Removal of toxic metals using endocarp of açaí berry as biosorbent

Among the several contaminating elements of water resources, heavy metals are dangerous compounds derived from the inadequate storage of non-treated industrial waste. They are priority contaminants due to their toxicity and to their mobility in surface or underground waters, constituting a serious environmental and public health issue. Cadmium (Cd), lead (Pb), chromium (Cr) and other metals are highly toxic in human physiology, causing several diseases and disorders (Bulgariu & Bulgariu 2012).

There are several methods for the removal of these contaminants, such as chemical and physical precipitation, ionic exchange, extraction by solvents, bio-accumulation by aquatic plants or micro-organisms, and filtration by membranes. The adsorption process is one of the most promising for metal remediation (Witek-Krowiak 2012).

Activated carbon is one of the most frequently used adsorbents, although at high costs of production (Santhi et al. 2010). The main characteristics of this material are high surface area, high porosity and surface reactivity, which are excellent characteristics for an adsorbent material. The high cost of production is due to the dependence on controlled burning of biomass with low oxygen content at temperatures of 800 to 1,000 °C, i.e., with great energy expenditure to obtain a small amount of carbon mass (Peireira et al. 2008), which is the main reason for not using it in large scale adsorption processes.

With this in mind, biosorption is a method with a significant contribution for the removal of chemical contaminants (Febrianto et al. 2009).

Biosorption is the natural capacity of biomass to adsorb dissolved components, i.e., the removal of contaminants in the environment, such as from aqueous solutions. Main requirements for the selection of adequate biosorbents are adsorption and regeneration capacity, kinetic and thermodynamic parameters, costs and availability of adsorbent material (Witek-Krowiak 2012).

The search for new adsorbents has been focused on biomaterials, because they are of high availability, biodegradable, economically viable and derived from renewable resources. In general, these materials are locally and easily available in large amounts in the agroindustry. Therefore, they are usually cheap and have little or no economic value (Barreiro et al. 2014; Quintáns-Fondo et al. 2016); i.e., these materials are wastes with no industrial or agricultural use, with their accumulation being in many cases a problem.

Another advantage of the use of such adsorbents is that the content of these materials is lignin, cellulose and other organic species, which include functional groups such as carboxylic groups, phenolic groups, amides, and others, which usually are indicative of good adsorbent materials (Feng et al. 2011).

The ‘açaizeiro’ (Euterpe oleracea Mart.) is a tropical, perennial palm tree, common in Brazil, which occurs in the North and Northeast, belonging to the Arecaceae family (Gonçalves et al. 2016). This plant can reach heights of more than 25 meters, with trunks of 9 to 16 centimeters in diameter. Its fruits, the main product of this palm, are rounded, with one to two centimeters in diameter and an average weight of 0.8 to 2.3 grams. The endocarp is bulky and hard, constitutes about 80% of the total volume of the fruit, and is covered by fibrous layers, which are rich in cellulose, hemicellulose and lignin (Pacheco-Palencia et al. 2009), which can be excellent composition characteristics for biosorption of metallic ion processes.

About 216 thousand metric tons of Euterpe oleracea berries, commonly known as açaí berries, are produced only in Brazil every year, mainly in the Amazon region. The consumption of açaí in the northern region of Brazil is generally combined with other regional foods or in the form of ice cream, creams, porridge, jellies and liqueurs, leaving the endocarp, which does not generate any benefit, with no industrial or agricultural use (Gonçalves et al. 2016).

Açaí berries have already been shown to have excellent characteristics for Cu(II) and Zn(II) removal from polluted waters (Gonçalves et al. 2016); however, studies examining the use of this adsorbent for toxic metals are not yet available in literature.

The current study investigates the potential use of the endocarp of the açaí berry as a biosorbent in the removal of Cd(II), Pb(II) and Cr(III) from water. The study also deals with the characterization of the adsorbent material by surface morphology, determination of functional groups and of point of zero charge, the evaluation of kinetic, equilibrium and thermodynamic factors of adsorption of metal ions, elution and comparisons with a commercial adsorbent.

Endocarps of the açaí berry used in the current experiment as biosorbent material were obtained from the southeastern municipality of Curionópolis, state of Pará, Brazil. The material was prepared by drying açaí endocarps in an oven (Biopar S36 BD) at 65 ± 2 °C for 48 h, after which it was ground in an Wiley mill (Marconi MA 048) and sieved through 20–48 mesh for the standardization of particle size.

To determine the original concentrations of the metal ions Cd²⁺, Pb²⁺ and Cr³⁺ in biosorbent in nature as well as potassium (K), calcium (Ca), magnesium (Mg), copper (Cu), iron (Fe), manganese (Mn) and zinc (Zn) (AOAC International 2005) nitroperchloric digestion was performed and the elemental composition as determined by FAAS – flame atomic absorption spectrometry (Welz & Sperling 1999).

Biosorbent surface morphology was analyzed by an FEI Quanta 200 scanning electron microscope (SEM) at 30 kV. Infrared spectroscopy analyses determined the functional groups in the biosorbent before and after the adsorption process. A Shimadzu FTIR-8300 Fourier transform infrared spectrophotometer was employed in the 400 and 4,000 cm⁻¹ region, with 4 cm⁻¹ resolution. Structural characterization of the biosorbent under saturation conditions was performed to verify alterations of functional groups.

The point of zero charge (pH_PZC) was determined according to the methodology proposed by Mimura et al. (2010). The procedure to define the zero load point, i.e., the pH at which the surface of the solid has a neutral charge, was determined by preparing a solution of KCl in the concentration of 0.5 mol L⁻¹ with initial pH values from 2.0 to 8.0 by adjustment with NaOH and HCl at 0.1 mol L⁻¹. Then, 0.4 g of each adsorbent was added to 40 mL of solution and kept under constant stirring for 24 hours. Subsequently the final pH was measured. By plotting the values of ΔpH versus initial pH, we obtain the point of intercept of the curve with the x-axis, which corresponds to the material pH_PZC.

Contaminated single solute solutions with metal ions Cd(II), Pb(II) and Cr(III) were prepared from salts (Sigma-Aldrich) of cadmium nitrate [Cd(NO₃)₂4H₂O P.A. (para análise; Portuguese analysis grade) ≥ 99%], lead nitrate [Pb(NO₃)₂ P.A. ≥ 99%] and chromium nitrate III [Cr(NO₃)₃9H₂O P.A. ≥ 99%], respectively, diluted in type I ultrapure water produced by a Puritech Permution^® system.

All adsorption tests were performed in triplicate and performed in batch systems; concentrations of metal ions were determined by FAAS (Welz & Sperling 1999), stirring in Erlenmeyer flasks of 125 mL at 200 rpm, with 50 mL of contaminated single solute solutions.

Three pH conditions (4.0; 5.0; 6.0) were studied, for three basic reasons: according to pHPZC result (5.09), because adsorption of cations is theoretically favored by values above the pHPZC; also because of the pH of normal band of wastewaters, which is in many cases about 4.0 to 6.0; and also to avoid chemical precipitation of the metals in solution, which usually occurs at pH rates higher than 7.0.

The pH of contaminated solutions was adjusted with NaOH (Vetec, 99%) or HCl (Vetec, 37%) at a concentration of 0.1 mol L⁻¹. Increasing quantities of biosorbent mass, varying between 200 and 1,200 mg, were employed.

The obtained results were linearized by the mathematical models of pseudo-first order, as described by Ho & McKay (2004), pseudo-second order (Ho & Mckay 1999), Elovich, as described by Ho & McKay (2004), and intraparticle diffusion, as described by Yang & Al-Duri (2005).

The optimal conditions obtained in the previous tests were employed in the isotherms tests. In all batch experiments the same conditions were kept. Initial concentrations of metal ions ranged between 5 and 200 mg L⁻¹. The obtained results were linearized by Langmuir's (Langmuir 1916), Freundlich's (Freundlich 1906) and Dubinin–Radushkevich's (Dubinin & Radushkevich 1947) models.

The elution process was performed after the isotherm tests, using the obtained mass added with 50 mL of HCl (0.1 mol L⁻¹) with constant shaking at 200 rpm. The biosorbent material was then separated by filtration.

Five temperature values ranging between 15 and 55 °C were tested to verify the effect of temperature in the adsorption process, using 50 mL of contaminant solution at 50 mg L⁻¹ concentration of metal ion, The experimental conditions were, for Cd(II) adsorption, 400 mg of adsorbent (8 g L⁻¹) at solution pH 6.0; for Pb(II), 1,000 mg of adsorbent (20 g L⁻¹) at solution pH 5.0; and for Cr(III) adsorption test, 600 mg of adsorbent (12 g L⁻¹) at solution pH 4.0. All these experiments were performed with 60 min of contact time between adsorbent/adsorbate, according to the obtained optimum results.

The obtained values of Q_eq were employed in the estimative of thermodynamic parameters ΔG (Gibbs free energy), ΔH (enthalpy) and ΔS (entropy), as equations described by Sari et al. (2007), which indicate, respectively, the spontaneity of the adsorption process, endothermic or exothermic reactions, and the disorder of the process.

Açaí endocarp was evaluated in comparative studies with powdered activated carbon (Synth, Diadema, São Paulo state, Brazil) in the same experimental conditions. For this purpose the isotherm studies were undertaken.

Table 1 shows all mathematical models employed in the current research, all of them in the used linear form.

No Cd²⁺, Pb²⁺ or Cr³⁺ metal ions were detected in the evaluated biosorbent. Figure 1 shows the SEM images at an enlargement of 150× (a) and 12,000× (b).

Analysis of the images reveals that the biosorbent's surface is fibrous, irregular and with significant voids. It also shows a laminar structure with fissures and pores on the surface, which indicates that the material has rather favorable morphology for the adsorption of contaminants.

Before adsorption (Figure 2(a)) a large and strong 3,342 cm⁻¹ biosorbent band is observed, attributed to the vibration lengthening of the O-H link. The band characterizes vibration stretching of the hydroxyl group in cellulose, lignin and water adsorbed at the surface of the adsorbent (Feng et al. 2011). The 2,923 cm⁻¹ band refers to the vibration lengthening of C-H links of alkane groups, whereas the 1,735 cm⁻¹ band may be attributed to carbonyl groups of aldehyde and ketone functions in lignin and holocellulose (Pastore et al. 2004). Bands 1,631, 1,517 and 1,440 cm⁻¹ may be attributed to the vibration lengthening of C-O links of starches and carboxylic groups (Han et al. 2010). The 1,247 cm⁻¹ band may be associated with C-O stretching in phenols (Han et al. 2010). Wave length bands less than 800 cm⁻¹ may be attributed to N with bio-links (Barka et al. 2010), whilst 771 and 667 cm⁻¹ bands may be attributed to the vibration lengthening of the C-N link (Salem & Awwad 2011).

After the adsorption process (Figure 2(b)) there is a decrease in the intensity of the vibrations due to chemical reactions related to the adsorption process. In this way, bands still exist in the material after the biosorption process, suggesting the presence of alkane groups, carbonyl groups, aldehyde, ketone, carboxylic groups, phenols, and others which are constituents of lignin and cellulose macromolecules. Moreover, the literature shows that açaí endocarp is rich in lignin and cellulose (Pacheco-Palencia et al. 2009), corroborating the obtained results.

The possible functional groups found in adsorbent materials suggest that the physical adsorption may be favored, with physical interaction between these groups and metals.

Results for pH_PZC of the biosorbent are shown in Figure 3. According to Santhi et al. (2010), cation adsorption must be favored by solution pH values higher than the pHPZC, which in this study is 5.09.

Figure 4 exhibits some results for ideal adsorption conditions. In the case of Cd(II), removal percentage was higher, on average 90%, at pH 6.0. Similar results were obtained in studies employing Crambe abyssinica seeds pie (Rubio et al. 2013) as biosorbents. As the solution's pH increased, removal efficiency increased too.

Moreover, 400 mg of biosorbent mass in studies on Cd(II) was used, equivalent to 8 g of biosorbent per litre of water solution, since higher removal percentage were not found with mass increase. Similar results were obtained when biosorbent consisted of a Moringa oleifera seeds pie (Meneghel et al. 2013a).

Removal percentage of Pb(II) (Figure 4) was similar no matter the evaluated pH value (4.0, 5.0 or 6.0), although pH 5.0 was selected in later studies, because Pb may precipitate or complex into other forms in pH rates higher than 5.0 and thus affect the adsorptive process. Pb may have different forms at different pH conditions. In water solutions with pH < 6, the Pb ions may become Pb(II) and/or Pb(OH)⁺. The formation of Pb(II) hydrolysis products occurs in pH > 6.0 conditions and may lead towards polymerization (Reddy et al. 2010). The use of 1,000 mg, the equivalent of 20 g of biosorbent per litre of contaminated solution was selected with regard to the ideal mass of the biosorbent in terms of Pb(II) removal.

Another study using Moringa oleifera showed that the pH range between 3 and 6 showed maximum removal of Pb, higher than 98%, agreeing with the previously results (Tavares et al. 2015). Further, a mass of 600 mg was decided upon, or rather, the equivalent of 12 g of biosorbent per litre of contaminated solution.

There was a variation in removal percentage for pH conditions under analysis for Cr(III) (Figure 4(c)). Therefore, pH 4.0 was selected due to a higher removal percentage of Cr(III) at this value.

Figure 5 provides the results on the quantity of metal ions Cd(II), Pb(II) and Cr(III) adsorbed per mass unit of the adsorbent açaí endocarp according to time.

Results show an increase in adsorption rates over time; after 60 min the adsorption process enters into dynamic equilibrium, reaching the higher adsorption capacity.

According to Witek-Krowiak (2012) adsorption kinetics revealed a fast initial removal of metals in solutions, followed by a slower process. In fact, Figure 5 shows a higher adsorption rate in the initial minutes followed by a gradual stabilization. Most active sites of the adsorbent are initially available. Proportionally to their occupation of sites, the molecules in the solution are adsorbed with greater difficulty due to the repulsion forces between the molecules adsorbed in the solid and those still in the solution (Ibrahim 2010).

According to Meneghel et al. (2013b) the best mathematical adjustment depends on the obtained coefficients of determination (R²) and the proximity of the quantity adsorbed in equilibrium (Q_eq calc.) to that experimentally obtained (Q_eq exp.), i.e., when R² presents values close to 1, and when the values of Q_{eq calc.} and Q_{eq exp.} are close to each other, the proposed mathematical model represents with fidelity the observed adsorption process. The values of kinetic parameters are shown in Table 2.

The kinetics tests show best fit by the pseudo-second order model, according to the R² (0.999; 0.998; 0.994) and proximity between Q_eq calc (1.170; 0.491; 0.493) and Q_eq exp (1.120; 0.459; 0.450) indicating chemical characteristics in the adsorption process (Ho & McKay 1999).

The models of pseudo-first order, Elovich and intraparticle diffusion do not show satisfactory fit or correlation between Q_eq values.

The pseudo-second order kinetics describes well the processes of chemical adsorption, involving donation or exchange of electrons between the adsorbate and the adsorbent, as covalent and ion exchange forces (Ho & McKay 2004); in this type of adsorption, the molecules are not attracted by all the points of the surface of the solid, but specifically to the active centers, in order to form a single layer initially, and other layers can be formed by physisorption (Neta et al. 2012). The obtained results for kinetics studies suggests that chemisorption is the main process that regulates the adsorption of Cd(II), Pb(II) and Cr(III) by Euterpe oleracea Mart. biosorbent.

Such results demonstrate that the process of metals adsorption is more complex than imagined. The adsorbent material appears to be extremely heterogeneous; the results through the FTIR analysis suggest the occurrence of physical adsorption, and the results observed by the pseudo-second order model suggest the occurrence of chemisorption.

Isotherms were constructed from data obtained experimentally and linearized according to Langmuir's (Witek-Krowiak 2012), Freundlich's (Witek-Krowiak 2012) and Dubinin–Radushkevich's (D-R) (Farooq et al. 2011) models (Table 3).

Langmuir's and Freundlich's models showed best fit for Cd(II) and Cr(III) biosorption on açaí endocarp, with a coefficient of determination of 0.990 and 0.981. According to Fávere et al. (2010), Langmuir's model suggested adsorption in monolayers, and Freundlich's describe a multilayer sorption; in this specific case we observe the occurrence of both, showing that the adsorption mechanism of these metals is complex. Freundlich's showed best fit for Pb(II) (R² = 0.979), indicating multilayer adsorption. In the case of adsorption by activated carbon, Freundlich's showed the best fit for Cd(II) and Pb(II) (R² = 0.982 and 0.979), whereas Langmuir's showed best fit for Cr(III) (R² = 0.985), indicating multilayers of Cd(II) and Pb(II), while predominance of monolayers of Cr(III).

Langmuir's parameters demonstrate that rates of the highest adsorption quantity (Q_m) for Cd(II), Pb(II) and Cr(III) are higher for activated carbon (Table 3). It may also be perceived in the case of K_L, a constant related to the adsorbent/adsorbed interaction forces, higher values are found for biosorbent than activated carbon. Also, R_L values show that within the conditions in which adsorption tests were developed, the adsorption process was favorable in all cases since rates ranged between 0 and 1 (Lin & Juang 2002).

The parameter ‘n’ (from Freundlich's) indicates the reaction of the adsorbent's active sites. When ‘n’ rates are over 1, there is a strong indication of high energetic sites and suggests that they are the first to be occupied by the metals. Consequently, high energetic interaction and reactivity behavior may be observed for all metal ions under analysis in the biosorbent and in activated carbon.

With regard to D-R's mathematical model, the obtained values of R² indicate low correlation between the experimental data and the mathematical model; in this case the parameter values are underestimated or overestimated, i.e., cannot be used for interpretation of the adsorption process.

Table 4 gives the values of the estimated thermodynamic parameters ΔG, ΔH and ΔS.

The variation of Gibbs's free energy (ΔG) is related to the spontaneity of the process; enthalpy variation (ΔH) indicates whether the process is endothermal or exothermal; entropy variation (ΔS) is related to the system order after the adsorption process (Sari et al. 2007).

There was a gradual increase in the adsorbed quantity per biosorbent unit for metal ions Cd(II) and Cr(III), demonstrating the influence of temperature on the biosorption process. In the case of Pb(II) a decrease occurred in the adsorbed amount per adsorbent unit with the temperature increase.

The values of ΔH indicate an endothermic process for Cd(II) and Pb(II) (8.126 × 10⁻⁶ and 5.204 × 10⁻⁶ J mol⁻¹, respectively) and exothermic process for Cr(III) (−6.679 J mol⁻¹) (Wan Ngah & Hanafiah 2008; Wan Ngah & Fatinathan 2010).

Further, the obtained values of ΔG for Cd(II) and Pb(II) indicate a spontaneous adsorption process, while Cr(III) showed positive values, indicating a non-spontaneous process (Farooq et al. 2011).

The positive values of ΔS confirm that the process has greater randomness in the system (0.01, 0.03 and 0.04 J mol⁻¹, respectively for Cd, Pb and Cr), suggesting, according to Singha & Das (2011) and Sotirelis & Chrysikopoulos (2015), high affinity of the sorbent for the sorbate, which is an excellent result, indicating high affinity of these toxic metals for the studied biosorbent.

The obtained results indicate low rates for biosorbent recovery, especially when the biosorbent is used for Cr(III) removal (44.5; 45.47 and 1.12% for Cd, Pb and Cr, respectively).

In this way, the obtained data suggest a chemisorption of Cr(III), as in the work of Schwantes et al. (2016), which shows that due to the low elution rate there are strong bonds between the metals and the biosorbent material. In this case, the reuse of adsorbent materials for new adsorption processes is not feasible. However, in the case of Cd(II) and Pb(II), the use of different concentrations for HCl solution may be possible or solutions such as nitric acid (HNO₃) or sulfuric acid (H₂SO₄) for better elution results (Sekhar et al. 2004).

Results show that the use of the açaí endocarp as biosorbent is an alternative for the recovery of water contaminated by Cd(II), Pb(II) and Cr(III), since the material is natural, low-cost and highly available.

The obtained results indicate that the adsorption is a complex process, especially when biosorbents are employed, which due to their heterogeneity can indicate chemical or physical adsorption of metals, as is the case of the present study.

More studies with the biosorbent of açaí endocarp must be conducted, evaluating its potential in removal of other inorganic and organic pollutants from waters.