fig. 3 and Table S1, the main compounds of the obtained organic phase of bio-oil were phenolic compounds, furans, organic acids, aldehydes, alcohols, ethers, and ketones that were mostly obtained from carbohydrates and lignin degradation. The main com-pounds were phenols and phenol derivatives from depolymerization of lignin as the major constituent of the solid digestate, which represent almost 65% of the total area of the detected peaks. Moreover, these results are in agreement with previous studies that investigated Py of anaerobic digestate (Liang et al., 2015; Opatokun et al., 2015; Wei et al., 2018). Wei et al. (2018) reported that the contents of phenolics com-pounds were 70.4% of the total area of the detected peaks in organic phase of bio-oil produced from digestate (originating from sargassum anaerobic digestion) pyrolyzed at 450 ◦C.

High selectivity to the phenol, cresol-derivatives, guaiacol, syringol and cyclopentanone was also observed, with 17.5%, 22%, 14.2%, 10.0% and 8.2% of the total area of the detected peaks, respectively (Table S1). Higher temperature (over 450 ◦C) facilitated the degradation of lignin in aromatic compounds, through the cleavage of C–C and C–O–C linkages among three phenylpropane units (namely coumaryl, coniferyl, and sinapyl alcohols) of lignin (Asmadi et al., 2011; Wei et al., 2018), resulting in increasing of phenol compounds content. Indeed, lignin has various functional groups of methoxyl, phenolic hydroxyl, aliphatic hydroxyl, benzyl alcohol, noncyclic benzyl ether, and carbonyl groups. Therefore, groups of phenol, alkyl phenols, methoxy phenols, alkyl-methoxy phenols, benzenes, and benzenediols were produced from decomposition of lignin in the solid digestate (Mansur and Sima-nungkalit, 2018).

In a recent study, Liang et al. (2015) have demonstrated that anaerobic digestion process can be considered as a pretreatment method for lignocellulose biomass to improve the quality of bio-oil and to in-crease the selectivity of pyrolytic products compared to biomass that was not anaerobically pretreated. Indeed, it was reported that the bio-oil recover from rice straw digestate showed a high total yields of phenols

compared to the yields of alcohols, acids, aldehydes, furans, anhy-drosugars, and ketones than the bio-oil from original rice straw (Liang et al., 2015).

In parallel, to have a clearer understanding of the compound distri-bution of the whole bio-oil, an analysis was carried out using 1H NMR in order to further examine the compound distribution (aromatic: aliphatic) of the organic phase of bio-oil (Aboulkas et al., 2017). The 1H-NMR spectrum of organic phase of bio-oil in Fig. 4 was explained in Table S2 (supplementary material).

The proton resonance between the chemical shift of 0.5–1.5 ppm corresponded to the presence of 15.9% of aliphatic protons attached to the paraffinic CH3. Moreover, peaks in the region between 1.5 and 3.0 ppm were assigned to the proton of aromatic ring or acetylenic (37.5%), which was previously confirmed by GC-MS analysis. The region of 3.0–4.0 ppm contributed to 9.1% of the protons in hydroxyls, ring- joining methylene, methyl or methoxy. The presence of lignin-derived methoxy phenol and non-conjugated olefins observed from the GC-MS results was also confirmed by the peaks between 4.0 and 6.0 ppm (14.2%). Finally, a region between 6.0 and 9.5 ppm corresponds to ar-omatic protons and hetero-aromatics (23.4%) (Garg et al., 2016).

3.2. Biochar characterization

The resulting biochar produced at 500 ◦C was also characterized, its physicochemical characteristics are presented in Table 1. The carbon content of biochar was 45.3 wt%, indicating it as class 2 biochar ac-cording to IBI, which is considered as bio carbon minerals and not as biochar according to EBC (Table 1). The amount of O and H decreased in the biochar due to the decarboxylation and dehydration reactions dur-ing the Py process, while N showed a slight decrease (1.5–1.3 wt%). These findings corresponded to the results reported by Neumann et al. (2015), where Py of solid digestate was performed at 500 ◦C, with the exception of higher amounts of carbon (65 wt%) and lower oxygen content (2.2 wt%) reported by these authors. Similarly, Opatokun et al. (2017) reported biochar carbon content varying from 35.7 wt% to 60.2 wt% after Py (performed between 300 and 700 ◦C) of solid digestate

Fig. 4. 1H NMR spectrum of organic phase of bio-oil.

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from anaerobic digestion of food wastes. Moreover, the ash content in biochar was found to be 23.4 wt%, similar to the 29.1 wt% reported by Neumann et al. (2015) after performing Py of solid digestate at 500 ◦C. During the AD, microorganisms convert the organic fraction of the or-ganics into CO2 and CH4, resulting in a high concentration of inorganics in the digestate. Generally, the inorganics exist as mineral salts and are bonded to the organic matrices through ionic or covalent bonds (Sad-dawi et al., 2012). Furthermore, P and other major nutrients essential for the plants were found to be higher in biochar compared to digestate, which is in agreement with previous publications that have investigated

biochar production from solid digestate (Calamai et al., 2019; Monlau et al., 2016). The biochar had the highest P (1.9 versus 1.1 wt%), Ca (4.1 versus 2.3 wt%), Mg (1.2 versus 0.7 wt%) and Na (0.6 versus 0.2 wt%) elemental contents compared to solid digestate. On the contrary, the solid digestate presented a slightly elevated K elemental content compared to its respective biochar (3.0 vs. 2.6 wt%). Trace metal con-tent (i.e., Pb, Cd, Cu, Ni, Hg, Zn, Cr, As) was also analyzed in the biochar. All the values obtained were lower than threshold levels recommended by the IBI and EBC as shown in Table 1.

The behavior of the solid digestate during thermogravimetric

Fig. 5. Cumulative concentration of nutrients leaching experiments (8 leachings over time) during 30 days of trials: a) NH4+, b) NO3

− , c) TMN (Total Mineral Ni-trogen), d) PO4

3, e) K+, and f) Na+ from soil; soil + LD (liquid digestate); soil + LD (liquid digestate) + B50 (biochar (50 t/ha)) and soil + LD (liquid digestate) + B100 (biochar (100 t/ha)). The data represents the cumulative means ± standard deviations.

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analysis is shown in Fig. S1 (supplementary material). According to the curve, the main loss of mass began at approximately 240 ◦C onward and progressed extensively until 500 ◦C, with a heating rate of 5 ◦C/min. This weight loss represents almost 64% of initial weight, and it is due to degradation of main recalcitrant compounds (fibers and lignin) of the solid digestate (Yang et al., 2007). The TGA curve of biochar revealed a clear difference compared to the solid digestate, with a slight loss from 110 to 900 ◦C, which is an indicative of the high stability of biochar after Py process. Slight loss could result from both moisture evaporation and volatilization of the incomplete carbonized phase of biochar (Tayibi et al., 2020). Table 1 also shows the volatile matter (VM) and fixed carbon (FC) of produced biochar. The VM of biochar was lower than those of solid digestate and estimated to 23.4% (Table 1). The FC of biochar was 43.2% compared to only 13% in solid digestate. The amounts of FC obtained from biochar in this study corresponded to the results of a previous study, where biochar was produced from pyrolyzed food waste digestate (Opatokun et al., 2015). However, our results differed significantly from those obtained from agricultural digestates pyrolyzed at 600 ◦C (ranging from 7.7 to 12.6 wt%) reported by Monlau et al. (2016). The scanning electron microscope (SEM) images of solid digestate and its biochar are presented in Fig. S2 (supplementary ma-terial). As shown in Fig. S2-a, the particle of solid digestate sample was dense and rough, and few pores were observed on the surface. In contrast, after Py, the surface of the material became loose and porous, and macroporous structures were observed (Fig. S2-b).

3.3. Agronomic assays by combining biochar and liquid digestate

3.3.1. Water retention and nutrients leaching The results of the effect of biochar on GWR of soil are presented in

Fig. S3 (supplementary material). Biochar was found efficient in improving gravimetric water retention of soil from 10 to 40%, compared to soil alone at biochar doses of 50 t/ha and 100 t/ha, respectively (Fig. S3). This result is in agreement with previous results published by Glaser et al. (2015), which reported an improvement of water retention after biochar addition at 40 t/ha that can be explained by an improve-ment of the soil porosity after biochar addition. Similarly, Novak et al. (2009) found that the water retention capacity was increased from 6.7 vol% to 15.9 vol%, after adding 2 wt% of switchgrass biochar on a loamy sandy soil.

Subsequently, leaching tests were performed. Although biochar is not considered as a nutrient-supplying biological source, its potential in crop fertilization has been demonstrated when combined with mineral fertilizers or other types of organo-fertilizers such as digestate and compost. In practical application, biochar is not used alone, but in co- application with a fertilizer and, consequently, the condition using biochar alone has not been retained.

The leaching tests were intended to represent the worst-case scenario with extremely heavy rainfall shortly after adding the liquid digestate causing it to spread (Sogn et al., 2018). The results of the leaching ex-periments are presented in Fig. 5. Interestingly, it was demonstrated that the application of biochar influenced positively the ammonium leach-ing. Compared to soil with LD, biochar application at 50 t/ha and 100 t/ha increased the cumulative NH4

+ leaching by 32% and 64% , respectively (Fig. 5a). On the contrary, biochar addition significantly reduced the cumulative of nitrate leaching (Fig. 5b). Indeed, compared with soil + liquid digestate, biochar application at 50 t/ha and 100 t/ha reduced the cumulative loss of NO3

− by 82% and 91%, and no significant difference was observed for the two concentrations. Gonzaga et al. (2018) found the same results testing the effect of biochar application on ammonium and nitrate leaching in two distinct soils (sandy and loamy) and demonstrated that the leaching of nitrogen in soil mainly depends on biochar properties and soil type. Similarly, Yao et al. (2012) demonstrated that a biochar produced from Brazilian Pepperwood at 600 ◦C effectively reduced the nitrate leaching in the sandy soil column by 34%, but caused additional phosphate release. The effect of biochar

on total mineral nitrogen (TMN) is presented in Fig. 5c, with results showing that the cumulative concentration of TMN in leachate under different treatments were similar to that of NO3

− (Fig. 5b), as the largest proportion of total mineral leached N was in the form of NO3

− . The re-sults of the cumulative leached phosphorus (PO4

3− ), potassium (K+) and sodium (Na+) were also investigated and are represented in Fig. 5d, e and f, respectively. Regarding the nutrient analysis of LD and biochar, it is obviously clear that the main source of the phosphorus, potassium and sodium was provided from biochar and not from LD or soil. In the case of cumulative PO4

3− leaching, the results showed that at application of 50 t/ha, phosphorus leaching was very low and was in the same range as leaching of soil and soil + LD. Such results are in agreement with pre-vious results demonstrated by Hamid Iqbal et al. (2015) in a study which showed that the co-application of biochar produced from Py of forest slash at 650 ◦C (25% by volume) and mature compost (75% by volume) did not affect the leaching of phosphorus (Iqbal et al., 2015). On the contrary, Laird et al. (2010), found that a biochar (mixed hardwood and hickory, using slow Py) application at 60 t/ha on a Midwestern agri-cultural soil resulted in a total dissolved P leaching of 69%. Surprisingly, at an application of 100 t/ha, the cumulative leached P increased significantly (from 0.002 mg PO4

3− /g to 0.044 mg PO43− /g of soil)

compared to soil with LD, suggesting that P loss is from biochar, as previously demonstrated by other studies (Nguyen et al., 2019). In addition, the same tendency was also observed for K, with a significant increase of cumulative K+ leaching (Fig. 5e), with increases of 0.40 and 1.35 mg K/g of soil observed for biochar application of 50 t/ha and 100 t/ha, respectively, compared to soil with LD application only. These results correspond to those reported by Widowati et al. (2014), which demonstrated that application of 45 t/ha of biochar obtained from co-conut shells significantly increased the leaching of K+ by 15 mg/L compared to soil only. Moreover, cumulative sodium leaching results are also presented in Fig. 5f. At application of 50 t/ha, the result showed that the cumulative sodium leaching was nearly the same as soil treated with LD. Nonetheless, an increase of the biochar dose at 100 t/ha resulted in higher cumulative sodium leaching, with a value of 0.58 mg Na/g of soil. Such results are in agreement with those reported in pre-vious study, which demonstrated that biochar (produced from rice husk and rice straw, at temperature ranging from 400 to 450 ◦C) incorpora-tion to a sandy soil at a proportion of 5% w/w increased the concen-tration of leached sodium by 92% compared to soil alone (Nguyen et al., 2019). In parallel, Nguyen et al. (2019) demonstrated that biochar addition linearly and significantly reduced Ca concentration (by 38%), but increased K (by 292%), and P (by 411%) concentrations in the leachate, compared to the non-biochar-added soil. Some recent studies have also suggested that when applied to soils, biochar may not only affect soil ion exchange capacity, but also provide refugia for soil mi-crobes to influence the binding of nutritive cations and anions (Liang et al., 2006; Yao et al., 2012). Further investigations are needed to un-cover the underlying mechanisms and will be the subject of future works. In our study, except for nitrate compounds, an application of biochar at 50 t/ha in combination with LD did not have significant effect on leaching behavior, whereas an increase of biochar load to 100 t/ha resulted in improvement of Na+, K+ and PO4

3− leaching and from an operational point of view, it can be recommended not to exceed appli-cation of 50 t/ha. Nonetheless, such results have also to be taken care-fully as the effect of biochar on the leaching of agricultural nutrients in soils is not uniform and varies by biochar, nutrient type and soil origin (Yao et al., 2012).

3.3.2. Growth plant test performances The impact of biochar addition was also evaluated on growth plant

tests (i.e., on wheat plants) to evaluate the potential phytotoxicity or benefits of biochar addition (at 50 and 100 t/ha) on the relative seed germination and plant growth measured in terms of aerial dry biomass (Fig. 6). Interestingly, biochar application at 50 t/ha in combination with LD did not exhibit negative impact on the relative seed

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germination. On the contrary, higher biochar application of 100 t/ha led to an inhibitory effect of the relative seed germination that can be attributed to the potential released of remaining toxicants (phenols, furans, sodium, etc.) from the biochar, as it was not washed prior to being used (Kookana et al., 2011). Furthermore, as previously reported in Fig. 5, the load of 100 t/ha of biochar resulting in higher sodium concentrations released and sodium content has been reported to affect the relative seed germination (Anaya et al., 2018).

In parallel, the growth plant efficiency of biochar (at 50 t/ha) in combination with LD exhibited a significant positive effect compared to soil alone and soil treated with liquid digestate. At 100 t/ha, besides the initial germination inhibition observed, plant growth in terms of aerial dry biomass was equivalent to 50 t/ha. Such results are in agreement with those reported by Greenberg et al. (2019), which demonstrated no impact on winter rye crop biomass by increasing the biochar load from 1 to 40 t/ha. Glaser et al. (2015) demonstrated that application of biochar-digestate (at biochar application of 1 and 40 t/ha and digestate at 200 kg N/ha) on maize yielded better results (e.g., yields and plant nutrition) compared to pure digestate. Interestingly, at a concentration of 40 t/ha of biochar, the co-application of digestate with biochar significantly improved maize yield by 42% compared to untreated plants without biochar addition (Glaser et al., 2015). On the contrary, Chan et al. (2007) have found that co-application of biochar at 10 t/ha (green waste produced at 450 ◦C) with nitrogen fertilizer (100 kg N/ha) decreased the dry biomass of radish by 29.7% compared to soil treated

with nitrogen fertilizer only. Nonetheless, the literature data currently available are sometimes contradictory and the benefits of coupling biochar and liquid digestate requires further in-depth study. Further-more, laboratory assays are not necessarily representative of real con-ditions and therefore, such experiments need to be extended to field-scale in the future. In parallel, several parameters could poten-tially influence the efficiency of coupling of LD and biochar, including environmental factors, quantity of biochar used, digestate origin and properties, soil composition, climatic conditions and plant tested, and should be investigated in the future.

4. Conclusion

The coupling of AD and Py has been demonstrated to serve as a promising strategy for solid digestate valorization into syngas, bio-oil and biochar. A specific focus was made on combining biochar and anaerobic liquid digestate for agronomic issues. The characteristics of biochar were in accordance with IBI and EBC recommendations for soil amendment. Biochar application improved the GWR of soil by 10% at application of 50 t/ha. The co-application of biochar with LD did not decrease nutrients leaching except for nitrate; however, their simulta-neous use improved the growth of wheat plant up to 27.5% and 67.8% in comparison to application of soil with LD and soil alone.

Fig. 6. a. Relative seed germination (after 10 days of sowing) and aerial dry biomass of wheat plant (after 24 days of sowing) in the different applied treatments: soil (S); S + LD (liquid digestate); S + LD (liquid digestate) + B50 (biochar (50 t/ha)) and S + LD (liquid digestate) + B100 (biochar (100 t/ha)), b. Plants before the harvesting step for each condition.

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Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

The authors would like to extend their gratitude to the Office Cherifien des Phosphates (OCP group, https://www.ocpgroup.ma/) for funding the agronomic trials through the ATLASS project. In addition, the authors gratefully acknowledge the European Commission Directorate-General for Research & Innovation for funding the project ‘‘NoAW: No Agricultural Wastes” (grant agreement No 688338), under which the pyrolysis assay was realized.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi. org/10.1016/j.jenvman.2020.111632.

Credit author statement

Saida Tayibi: Conceptualization, Investigation, Formal analysis, Writing - original draft. Florian Monlau: Conceptualization, Supervision, Review & Editing. Frederic Marias: Supervision, Review & Editing. Guillaume Cazaudehore: Investigation, Formal analysis. Nour-Elhouda Fayoud: Formal analysis, Review & Editing. Youssef Zeroual: Concep-tualization, Review, Project administration. Abdallah Oukarroum: Funding acquisition, Project administration. Abdellatif Barakat: Super-vision, Funding acquisition, Project administration, Conceptualization, Writing - review & editing.

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