The influence of biochar pyrolysis temperatures on the efficiency of soil amendment for Imazapic sorption

Weeds are responsible for losses in sugarcane productivity, often requiring the application of herbicides to control their infestation in crops. One of the herbicides commonly used in sugarcane cultivation is Imazapic. However, this chemical can be leached into environmental compartments when applied to soil, contaminating it. Scientific research has shown that the soil amended with biochar can reduce the leaching of herbicides, avoiding environmental pollution. Therefore, the present work aimed to evaluate the adsorption efficiency of Imazapic in a dystrophic Yellow Ultisol amended with biochar cultivated with sugarcane. Biochars were produced with sugarcane bagasse by pyrolysis at temperatures of 300, 500, and 700ºC to evaluate the adsorption capacity of Imazapic by the soil amended with biochar. The experiments revealed an increase in Imazapic adsorption with soil amended with biochar and that the adsorptive potential is more significant for pyrolyzed biochars at higher temperatures. In this way, the biochars produced can reduce the risks of groundwater contamination by increasing the residence time of Imazapic in the surface layer of the soil, being subject to the action of microbial degradation and other forms of degradation. é o caso do Imazapic (IMZ). No entanto, o IMZ pode ser lixiviado em compartimentos ambientais quando aplicado ao solo, contaminando-o. Pesquisas científicas mostraram que o solo corrigido com biocarvão pode reduzir a lixiviação de herbicidas, evitando a poluição ambiental. Portanto, o trabalho teve como objetivo avaliar a eficiência de adsorção do IMZ em um Argissolo distrófico modificado com biocarvão na cultura de cana-de-açúcar. Biocarvões foram produzidos com bagaço de cana por pirólise nas temperaturas de 300, 500 e 700ºC para avaliar a capacidade de adsorção do IMZ pelo solo corrigido com biocarvão. Um aumento na adsorção de IMZ com solo corrigido com biocarvão foi observado e que o potencial adsortivo é mais significativo para biocarvão pirolisado em temperaturas mais altas. Desta forma, os biocarvões produzidos podem reduzir os riscos de contaminação das águas subterrâneas aumentando o tempo de residência do IMZ na camada superficial do solo, ficando sujeito à ação da degradação microbiana e outras formas de degradação.


INTRODUCTION
Sugarcane cultivation in the Northeast region of Brazil has been carried out since the colonial period, with the predominance of cultivated areas in the coastal and wild regions of the states of Alagoas, Pernambuco, and Paraíba (OLIVEIRA et al., 2016).
According to CONAB (2022), this region produces more than 58 t ha -1 and, together with the country's northern region, accounts for 6% of the national sugarcane harvest.
Sugarcane cultivation can be harmed by pests, diseases, and weeds, causing significant losses in productivity when not adequately controlled. Herbicides are commonly employed to control weed infestation and minimize their effects on crops.
However, these chemicals can be harmful not only to weeds but also to the cultivation of sugarcane. This feature is due to their ability to move in the environment, being able to be transported together with the percolation water (leaching), as well as by surface runoff, thus reaching the water reservoirs (surface and subsurface water) (LOPES; ALBUQUERQUE, 2018).
One of the herbicides commonly used in sugarcane cultivation is Imazapic, which can control the purple nutsedge (Cyperus rotundus L.), one of the leading invasive plants in areas cultivated with sugarcane (ASSIS et al., 2021). The study developed by Assis et al. (2021) points out that the use of Imazapic in the cultivation of sugarcane in the state of Pernambuco demands attention regarding the application of the product.
The high rainfall in the southern and northern forests of the state (> 1500 mm per year), associated with the irrigation system, raises concerns about the concentration of this product used as a pre-emergent herbicide. In this way, the herbicide can be leached to other environmental compartments, becoming a contaminant.
On the other hand, the presence of organic matter in the soil can increase the adsorption of contaminants, consequently reducing their leaching to deeper layers. Some researchers, such as Abdelhafez, Abbas, & Li (2017); de Figueredo, da Costa, Melo, Siebeneichlerd, & Tronto (2017);Hai Nguyen Tran et al. (2020); Petter et al. (2019) point to the application of biochar on the soil as a way to reduce the leaching of organic contaminants, such as Imazapic, which can reduce the risks of soil and water contamination. Therefore, it becomes relevant to study the addition of biochar to the soil as a retention agent for Imazapic.
In this context, the present work aimed to evaluate the efficiency of adding pyrolyzed biochar to the soil at different temperatures, obtained from sugarcane bagasse, in the adsorption of the herbicide Imazapic in a Yellow Ultisol with sugarcane cultivation.

Study area and soil sampling
The study area is characterized by the predominance of dystrophic Yellow Ultisol (YUd) of medium texture with sugarcane cultivation on a half slope (7°47'59.02"S and 35°0'18.45"W). According to Vale et al. (2019), the soil has a total porosity of 36.74%, a pH of 6.7, and a potential Cation Exchange Capacity (CEC) of 4.83 cmolc dm -3 .
The sampling of the soils was carried out in soil with the herbicide Imazapic during the dry period (February 2016). Twenty simple samples were randomly collected to form a composite sample from the 0-20 cm layer of soil.
To obtain Air Dry Soil (ADS), the soil samples were crushed, air-dried, and passed through a 2.00 mm sieve for further physical and chemical analysis using the EMBRAPA method (TEIXEIRA, P. C. et al., 2017).

Production and analysis of biochar
Biochar was produced from sugarcane bagasse collected in the same sugarcane mill where the soil was collected. The bagasse was washed and placed to dry in an oven at 105ºC for 72h. The material was crushed in an industrial blender with titanium blades, sieved in a 1 mm mesh sieve, stored in bags, and sealed until the beginning of the biochar production process.
Biochar was produced by the slow pyrolysis of sugarcane bagasse in a Muffle furnace JUNG Model LF2312O, with Nitrogen (N2) being the carrier gas used in the pyrolysis to eliminate oxygen (O2) from the system. Table 1 presents the pre-established operating conditions for the pyrolysis process. After production, the biochars were placed in a desiccator later used in kinetics and adsorption isotherms assays and submitted to physicochemical characterization analyses.
To calculate the yield of biochar (Y), the mass of bagasse verified before pyrolysis and the mass obtained after pyrolysis were considered. The pH, electrical conductivity

Assessment of the interaction of Imazapic with the soil
The adsorption of the herbicide Imazapic in unamended (control) and biocharamended soil samples was assessed through kinetic and adsorption isotherm assays. In the analytical curves prepared for reading Imazapic in the High-Performance Liquid Chromatography (HPLC) device, the Imazapic molecule with 99.5% purity (CAS nº 104098-48-8, PESTANAL ® , analytical standard) was used, obtaining a coefficient of determination (r 2 ) above 0.99.
The mobile phase used for the HPLC readings consisted of a mixture of Acetonitrile: water (60:40, v/v), acidified to pH 3.0 with phosphoric acid (1:1, v/v), and a flow rate of about 1.0 mL min -1 . The maximum wavelength for detection was 212 nm.
The kinetics experiment for soil unamended with biochar consisted of mixing 10 mL of solute (V1) of known concentration of Imazapic 0.5 g L -1 (Co) and a mass of soil (ms) of 5 g. For the soil amended with biochar, the total mass consisted of the addition of 4.95 g of soil and 0.05 g of biochar. This procedure was used for the three pyrolysis temperatures.
After reading in HPLC, the data were fitted to two kinetic models, one of pseudofirst-order and the other of pseudo-second-order, using the methodology of Yaneva;Koumanova (2006). The Nash-Sutcliffe methodology has been employed to evaluate the modeling efficiency (NASH; SUTCLIFFE, 1970).
The study of adsorption isotherms was carried out for unamended and biocharamended soil samples. The commercial product Plateau® (BASF, composed of 70% of the Imazapic molecule and 30% of inert material) was used. As observed in the kinetic assays, a time interval of 24 hours of agitation at room temperature was considered for the Imazapic to reach equilibrium with the soil.
In the batch equilibrium tests, a volume of 10 mL of Plateau herbicide (Imazapic) and a proportion of 4.95 g of soil + 0.05 g of biochar was mixed in a reaction tube (falcon) to maintain the percentage of 1% of biochar in the soil, which according to Rezende et al., (2011) is within the optimal range for soil conditioning. The concentrations of the herbicide Imazapic (mg L -1 ) used in the assays in three replicates were 20, 50, 125, 255, 510, 1020, 1590, and 2040 mg L -1 . These values were adopted because they include the herbicide concentrations applied in the field in the study area. The pH of the solution containing Imazapic was adjusted to the soil one. The extracts were analyzed by HPLC, which allowed estimating the equilibrium concentration (Ceq).
The concentration of Imazapic, adsorbed to the soil, was the difference between its value before contact with the soil (C0) and after reaching equilibrium (Ceq).
The calculation for the assessing of the adsorbed Imazapic concentration was performed according to equation 1 (LAVORENTI; PRATA; REGITANO, 2003): where, S is the adsorption capacity (g kg -1 ); C0 is the initial solute concentration (mg L -1 ); Ceq is the solute concentration after equilibrium (mg L -1 ); Vl is the volume of the solution (mL); ms is the sum of soil and biochar masses (g).
For the statistical analysis of the data, calculations of the means and standard deviation of the three repetitions were performed. With the help of Solver from Excel (Microsoft Office 365), the best fit of the experimental data was estimated using the Freundlich and Langmuir isotherm models (Table 2) in their direct or even linearized forms (models of Freundlich and Langmuir).
The parameters of Freundlich and Langmuir models in linearized forms were determined in data analysis by Regression using the Excel application (Microsoft Office 365). The linear model was determined directly from Excel.

Characterization of biochar
The biochars produced at different temperatures (300, 500, and 700°C) differed in several physical and chemical aspects. It is worth noticing that the temperature used in the pyrolysis of biomass influences the various properties of biochar, as attested by Figueredo et al. (2017). Table 3 shows the characterization of the biochars produced at different pyrolysis temperatures.  Table 3 shows that with the increase in the pyrolysis temperature, there was a reduction in the yields of the biochars produced. For Rodrigues et al. (2013) The pH values obtained in the biochar analyzes (Table 3)  Still, considering Table 3, each biochar's electrical conductivity (EC) varied with the increase in the pyrolysis temperature, increasing its values between 300°C and 500°C and a slight reduction in the temperature of 700°C. These results corroborate those of Abdelhafez;Abbas;Li (2017), who state that in biochars of plant origin, the increase in temperature is capable of causing an increase in EC. The temperature rise caused a reduction in the apparent density of the biochar.
It is worth mentioning that the introduction of biochar to the dystrophic Yellow Ultisol probably increases its porosity, which, consequently, contributes to water retention and aeration since the apparent density of the biochars is significantly lower than the dry bulk density of the studied soil and, the lower the density, the greater the pore volume. In this sense, when there is a reduction in the apparent density, there is an increase in the specific surface area (SSA). In practical terms, this implies that biochars produced with high pyrolysis temperatures present higher SSA and, consequently, greater capacity to retain contaminants by adsorption (AHMAD et al., 2014;SAFAEI KHORRAM et al., 2016).
Another parameter capable of affecting the adsorbent potential of biochar is microporosity, expressed in terms of Micropore Area (MA). It was observed that the parameter was considerably higher for the 500°C and 700°C biochars. These results follow Maia (2011), who showed that the increase in temperature in the pyrolysis process leads to an increase in micropores in the material.    The H contents reduced 2.5% from the temperature of 300°C to 700°C. This gradual hydrogen reduction behavior with increasing pyrolysis temperature was also observed by Pergoraro (2015). (A) BC300magnification 30X (B) BC300magnification 3000X (C) BC500magnification 30X (D) BC500magnification 3000X (E) BC700magnification 30X (F) BC700magnification 3000X.

A B
C D

E F
The three types of biochar presented porous surfaces, which can be attributed to the loss of gaseous and volatile compounds (SONG; GUO, 2012). It is possible to observe the presence of transverse channels, similar to the shape of a rod, and smoother and elongated surfaces in the BC500 and BC700 biochars.
BC300 showed a more significant amount of macropores, while BC700 showed the appearance of micropores in its morphological structure. BC700 presented a distinct characteristic, which refers to the presence of sub-pores on the internal walls of the pores, which can offer greater adsorptive capacity for this material. According to Pereira et al. (2020), the high porosity of biochars reveals the adsorbent potential to contaminants and toxic substances in the soil.

Soil adsorption kinetics
The kinetics assay allowed us to determine the time interval for the adsorption of Imazapic to become approximately constant in the soil, that is, to reach equilibrium. This data is relevant since the observed equilibrium time was used as the sample agitation time in the isotherm assays. The curves presented in Figure 3 represent the behavior of the herbicide when in contact with the soil, with higher amounts of Imazapic adsorbed in the initial phase of the assay.  Table 4 shows the kinetic parameters associated with the pseudo-first-order and pseudo-second-order models. From the kinetic curves shown in Figure 3, it can be seen that the sorption of Imazapic occurred more quickly in the first 12 hours and then showed slower growth of adsorbed concentrations, with a smaller increase in sorption until reaching the stabilization. It can be noted that 24 hours after the beginning of the assay, Imazapic came into equilibrium with the soil, with a slight variation of adsorption over time. Similar BC300 BC500 BC700 The form of kinetics observed in Figure 3 for each type of biochar was similar, suggesting the involvement of similar mechanisms in the adsorption process. However, it was observed that the amount (S) and the adsorption rate (k) of adsorbed Imazapic were slightly higher for BC700.
The pseudo-first-order kinetic model presented Modeling Efficiency (EM) values closer to unity (1) and higher than those obtained by the pseudo-second-order kinetic model. Therefore, the model that best represented the observed data was the pseudo-firstorder kinetic model. Figure 4 shows the adsorptive behavior of the soil unamended and amended with biochars produced at temperatures of 300, 500, and 700°C. The isotherms were plotted as a function of the concentration of Imazapic adsorbed to the soil (mg kg -1 ) and the substance concentration in the solution after reaching equilibrium (mg L -1 ).   When observing the graphs presented in Figure 5, it was verified that the curvature of the Langmuir and Freundlich isotherms was more remarkable as the pyrolysis temperature increased, approaching the linear format at the temperature of 300°C.

Adsorption isotherms
In the Freundlich isotherm model, the values of the coefficient n did not approach unity (Table 5). Therefore, it can be considered that the adsorption is not linear because the binding energies are not identical for all adsorption sites (NASCIMENTO et al., 2014).
Based on the values of the adsorption coefficients KF (Freundlich) and KL (Langmuir), as well as the values of the coefficients of determination (R 2 ) observed in Table 5, the best adjustments were made using the Freundlich model. The isotherms here presented are similar to type I, which are associated with adsorption to micropores, according to Silva (2016).
The biochar showed good adsorption capacity of Imazapic, which differed considerably in the temperature at which the biochar was produced. According to the constructed isotherms, the higher the biochar's temperature, the more significant the increase in the adsorptive potential. The premise that more significant adsorption of organic substances is obtained with the application of biochar produced under high temperatures and being reaffirmed in this research is defended by Abdelhafez;Abbas;Li (2017). For the authors, pyrolyzed biochars at high temperatures exert greater adsorption of organic contaminants, while those at lower temperatures have an essential role in retaining heavy metals.
The value of KD (direct adjustment) for YUd unamended with biochar was 0.1596, being lower than those obtained with the same soil amended with biochar (Silva, 2016), which obtained a higher KF (11.06) when BC700 was used (Table 5). Thus, it is considered that the addition of biochar to YUd increased the adsorption capacity of Imazapic.
In the nonlinear fit of the Langmuir isotherms, the KL constant increased with the pyrolysis temperature, with the highest value observed for BC700 (0.0025). Increasing these values means the binding energy between the soil and the herbicide is higher for biochars produced at high temperatures.
The biochars' distribution coefficients (KD) varied from 0.149 to 0.233 L kg -1 , registering an increase in the values with the addition of the pyrolysis temperature of the biochars. This variable demonstrates the tendency of Imazapic to become adsorbed to the soil or sediment. Thus, there was a higher KD value for BC700, demonstrating greater adsorption potential attributed to this biochar. Barbosa et al. (2013) obtained results in studies in which biochars promoted the most significant adsorption with higher pH. As in this research, the higher pH biochars were pyrolyzed at higher temperatures (Table 2). For the authors, the increase in pH may have favored the deprotonation of the functional groups of the biochar, resulting in more significant adsorption of cations. However, in the adsorption of Imazapic, possibly the pH was not the decisive factor in the increase of the adsorption. Thus, other characteristics attributed to biochars produced under high temperatures may have been responsible for the increase in adsorption, such as specific surface area (SSA), porosity, fixed carbon content, and mineral fraction. It is worth mentioning that BC700 presented SSA 40 times greater than BC300 and twice that of BC500 (Table 2) and presented in its porous structure, the presence of sub-pores, which may have contributed to the increase of its adsorptive potential.
As confirmed in the data obtained, biochar is an effective adsorbent in immobilizing organic pollutants. The high adsorbent capacity of this material can be translated into the reduction of Imazapic leaching and the risks of groundwater contamination. In addition, if the greater immobilization of Imazapic resulted in a slow release to the soil solution, it could reflect greater crop use. If proven, it would avoid the doses applied to the soil being lost to the water table and decrease the productive potential of the soils, thus reducing the risks of environmental pollution. The benevolent effect of applying biochar to the soil is also justified because Imazapic can persist in the soil for up to 410 days.
Considering that Assis et al. (2021) report that Imazapic has a high Groundwater Vulnerability Index (GUS), the YUd amended with sugarcane bagasse biochar may cause its immobilization in the more superficial layers of the soil (0-20 cm), decreasing its movement to other environmental compartments. Therefore, adopting this technique can reduce the risks of water contamination by Imazapic.
It is worth mentioning that the greater adsorption capacity conferred on the soil can be obtained through the application of BC700, which, according to the results of this research, caused more significant adsorption between the herbicide and the solid adsorbent material.
BC500 can offer intermediate adsorption greater than BC300, but not as expressive as that observed with the addition of BC700. In this way, the application of BC500 can be helpful to prevent a "trapping" of Imazapic, preventing it from being so retained on the surface that it cannot be used to control weeds; being necessary to carry out desorption studies to confirm this hypothesis. Applying this biochar can considerably reduce leaching rates and allow the release of the adsorbed Imazapic to the soil solution, increasing its availability to weed seeds.
In general, the biochar produced from sugarcane bagasse can reduce the risks of contamination of groundwater since it makes Imazapic stay longer in the surface layer, being subject to the action of microbial degradation and other forms of degradation.

CONCLUSIONS
This research showed that changes in pyrolysis temperatures influence the properties of the produced biochar, such as morphological structure, specific surface area, and amount and area of micropores present. Using the Freundlich isotherm model, our experimental data pointed out that the higher the biochar pyrolysis temperature, the higher the augmentation in the dystrophic Yellow Ultisol's adsorptive potential. Overall, the present work indicates that incorporating sugarcane bagasse biochar in the soil can increase the adsorption of herbicide Imazapic in the dystrophic Yellow Ultisol (YUd), reducing leaching risks and contamination of the groundwater.

AUTHORS' CONTRIBUTION
Daniele Aparecida wrote the master's thesis that gave rise to this article, being responsible for biochar production and participating in laboratory assays. André Maciel designed and supervised this research work, contributing to the discussion and revision of this manuscript. João Paulo actively participated in the laboratory's experimental assays and the construction of the graphs of the results. José Victor Chaves performed experimental procedures for isotherm assays. Ademir Amaral participated in discussing and reviewing the text and its translation into English.