Bioadsorption of lead(II) over the pulp of Acrocomia aculeata

The adsorption of lead in aqueous solution onto Acrocomia aculeata pulp was examined. The pulp was characterized in the presence and absence of lead using Fourier transform infrared spectroscopy (FTIR), thermogravimetric analysis (TG-DTA), and scanning electron microscopy (SEM). Sulfur and oxygen bonds were responsible for adsorbing lead onto the pulp surface. The TG-DTA profile proved that adding sodium azide increases the pulp’s thermal stability until 200 °C. Adsorption data in batch and column systems were analyzed to understand the pulp adsorption compared to other biomaterials. In the batch experiments, the removal efficiency reached a maximum of 91.9% when a solution of 50 ppm of lead was placed in contact with the pulp for 30 min and fit Freundlich isotherm behavior. In the column experiments, the theoretical maximum adsorption capacity was found to be 11.97 mg g; more column data is needed to compare column results to other studies. Further studies to improve the pulp adsorption capacity are needed for it to be a competitive biomaterial for water treatment.

onto Acrocomia aculeata pulp was examined. The pulp was characterized in the presence and absence of lead using Fourier transform infrared spectroscopy (FTIR), thermogravimetric analysis (TG-DTA), and scanning electron microscopy (SEM). Sulfur and oxygen bonds were responsible for adsorbing lead onto the pulp surface. The TG-DTA profile proved that adding sodium azide increases the pulp's thermal stability until 200 °C. Adsorption data in batch and column systems were analyzed to understand the pulp adsorption compared to other biomaterials. In the batch experiments, the removal efficiency reached a maximum of 91.9% when a solution of 50 ppm of lead was placed in contact with the pulp for 30 min and fit Freundlich isotherm behavior. In the column experiments, the theoretical maximum adsorption capacity was found to be 11.97 mg g -1 ; more column data is needed to compare column results to other studies. Further studies to improve the pulp adsorption capacity are needed for it to be a competitive biomaterial for water treatment.

Introduction
Lead is one of the five most harmful elements to human health (Tchounwou et al., 2012). Due to its high bioavailability, lack of biological function, and persistence in the environment, it is extremely toxic to ecosystems and living organisms (Jaishankar et al., 2014;Tchounwou et al., 2012). Some toxic effects of lead include damage to the central and peripheral nervous system, birth defects, inhibition of plant growth, and ecosystem bioaccumulation (Cardwell et al., 2013;Flora et al., 2012;Goyer, 1993;Jaishankar et al., 2014).
Though lead is naturally occurring, the majority of lead contamination results from anthropogenic sources (Tchounwou et al., 2012). Industrial sources of lead include fossil fuels, production of metals, mining, soldering, battery production, and pipping. Domestic sources of lead include decorative paint, children's toys, and cosmetics (Flora et al., 2012;Jaishankar et al., 2014;Tchounwou et al., 2012). Humans are exposed to lead from these products via respiration of dust containing lead or the ingestion of contaminated water. Cases of lead contamination are found on every continent, excluding Antarctica, and 49% of children and 52% of adults in the world have blood levels of lead higher than 5 ug dL -1 (Kessler, 2014). Thus, it can be concluded that lead contamination is a global public health crisis (Tong et al., 2000).
The World Health Organization standard for lead in potable water is below 0.01 ppm, recommending that contaminated water be treated so that lead levels are below the standard (WHO, 2006). The most common methods of water treatment for lead are chemical precipitation and ionic exchange. Chemical precipitation uses hydroxides and sulfides to produce a solid precipitate containing lead. This process is fast and easy to control, however, the chemicals used and the disposal of toxic solids generate high operation costs. Ionic exchange uses a synthetic organic resin to attract soluble ions from a liquid phase to a solid phase. Although this method has low operation costs, it is very sensitive to pH changes and only works with low concentrations of lead (Gunatilake, 2015).
Bioadsorption is an alternative method for treating water contaminated with heavy metals such as lead. In this study, bioadsorption is defined as the mass transfer of a substance to the surface of a biomass-derived solid via physical and chemical interactions. Bioadsorption is efficient in purification and separation, low cost, and easy to control. Furthermore, it is a process that is environmentally friendly. Common materials for bioadsorption include agricultural wastes, biopolymers, and industrial byproducts (Gunatilake, 2015).
In Paraguay, a biomaterial of interest is the coconut palm Acrocomia aculeata, known by its common name as "mbokayá" (Yubero et al., 2015). Acrocomia aculeata is a species native to South America with a high cultivation potential in Paraguay, home to over 4,546,000 hectares of the species (Plath et al., 2016). Unlike the African palm and soy, A. aculeata can be grown in a mixed culture and in infertile, sandy soils (Poetsch et al., 2012;Roman, 1996). This means that its cultivation does not compete with the nutrient-rich rainforest soil nor causes the loss of biodiversity associated with land clearing for monocultures (Plath et al., 2016). As this palm survives in extremely low temperatures, fire, and drought, it is resistant to extreme weather events brought on by climate change (Poetsch et al., 2012). The kernel oil from the coconut is already used in a variety of local products and industries in Paraguay, such as food, biofuel, cosmetics, and medicinal soap, and thus is an important economic resource for the country (Poetsch et al., 2012;Roman, 1996).
In addition to the environmental, social, and economic benefits of A. aculeata, the pulp of the coconut, a byproduct of kernel oil extraction, has proven capabilities in the bioadsorption of heavy metals from water. According to Yubero et. al (2015), the pulp of A. aculeata can adsorb up to 66% of chromium (VI), another heavy metal toxic to human health. Thus, it is probable that this material could effectively remove other heavy metals such as lead. This study aims to explore A. aculeata as a sustainable material for lead bioadsorption through the characterization of the pulp composition and structure and the analysis of lead adsorption in both column and batch systems.

Pulp preparation
The coconuts were collected in February of 2016, in semi-open field at the Jack Norment Camp in Caacupé, Paraguay. The pulp was processed by the Botany and Physical Chemistry Departments at Universidad Nacional de Asunción. First, the epicarp was removed and mesocarp cuts were made. The slightly insoluble fibers were then dried at 40 °C for two days (González et al., 2018;Yubero et al., 2016a;b). The size of the dry fiber was sieved for size selection, to be between 297 and 350 µm. To conserve the fiber, 0.5 g of sodium azide was added and homogenized in about 4 g of the size-selected fiber.

Characterization methods
Fourier transform infrared spectroscopy (FTIR) analysis from 500-4000 cm -1 was conducted on the native pulp and the pulp in contact with a 25 ppm Pb(II) solution for 5 min, 30 min, and 5 h, using the Shimadzu Europa GmbH IR Prestige-21. Thermogravimetric analysis (TG-DTA) was carried out using TA Instruments ST 2960 Simultaneous DTA-DTG on a sample of m = 5.6 mg of native pulp/sodium azide mix. The sample was heated at β = 20 °C min -1 under air atmosphere (100 mL min -1 ) in an open aluminum crucible (70 L) during thermogravimetric analysis (TG-DAT analysis. Scanning electron microscopy (SEM) images of the pulp azide mix after contact with Pb(II) were taken using FEG-SEM JEOL Model 7500F.

Solution preparation
The distilled water was tested with a PHS-38W microprocessor from Bante Instruments. The pH was found to have a pH of 5.84 at 25.4 °C. As lead has a solubility between a pH of 2 to 7, distilled water was used in the following solutions (Wang et al., 2017). Lead nitrate, Pb(NO3)2, were used in the preparation of all solutions.

Batch study
To prepare the pulp for batch experiments, 200 mg samples of the pulp were washed three times with 25 mL of distilled water. The batch experiment was carried out by adding a sample of 200 mg of pulp to a 13 mL solution with an initial concentration of either 30, 40, or 50 ppm Pb(II) to conical centrifuge tubes. Each sample was rotated for a required time of either 5 min, 30 min, and 5 h at 8 rpm. Next, the pulp and solution were centrifuged for 5 min at 6000 rpm. The supernatant was extracted and the final concentration of Pb(II) was tested using AA-6300 Shimadzu atomic absorption spectrometer. It must be noted that this experiment was performed in duplicate (i.e. two samples of pulp in contact with 30 ppm Pb(II) for 5 min, two samples in contact with 30 ppm Pb (II) for 30 min).
The Langmuir (Eq. 1) and Freundlich (Eq. 2) adsorption isotherms were applied to the batch data using the following equations.
where KL is the Langmuir constant (L mg -1 ), qm is the maximum adsorbed capacity (when the adsorbate monolayer has formed, mg g -1 ), KF is the Freundlich constant for adsorption capacity (L mg -1 ), n is Freundlich constant for adsorption intensity, and ci is the initial concentration adsorbate in solution (mg L -1 ). qe is the adsorption capacity at equilibrium (mg g -1 ), solved for using Eq. 3.
where cf is the final solution (mg L -1 ), m is the mass of adsorbent (g), and V is the volume of solution (L). Removal efficiency (Eq. 4) was also calculated for batch data using the following equation. (4)

Column study
A 5 mL syringe with needle was used as the column. A sheet of packing plastic was placed at the bottom of the syringe and 200 mg of pulp were loaded into the column. The syringe needle was connected to a tube that fed through a peristaltic pump that regulated a flow rate of 4 mL min -1 , as seen in Fig. 1.
Twenty-five mL of distilled water were passed through the column to stabilize the column bed. After the pulp was stabilized, a 35 ppm Pb(II) solution was continuously passed through the column. Over a 3-time period, 15 mL samples of effluent solution were collected every 15 min in conical centrifuge tubes. In between sampling times, the effluent was collected in a waste beaker. The levels of Pb(II) in the conical centrifuge tube samples were tested using atomic absorption spectroscopy.  The Thomas (Eq. 5) and Yoon-Nelson (Eq. 6) models were applied to column data using the following equations.
where Co is the original concentration of the solution (mg L -1 ), Ct is the concentration of the effluent solution (mg L -1 ), Q is the flow rate (mL min -1 ), KTH is the Thomas model constant (mL mg -1 min -1 ), qTH is the theoretical adsorption capacity, and t is the time (min).
where Co is the original concentration of the solution (mg L -1 ), Ct is the concentration of the effluent solution (mg L -1 ), flow rate of the influent solution (mL min -1 ), t is the time (min), KYN is the Yoon-Nelson constant (min -1 ), and τ is the time to reach 50% saturation of the column.

Materials characterization
The data for the infrared (IR) spectrum of the native pulp is found in Tab. 1. The native pulp had a characteristic fingerprint region, defined by bands 1-8 in Tab. 1, with representative bands at 1735, 1374, and 1064 cm -1 (Yubero et al., 2015). These bands correspond with C=N/C=O, C-O-C, and C=S/S=O bonds (Chang, 1981). When the pulp was in contact with a 25 ppm Pb(II) solution, the bands in the fingerprint region shrink in intensity as the contact time with the lead solution increased, as seen in Fig. 2. This change in intensity, an indicator of change in dipole movement, indicates that the oxygen and sulfur bonds are most likely involved in capturing the Pb(II). Additionally, a band appears at around 2300 cm -1 in the Pb(II) contact spectra, highlighted in Fig. 2, at a stronger intensity than in the raw pulp IR spectrum. This band could indicate the presence of Pb(II) nitrate. The results of the scanning electron microscopy (SEM) imaging are found in Fig. 3. These images reveal the pulp to have a rough, fibrous surface texture. The thermogravimetric analysis (TGA) profile of the pulp azide mixture (Fig. 4) was compared to the TGA of A. aculeata pulp in absence of sodium azide, from Fig. 4. It must be noted that in Corrêa et al. (2019) the pulp was heated at 10 °C min -1 under synthetic air while the conditions for this experiment was 20 °C min -1 . The raw pulp had four decomposition steps, while the thermogravimetric/derivative thermogravimetric (TG/DTG) curves of the pulp sodium azide mixture reveals that there are three distinct decomposition steps (Fig. 4). In the raw pulp TG/DTG curve, the first step occurred between room temperature and 160 °C and was endothermic due to the presence of water in the fibers (Corrêa et al., 2019). Similarly, the first step in the pulp azide mechanical mixture is endothermic between 25 and 100 °C and can be associated with water molecule evolution.  The next decomposition step in the raw pulp TGA was exothermic and the largest; it occurred between approximately 190 and 300 °C and can be attributed to the decomposition of hemicellulose and cellulose. This step was followed by two small exothermic mass losses between approximately 390 and 425 °C that can be attributed to the decomposition of lignin (Corrêa et al., 2019). On the other hand, the pulp azide mixture demonstrated thermal stability until about 200 °C, proving that the sodium azide causes a slight stabilization in the material. The following step for the sodium azide mixture is strongly exothermic and can be associated with the kinetically fast decomposition of cellulose and the formation of the metallic Na species from sodium azide, which both simultaneously occur between 200 and 340 °C. The largest percentage weight loss occurs during this step at T DTA peak = 336 °C, which is right around the temperature that sodium azide decomposes according to literature. It can be concluded that the presence of sodium azide accelerates the decomposition of the material in this step. The residues from the decomposition reaction of cellulose and sodium azide to metallic Na then decomposes in the step between 350 and 510 °C. The DTG and DTA curves are in agreement with each other and the literature, revealing two small peaks that are associated with the slow kinetics steps of consecutive reactions (Fujimoto et al., 1990). A total of 94.3% of the pulp sodium azide mixture decomposed.

Batch study
In the batch study, the removal efficiency (see Eq. 4), or performance in terms of amount of lead removed was found to reach a maximum of 91.9% when a 13 mL solution of 50 ppm of Pb(II) was placed in contact with 200 mg of pulp for 30 min. The Langmuir and Freundlich adsorption isotherms for 5 min of contact with the lead solution are found in Figs. 5 and 6, respectively. It is important to note that most results from the 5 h and 30 min contact time were found to be under the limit of quantification of the instrument (6.30 ppm Pb(II)), so these isotherms were not included in this paper (Silva, 2016). The results from the application of the Langmuir and Freundlich isotherm models applied to the batch results are summarized in Tab. 2.   The R 2 value suggest that the Freundlich model fits the adsorption behavior slightly more than the Langmuir model. This indicates that the distribution of surface energy is heterogenous. The Freundlich model also is in accordance with the SEM images, as Freundlich adsorption commonly occurs on rough surfaces (Fig. 3) (Chang, 1981). The n value, the Freundlich constant for adsorption intensity is greater than 1, which indicates that the adsorption reaction is kinetically favorable. The Freundlich constant for adsorption capacity, KF, however, is low compared to other biomaterials in batch, as seen in Tab. 3. The pulp was found to have a low adsorption capacity, qe (Eq. 3), of 2.3 mg g -1 in comparison to other biomaterials (Tab. 3). Since the adsorption capacity defines the amount of adsorbate taken up by the adsorbent, the low value indicates that it is not a promising biomaterial for filtration (Tab. 3). Future optimization studies regarding ideal conditions for adsorption or chemical treatment of the material are needed to improve the adsorption capacity.

Column study
The experimental breakthrough curve from the column experiment is found in Fig. 7 and the breakthrough parameters, along with the Thomas and Yoon-Nelson results, are summarized in Tab. 4. The breakthrough curve resembles the typical shape for column adsorption. The breakthrough time, which is defined as the time at which the concentration of the effluent solution is equal to 5% of the influent concentration, occurs in the first 15 min. This signifies an efficient mass transfer rate. The exhaustion time, the time at which the concentration of the effluent solution reaches 95% of the influent concentration, was found to occur between 2.50 and 2.75 h. The long exhaustion time indicates that the pulp-column system would have a long operating life.  The Thomas (Eq. 5) and Yoon-Nelson (Eq. 6) are mathematical models for Langmuir adsorption used to describe the performance of the column. The Thomas model is typically used to calculate qth, the theoretical adsorption capacity of the pulp, which describes the maximum solid phase concentration of Pb(II) on the pulp. This was found to be 11.97 mg g -1 . The Yoon-Nelson model is a model for fixed bed, single component adsorption that assumes the decrease in probability of adsorption for each Pb(II) molecule is proportionate to the probability of breakthrough on the pulp by the Pb(II). When applied to the data from the column study, the Thomas and Yoon-Nelson models had low R 2 and, therefore, did not fit the adsorption behavior of Pb(II) (Tab. 2). The Rq, which is the ratio of the theoretical adsorption maximum in column compared to batch, was calculated using the results from the Thomas model in column and Langmuir model. The ratio of 1.022 shows that the column and batch systems have almost equal efficiency in adsorption of Pb(II), however, as the adsorption does not follow Langmuir behavior and the Thomas and Yoon-Nelson models have poor R 2 coefficients, the column results cannot truly compare the efficacies of both systems. It is necessary that more column data be collected so that an accurate performance assessment can be made.

Conclusions
The IR characterization revealed that bonds containing oxygen and sulfur were involved in the adsorption of Pb(II) ions from water. The TGA analysis demonstrated that sodium azide increases the pulp stability. In accordance with the rough surface revealed from the SEM images, the pulp adsorption of Pb(II) specie follows the Freundlich model preferentially, indicating that the binding sites have a  heterogenous distribution of energy and do not form a single layer. The adsorption parameters in batch, however, indicate lower performance when compared to other biomaterials. While the breakthrough curve from the column experiments demonstrated efficiency and operation durability, more column experiments need to be conducted in order to determine which model best describes the adsorption behavior and performance. Future studies on improving the adsorption capacity of A. aculeata are needed to understand this biomaterial full capabilities as a sustainable water treatment for Pb(II).