Fernanda Jorge Gonçalves

L V A Alves Gurgel

Liliane Catone Soares

Filipe Simões

Guilherme Max

Dias Ferreira

Yara Luíza Coelho

Henrique Luis

Damien Mendes Da Silva

L F Prim

Gil

Leandro Vinícius

Alves Gurgel

Max Dias Ferreira

Yara Luiza Coelho

Mendes Da Silva

Damien Prim

Laurent Frédéric Gil
email: laurent@ufop.edu.br

Application of pyridine-modified chitosan derivative for simultaneous adsorption of Cu(II) and oxyanions of Cr(VI) from aqueous solution

Keywords: one-step synthesis, pyridine-2-carbaldehyde, copper, chromium, Real Adsorbed Solution Theory, Corsel model. 1164

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Introduction

Many environmental and public health problems are related to the contamination of water resources [START_REF] Li | Crosslinked electro-spun chitosan nanofiber mats with Cd(II) as template ions for adsorption applications[END_REF][START_REF] Purkayastha | A comprehensive review on Cd(II) removal from aqueous solution[END_REF][START_REF] Wu | Electrospun chitosan nanofiber membrane for adsorption of Cu(II) from aqueous solution: Fabrication, characterization and performance[END_REF]. Metals are often found as major contaminants of aquatic systems, and can be highly toxic to humans and animals [START_REF] Teodoro | Synthesis and application of a new carboxylated cellulose derivative. Part I: Removal of Co 2+ , Cu 2+ and Ni 2+ from monocomponent spiked aqueous solution[END_REF][START_REF] Uddin | A review on the adsorption of heavy metals by clay minerals, with special focus on the past decade[END_REF][START_REF] Xin | Recyclable Saccharomyces cerevisiae loaded nanofibrous mats with sandwich structure constructing via bio-electrospraying for heavy metal removal[END_REF]. The main causes of contamination of water by toxic metals include industrial activities such as the manufacture of batteries, textiles, paints, and pesticides, as well as petroleum refining and mining operations [START_REF] O'connell | Heavy metal adsorbents prepared from the modification of cellulose: A review[END_REF][START_REF] Ramos | Modeling mono-and multicomponent adsorption of cobalt(II), copper(II), and nickel(II) metal ions from aqueous solution onto a new carboxylated sugarcane bagasse. Part I: Batch adsorption study[END_REF]. The toxic metals discharged by industries include cadmium, mercury, lead, chromium, copper, nickel, and zinc (Wan [START_REF] Ngah | Adsorption of dyes and heavy metal ions by chitosan composites: A review[END_REF].

Copper is widely used in electrical materials, alloys, fungicides, and herbicides, and is associated with industrial wastes, mining activities, and power generation [START_REF] Ayres | The Life Cycle of Copper, Its Co-Products and Byproducts[END_REF]. High concentrations of copper lead to health impacts including chronic or acute liver disease, neurological problems, and psychiatric disorders such as Wilson's disease [START_REF] Mulligan | Wilson Disease: An Overview and Approach to Management[END_REF]. Chromium is used in stainless steel and alloys, chrome plating, leather tanning, dyes and pigments, and wood preservation [START_REF] Morrison | Environmental Forensics: Contaminant Specific Guide[END_REF]. Cr(VI) is toxic and a well-known human carcinogenic. It causes damage to the immune, respiratory, gastrointestinal, reproductive, and hematological systems [START_REF] Wilbur | Toxicological profile for chromium[END_REF].

Cr(VI) and Cu(II) are common ions and generally coexist in wastewater, notably in discharges from the electroplating and tanning industries. For example, [START_REF] Sarkar | Study of hydrochemistry and pollution status of the Buriganga river, Bangladesh[END_REF] showed concern to analyze the concentrations chromium and copper in the Buriganga river (Bangladesh) due to the pollution caused by the tannery effluent. In addition to the tannery industry, copper is also emitted from the sewage pipe lines [START_REF] Sarkar | Study of hydrochemistry and pollution status of the Buriganga river, Bangladesh[END_REF]. Regarding this kind of waste, some works reported the use of photoreduction [START_REF] Yan | Simultaneous Removal of Cu(II) and Cr(VI) Ions from Wastewater by Photoreduction with TiO2-ZrO2[END_REF] and adsorption on carbonized crofton weed [START_REF] Chen | Study on adsorption of Cu(II)-Cr(VI) binary system by carbonized Eupatorium adenophorum[END_REF] and hyacinth shoot powder [START_REF] Sarkar | Remediation of chromium and copper on water hyacinth (E. crassipes) shoot powder[END_REF] for simultaneous removal of Cr(VI) and Cu(II). Copper and chromium are also present in the formulation of chromated copper arsenate (CCA), a wood preservative to avoid attack by termites and fungi (ATSDR, 2011). CCA is no longer used for residential construction but it still used for industrial and commercial constructions (NPIC, 2014). Since CCA is a water-soluble substance, there is a concern about water and soil contamination by leaching from CCA-treated wood (ATSDR, 2011).

Inefficient treatment of effluents contaminated with toxic metals in wastewater treatment plants (WWTPs) can cause long-term risks to ecosystems and humans. Various techniques have been used for removal of toxic metals in WWTPs, such as chemical precipitation, flocculation and coagulation, oxidation/reduction, and nanofiltration [START_REF] Mosa | Potential biotechnological strategies for the cleanup of heavy metals and metalloids[END_REF][START_REF] Purkayastha | A comprehensive review on Cd(II) removal from aqueous solution[END_REF][START_REF] Teodoro | Synthesis and application of a new carboxylated cellulose derivative. Part I: Removal of Co 2+ , Cu 2+ and Ni 2+ from monocomponent spiked aqueous solution[END_REF]. Adsorption may be used as a treatment or as a polishing technique in WWTPs, offering high efficiency and flexibility of operation [START_REF] Li | Removal of cadmium(II) cations from an aqueous solution with aminothiourea chitosan strengthened magnetic biochar[END_REF][START_REF] Silva-Yumi | Kinetics, adsorption and desorption of Cd(II) and Cu(II) on natural allophane: Effect of iron oxide coating[END_REF][START_REF] Xin | Recyclable Saccharomyces cerevisiae loaded nanofibrous mats with sandwich structure constructing via bio-electrospraying for heavy metal removal[END_REF]. As a polishing technique, adsorption can be used to achieve drinking water standards. According to the WHO, the provisional guideline values for Cr and Cu in drinking water are 0.05 and 2.0 mg L -1 , respectively (WHO, 1996a, b).

The availability of cost-effective, highly efficient, and environmentally friendly adsorbents is extremely important for the feasibility of adsorption techniques applied to treat water and wastewater [START_REF] Rahimi | Preparation of nanoparticlemodified polymeric adsorbent using wastage fuzzes of mechanized carpet and its application in dye removal from aqueous solution[END_REF][START_REF] Silva-Yumi | Kinetics, adsorption and desorption of Cd(II) and Cu(II) on natural allophane: Effect of iron oxide coating[END_REF][START_REF] Teodoro | Synthesis and application of a new carboxylated cellulose derivative. Part I: Removal of Co 2+ , Cu 2+ and Ni 2+ from monocomponent spiked aqueous solution[END_REF]. To this end, the use of adsorbents prepared from chemical modification of biopolymers has attracted attention in recent years [START_REF] Almeida | Application of a new bifunctionalized chitosan derivative with zwitterionic characteristics for the adsorption of Cu 2+ , Co 2+ , Ni 2+ , and oxyanions of Cr 6+ from aqueous solutions: Kinetic and equilibrium aspects[END_REF][START_REF] De Gisi | Characteristics and adsorption capacities of low-cost sorbents for wastewater treatment: A review[END_REF].

Polysaccharide-based biopolymers are a potential source of adsorbent materials.

Polysaccharides are widely found in nature, have varied molecular structures, and present a wide range of physicochemical properties that can be exploited for different applications [START_REF] Kurita | Controlled functionalization of the polysaccharide chitin[END_REF]. Among the many types of natural polysaccharides, cellulose and chitin are the most abundant [START_REF] Ahmad | Versatile nature of hetero-chitosan based derivatives as biodegradable adsorbent for heavy metal ions; a review[END_REF][START_REF] Almeida | Application of a new bifunctionalized chitosan derivative with zwitterionic characteristics for the adsorption of Cu 2+ , Co 2+ , Ni 2+ , and oxyanions of Cr 6+ from aqueous solutions: Kinetic and equilibrium aspects[END_REF]. Chitin is mainly isolated from shrimp or lobster carapaces, as well as from the cell walls of some fungi [START_REF] De Gisi | Characteristics and adsorption capacities of low-cost sorbents for wastewater treatment: A review[END_REF][START_REF] Kurita | Controlled functionalization of the polysaccharide chitin[END_REF]. The partial deacetylation of chitin results in the formation of chitosan, a polyaminosaccharide with glucose-like structures (2-amino-2-deoxy-β-Dglucose and 2-acetamido-2-deoxy-β-D-glucose units) connected by β(1→4) linkages [START_REF] Ahmad | Versatile nature of hetero-chitosan based derivatives as biodegradable adsorbent for heavy metal ions; a review[END_REF][START_REF] Kyzas | Chitosan adsorbents for dye removal: a review[END_REF]. The presence of hydroxyl and free amine groups in the chitosan structure provides excellent capacity of this material to act as a scavenger of metal ions, so it is a promising starting material for the synthesis of different adsorbents with improved properties [START_REF] Divya | Chitosan nanoparticles preparation and applications[END_REF][START_REF] Li | Removal of cadmium(II) cations from an aqueous solution with aminothiourea chitosan strengthened magnetic biochar[END_REF][START_REF] Wu | A review and experimental verification of using chitosan and its derivatives as adsorbents for selected heavy metals[END_REF]. Several recent studies have discussed the development of low-cost adsorbents based on biopolymers such as chitosan, as an alternative to synthetic polymers [START_REF] Ahmad | Versatile nature of hetero-chitosan based derivatives as biodegradable adsorbent for heavy metal ions; a review[END_REF][START_REF] De Gisi | Characteristics and adsorption capacities of low-cost sorbents for wastewater treatment: A review[END_REF].

The aim of the present study was to model the simultaneous adsorption of a cation and an anion using a versatile bioadsorbent. The present study is the first study to model the simultaneous adsorption of a cation and an anion using the Corsel model for kinetics and the Real Adsorbed Solution Theory (RAST) model for equilibrium data. These models provide a more in-depth analysis of the interactions involved in the simultaneous adsorption of Cu(II) and Cr(VI). It was employed a bioadsorbent, denoted C1, prepared by modification of chitosan with pyridine-2-carbaldehyde [START_REF] Goncalves | Synthesis, characterisation and application of pyridine-modified chitosan derivatives for the first non-racemic Cu-catalysed Henry reaction[END_REF]. The use of C1 is relevant, because it was prepared using a one-step synthesis employing a green solvent. C1 was subsequently used to remove Cr(VI) and Cu(II) from single and binary aqueous solutions.

Reuse of the spent adsorbent was also investigated. Isothermal titration calorimetry was used to understand the differences between the adsorption of Cu(II) and oxyanions of Cr(VI) on C1, with determination of the adsorption thermodynamic parameters.

Material and methods

Material

Chitosan (medium molecular weight, cat. no. 448877), pyridine-2-carbaldehyde, CuSO4•5H2O, and sodium chloroacetate (98%) were purchased from Sigma-Aldrich. K2Cr2O7, monochloroacetic acid (99%), CH3COONa•3H2O, Na2CO3, anhydrous CaCl2, NaH2PO4, Na2HPO4, and ethylenediaminetetraacetic acid (EDTA) were purchased from Synth (Brazil). Glycine was purchased from Isofar (Brazil). Glacial acetic acid (99.5%) was purchased from Neon (Brazil). Ethyl alcohol (99.8%) was purchased from Dinâmica (Brazil). HCl (37 wt.% in H2O) was purchased from Vetec (Brazil). Filter paper (quantitative, black ribbon, C-41, 12.5 cm diameter, 0.01% ash content, and grammage of 85 g m -2 ) was purchased from Unifil (Brazil).

The degree of acetylation (DA) of the chitosan was determined in a previous study of our research group [START_REF] Goncalves | Synthesis, characterisation and application of pyridine-modified chitosan derivatives for the first non-racemic Cu-catalysed Henry reaction[END_REF], using quantitative solid-state 13 C nuclear magnetic resonance (SS 13 C NMR) spectroscopy. The estimated DA value of the chitosan was 33 ± 2%.

Synthesis of C1

The synthesis of C1 was performed as described previously by [START_REF] Goncalves | Synthesis, characterisation and application of pyridine-modified chitosan derivatives for the first non-racemic Cu-catalysed Henry reaction[END_REF].

Chitosan (5 g) was added to a 500 mL round-bottom flask, together with 0.525 mols of pyridine-2-carbaldehyde (50 mL) dissolved in 125 mL of ethyl alcohol (99.8%). A reflux condenser with a drying tube filled with anhydrous CaCl2 was attached to the flask. The suspension was heated at 80.0 ºC for 18 h, under gentle agitation (300 rpm) in an oil bath (Model PC-420, Corning ® ). Subsequently, the cooled suspension was filtered under reduced pressure, using a sintered glass funnel (porosity 3), followed by washing with ethyl alcohol (95%), distilled water, ethyl alcohol (95%), and diethyl ether. The C1 obtained was dried in an oven (Model 400/3ND, Nova Etica) at 70.0 ºC for 20 min.

Characterization of C1

Elemental and spectroscopic analyses

Elemental carbon, hydrogen, and nitrogen analyses of the chitosan and C1 were performed using an elemental CHNS/O analyzer (Model 2400 Series II, Perkin-Elmer).

Before analysis, the materials were dried at 85.0 ºC in an oven for 1 h. The analyses were performed in duplicate. Procedures used for characterization of the chitosan and C1 by Fourier transform infrared (FTIR) and SS 13 C NMR spectroscopies were reported by [START_REF] Goncalves | Synthesis, characterisation and application of pyridine-modified chitosan derivatives for the first non-racemic Cu-catalysed Henry reaction[END_REF].

Surface analyses

The pH of zero charge (pHPZC) of C1 was determined by the method of [START_REF] Noh | Effect of HNO3 treatment on the surface-acidity of activated carbons[END_REF]. Aqueous 0.10 mol L -1 NaNO3 solutions (150 mL) were prepared and the pH of each solution was adjusted to 3.00, 6.00, or 11.00 by adding drops of aqueous HNO3 (0.1 mol L -1 ) or NaOH (0.1 mol L -1 ) solutions. Aliquots of 20.00 mL of each NaNO3 solution at pH 3.00, 6.00, or 11.00 were then added to 125 mL Erlenmeyer flasks to prepare aqueous suspensions of 0.05, 0.1, 0.5, 1.0, and 2.0% (w v -1 ) of C1. The flasks were stirred at 130 rpm and 25.0 ºC for 24 h in an orbital shaker incubator Tecnal). At the end of the experiment, the equilibrium pH of each suspension was measured using a pH meter (Model HI 223,Hanna Instruments). The convergence point of the three curves of equilibrium pH against C1 concentration (w v -1 ) gave the PZC value.

The surfaces of the chitosan and C1 were analyzed by scanning electron microscopy (SEM) (Model 6510, JEOL). The materials were dried in an oven for 1 h at 80.0 ºC, before metallization with a thin layer of carbon graphite (Model JEE-4C, JEOL).

The textural properties of C1 were determined using N2 adsorption and desorption isotherms obtained using a pore and surface area analyzer (Model Nova 1200e, Quantachrome). C1 was degassed at 60.0 ºC for 24 h before analysis. The specific surface area was determined by the method of [START_REF] Brunauer | Adsorption of gases in multimolecular layers[END_REF]. The maximum pore diameter was determined by the method of [START_REF] Barrett | The Determination of Pore Volume and Area Distributions in Porous Substances. I. Computations from Nitrogen Isotherms[END_REF].

Adsorption experiments

The C1 adsorbent was used to adsorb oxyanions of Cr(VI) and Cu(II) from spiked aqueous solutions in batch mono-and bicomponent systems. The adsorption experiments were performed in duplicate, using the experimental conditions described in Table 1. The pH values and buffer solutions were chosen considering the solubility of Cu(II) and Cr(VI) in each buffer solution [START_REF] Almeida | Application of a new bifunctionalized chitosan derivative with zwitterionic characteristics for the adsorption of Cu 2+ , Co 2+ , Ni 2+ , and oxyanions of Cr 6+ from aqueous solutions: Kinetic and equilibrium aspects[END_REF] (see section 4.2.1). The equilibrium pH of each solution was measured using a pH meter (Model HI 223,Hanna Instruments).

All flasks (250 mL Erlenmeyers) containing C1 and solute solutions were stirred in an orbital shaker incubator (Model MA-830, Marconi), followed by a single filtration (C-41 (20 μm) filter paper) to separate the spent C1 adsorbent and the liquid phase. The liquid phases were analyzed by flame atomic absorption spectrophotometry (FAAS) (Model SpectrAA 50B, Varian) (λCu = 324.7 nm, λCr = 425.4 nm) for determination of the Cr(VI) and Cu(II) concentrations [START_REF] Elias | Synthesis and application of sugarcane bagasse cellulose mixed esters. Part I: Removal of Co 2+ and Ni 2+ from single spiked aqueous solutions in batch mode using sugarcane bagasse cellulose succinate phthalate[END_REF]. The FAAS analyses were performed in triplicate.

The adsorption capacity (q) of C1 for oxyanions of Cr(VI) or Cu(II) was determined as follows:

(1) where, C0 (mmol L -1 ) is the initial concentration of oxyanions of Cr(VI) or Cu(II) in the aqueous solution, Cx (mmol L -1 ) is the concentration of oxyanions of Cr(VI) or Cu(II) at time t or equilibrium, V (L) is the volume of Cr(VI) or Cu(II) aqueous solution, and wC1 (g) is the weight of C1.

Table 1

Isothermal titration calorimetry (ITC)

Isothermal titration calorimetry (ITC) experiments were conducted for single adsorption of Cr(VI) (at pH 3.6) and Cu(II) (at pH 5.5), using an Isothermal Titration Nanocalorimeter (Model TAM III, TA Instruments, USA) controlled by dedicated TAM Assistant™ software and equipped with two 4.00 mL reaction cells (sample and reference). Using a Hamilton syringe (500 μL) controlled by a piston pump, stepwise 20 μL injections of concentrated buffered aqueous solutions of the metal ions (500.0 mg Cr(VI) L -1 or 270.0 mg Cu(II) L -1 ) were titrated against a mixture of 8.00 mg

( ) 0 -1 1 / (mmol g ) x C C C V q w - =
of C1 and 2.70 mL of buffer solution in the reaction cell. The reference cell was filled with the same buffer solution, without the adsorbent. During titration, the time interval used between consecutive injections was 60 min and a propeller stirrer operating at 180 rpm was used to ensure homogenization of the suspension inside the reaction cell. Control experiments were performed by i) adding the metal ion solution to the buffer solution in the absence of C1, and ii) adding the buffer solution to the mixture of adsorbent and buffer solution, in order to discount the heat effect associated with the dilutions of the metal ion solutions and C1 during the adsorption processes. The measurements were performed at a temperature of 25.0000 ± 0.0001 ºC. The solutions were degassed for 10 min, prior to the titration experiments, in order to avoid bubble formation in the system. Each titration was performed in duplicate.

The change in enthalpy of adsorption for the metal ion adsorption on C1 (∆adsH)∆ !"# H, associated with the i-th injection in the titration experiment, was calculated as follows:

(2) where, qi q $ and qi,dilq $,"$& (kJ) are the energies absorbed or released in the sample reaction cell due to the titration processes in the presence of metal ions (Cr(VI) or Cu(II)) and adsorbent, and in the absence of metal ions or adsorbent, respectively, and ni (mol) is the amount of metal ions adsorbed on C1 during the same injection.

Thermodynamic parameters of adsorption

The approach used for determination of the changes in the standard free energy of adsorption (ΔadsGº) for adsorption of Cu(II) and oxyanions of Cr(VI) on C1 was that described by [START_REF] Liu | Is the free energy change of adsorption correctly calculated?[END_REF], as follows:

,dil -1 ads / (kJ mol )

i i i q q H n - D = (3)
where, R is the gas constant (8.314 J K -1 mol -1 ), T (K) is the absolute temperature, and γe is the equilibrium activity coefficient.

The value of γe can be calculated from the extended Debye Hückel law [START_REF] Debye | Zur Theorie der Elektrolyte. I. Gefrierpunktserniedrigung und verwandte Erscheinungen[END_REF], as follows:

(4)

where, z is the charge of the ion, Ie (mol L -1 ) is the ionic strength at equilibrium, and α (pm) is the hydrated ion size (αCu 2+ = 419 pm, αHCrO 4 -= 375 pm) [START_REF] Nightingale | Phenomenological theory of ion solvation. Effective radii of hydrated ions[END_REF].

To obtain the changes in the standard enthalpy of adsorption (ΔadsH°) for adsorption of

G H T S D °=D °-D °
6 tons, to obtain discs 13 mm in diameter. The discs were metalized with a thin layer of carbon graphite (Model JEE-4C, JEOL) before analysis. The surfaces of the materials were mapped using a scanning electron microscope (Model 6510, JEOL) equipped with an EDX spectrometer (Model X-Max, Oxford Instruments).

Desorption and reuse of spent adsorbent

The experiments of adsorption and desorption were carried out using the experimental conditions described in Table 2. After desorption, C1 loaded with Cr(VI) or Cu(II) was recovered by single filtration, washed with an excess of ultrapure water, and dried in an oven at 80.0 ºC for 6 h [START_REF] Elias | Synthesis and application of sugarcane bagasse cellulose mixed esters. Part I: Removal of Co 2+ and Ni 2+ from single spiked aqueous solutions in batch mode using sugarcane bagasse cellulose succinate phthalate[END_REF]. The other procedures were the same as described in Section 2.4. The desorption efficiency (Edes) was determined as follows [START_REF] Elias | Synthesis and application of sugarcane bagasse cellulose mixed esters. Part I: Removal of Co 2+ and Ni 2+ from single spiked aqueous solutions in batch mode using sugarcane bagasse cellulose succinate phthalate[END_REF]:

(6)
where, Qmax (mg g -1 ) is the maximum adsorption capacity determined for Cr(VI) or Cu(II), and w'C1 (g) is the weight of C1 in C1 loaded with Cr(VI) or Cu(II) (wC1,M).

The value of wC1,M was determined as follows [START_REF] Elias | Synthesis and application of sugarcane bagasse cellulose mixed esters. Part I: Removal of Co 2+ and Ni 2+ from single spiked aqueous solutions in batch mode using sugarcane bagasse cellulose succinate phthalate[END_REF]:

(7)
The experiments of re-adsorption were carried out using the experimental conditions described in Table 2. The other procedures were the same as described in Section 2.4. / % 100 '

C V E Q w ae ö = ḉ ÷ è ø C1,M C1 C1 max 1 C1 ' / g 1000 C w w w Q w w = ae ö + ç ÷ è ø
The re-adsorption efficiency (Ere-ads) was determined as follows [START_REF] Elias | Synthesis and application of sugarcane bagasse cellulose mixed esters. Part I: Removal of Co 2+ and Ni 2+ from single spiked aqueous solutions in batch mode using sugarcane bagasse cellulose succinate phthalate[END_REF]:

(8)
where, Qre-ads,max (mg g -1 ) is the maximum adsorption capacity of C1 determined after desorption.

The value of Qre-ads,max was obtained as follows [START_REF] Elias | Synthesis and application of sugarcane bagasse cellulose mixed esters. Part I: Removal of Co 2+ and Ni 2+ from single spiked aqueous solutions in batch mode using sugarcane bagasse cellulose succinate phthalate[END_REF]):

(9)

Modeling of the adsorption data

Monocomponent adsorption

The data for adsorption of Cu(II) and oxyanions of Cr(VI) on C1, as a function of contact time, were modeled using pseudo-first order [START_REF] Lagergren | Zur theorie der sogenannten adsorption gelöster stoffe, kungliga svenska vetenskapsakademiens[END_REF] and pseudo-second order models [START_REF] Ho | Pseudo-second order model for sorption processes[END_REF]. The mechanism involved in the adsorption of Cu(II) and oxyanions of Cr(VI) on C1 was investigated using the intraparticle diffusion (IPD) [START_REF] Weber | Kinetics of adsorption on carbon from solution[END_REF] and [START_REF] Boyd | The exchange adsorption of ions from aqueous solutions by organic zeolites[END_REF] models. The data for adsorption of oxyanions of Cr(VI) and Cu(II) on C1, as a function of initial solute concentration, were modeled using the [START_REF] Langmuir | The adsorption of gases on plane surfaces of glass, mica and platinum[END_REF], [START_REF] Sips | On the structure of a catalyst surface[END_REF], and [START_REF] Redlich | A useful adsorption isotherm[END_REF] models.

Microcal OriginPro ® 2015 software was used to perform nonlinear regression (NLR)

analysis of the monocomponent adsorption data and to estimate the parameters of the kinetic and equilibrium models. The reduced chi-square (χ 2 red) and residual sum of squares (RSS) error functions were used.

re-ads,max re-ads max

/ % 100 Q E Q ae ö = ḉ ÷ è ø ( )( ) ( ) C1,M C1 des e -1 re-ads C1 ' 1 100 / (mg g ) ' w w E C C V Q w é ù - - - - é ù ë û ë û =
The equations of the kinetic and equilibrium models as well as the error functions can be found in the Supplementary Material.

Bicomponent adsorption

The data for the simultaneous adsorption of Cu(II) and oxyanions of Cr(VI) on C1, as a function of contact time, were modeled using the model of [START_REF] Corsel | The role of intrinsic binding rate and transport rate in the adsorption of prothrombin, albumin, and fibrinogen to phospholipid bilayers[END_REF]. The data for simultaneous adsorption of Cu(II) and oxyanions of Cr(VI) on C1, as a function of initial solute concentration, were modeled using the real adsorbed solution theory model (RAST) [START_REF] Costa | Adsorption of binary and ternary hydrocarbon gas mixtures on activated carbon: Experimental determination and theoretical prediction of the ternary equilibrium data[END_REF][START_REF] Myers | Activity coefficients of mixtures adsorbed on heterogeneous surfaces[END_REF][START_REF] Talu | Multicomponent adsorption equilibria of nonideal mixtures[END_REF]. The equations of the Corsel and RAST models were those reported by [START_REF] Teodoro | Synthesis and application of a new carboxylated cellulose derivative. Part II: Removal of Co 2+ , Cu 2+ and Ni 2+ from bicomponent spiked aqueous solution[END_REF]2018). MATLAB ® 2010a software (Mathworks Inc., Massachusetts) was used to model the bicomponent adsorption data and estimate the parameters of the kinetic and equilibrium models. The RSS error function was used. The computational methods used to solve the equations of the [START_REF] Corsel | The role of intrinsic binding rate and transport rate in the adsorption of prothrombin, albumin, and fibrinogen to phospholipid bilayers[END_REF] and RAST [START_REF] Costa | Adsorption of binary and ternary hydrocarbon gas mixtures on activated carbon: Experimental determination and theoretical prediction of the ternary equilibrium data[END_REF][START_REF] Myers | Activity coefficients of mixtures adsorbed on heterogeneous surfaces[END_REF][START_REF] Talu | Multicomponent adsorption equilibria of nonideal mixtures[END_REF]) models were those reported by [START_REF] Teodoro | Synthesis and application of a new carboxylated cellulose derivative. Part II: Removal of Co 2+ , Cu 2+ and Ni 2+ from bicomponent spiked aqueous solution[END_REF]2018).

Results and discussion

Synthesis and characterization of C1

Figure 1 shows the synthesis scheme for preparation of C1 from the reaction between chitosan and pyridine-2-carbaldehyde. It involved only one step and used ethanol as a green solvent. This synthesis was first reported by our research group [START_REF] Goncalves | Synthesis, characterisation and application of pyridine-modified chitosan derivatives for the first non-racemic Cu-catalysed Henry reaction[END_REF]. The characterization of the chitosan and C1 by Fourier transform infrared (FTIR) and SS 13 C NMR spectroscopies were reported by [START_REF] Goncalves | Synthesis, characterisation and application of pyridine-modified chitosan derivatives for the first non-racemic Cu-catalysed Henry reaction[END_REF].

The C, H, and N elemental analysis of the materials showed that the chitosan and C1 presented carbon, hydrogen, and nitrogen contents of 41 ± 1 and 49 ± 1%, 7.4 ± 0.2 and 6.2 ± 0.2%, and 7.0 ± 0.2 and 9.0 ± 0.2%, respectively. The contents of carbon and nitrogen increased, while the content of hydrogen decreased, after modification of the chitosan with pyridine-2-carbaldehyde (C = 67.3%, H = 4.71%, N = 13.1%). This indicated that the introduction of pyridine moiety on the biopolymer chain was successfully accomplished.

The nitrogen atoms of the imine, pyridine, and remaining amine groups are involved in the adsorption interaction with both species, Cu(II) and Cr(VI), as will be discussed in section 4.2.

Figure 1

The pH of zero charge (pHPZC) of C1 was determined by the convergence point of three curves of pH (pHi of 3.00, 6.00, and 11.00) plotted against the C1 concentration (w v -1 ) (Figure not shown), obtaining a value of 7.6 ± 0.8. At pH < pHPZC, the surface of C1 is positively charged, due to protonation of the nitrogen atoms of imine, pyridine, and remaining amine groups not modified with pyridine-2-carbaldehyde. Therefore, it is expected that the adsorption of anionic species, such as HCrO4 -, CrO4 2-, and Cr2O7 2-, should be favored at pH < pHPZC. Contrarily, the adsorption of cationic species, such as Cu 2+ and CuOH + , should be favored with increase of the pH, with the nitrogen atoms of the imine, pyridine, and remaining amine groups being deprotonated, hence decreasing the positive charge of the C1 surface, as will be discussed in subsection 4.2.1.

Figure 2 presents SEM images of the chitosan and C1 at 60× and 3,000× magnifications.

As can be seen in Figures 2a and2b (60× magnification), the physical aspect of the C1 particles appeared to be unchanged after chemical modification of the chitosan with pyridine-2-carbaldehyde. However, the SEM images at 3,000× magnification (Figures 2b and2d) revealed that the surface texture of C1 was significantly different from the chitosan surface texture. The C1 surface was rougher than the chitosan surface, indicating that it had been chemically modified by the grafting of pyridine-2-carbaldehyde molecules. In addition, the C1 surface presented some cracks, indicating that the C1 particles swelled after chemical modification with pyridine-2-carbaldehyde.

Figure 2

The specific surface areas of the chitosan and C1 were 19 m 2 g -1 , the average diameter of micropores were 20 Å while the maximum pore diameters were 444 and 595 Å, respectively. Therefore, chitosan and C1 also present meso and macropores, respectively. These results showed that the chemical modification of chitosan with pyridine-2carbaldehyde did not change the specific surface area of C1, compared to the nonmodified chitosan. Contrarily, the maximum pore diameter increased after modification of the chitosan. To know the distribution of micro, meso, and macropores is important for the evaluation of ion diffusion and ion transportation process from the solution bulk to porous structure of the C1 adsorbent (subsections 4.2.2 and 4.3.2).

The average particle size was 0.5 mm and no disintegration or swelling of the C1 particles was observed during the adsorption experiments described in the following sections.

Monocomponent adsorption of Cu(II) and oxyanions of Cr(VI) on C1

Adsorption of Cu(II) and oxyanions of Cr(VI) on C1, as a function of solution pH

Figure 3a shows the changes in equilibrium adsorption capacity (qe), as a function of solution pH, for the adsorption of Cu(II) and oxyanions of Cr(VI) on C1.

Figure 3

At low pH (pH < 3.5), the nitrogen atoms of imine, pyridine, and remaining amine groups on C1 (pHPZC = 7.6 ± 0.8) are protonated (pKa,imine = 5-7, pKa,pyridine = 5.2), so Cu(II) adsorption was not observed (Figure 3a). From pH 4.0, the value of qe for Cu(II) adsorption augmented with increasing solution pH up to pH 5.5, because the nitrogen atoms of the imine, pyridine, and remaining amine groups became deprotonated as the solution pH increased. This enabled interaction between the lone electron pairs of nitrogen atoms and the Cu(II) ions (Figure 1b, C1-Cu 2+ ). The adsorption of Cu(II) was not evaluated at pH higher than 5.5, due to the formation of hydrolyzed Cu(II) species, such as Cu(OH) + and Cu(OH)2 (Eqs. ( 17)-( 20)).

Cr(VI) can form various species in aqueous solution, such as H2CrO4, HCrO4 -, CrO4 2-, and Cr2O7 2-, depending on the total Cr(VI) concentration, pH, and ionic strength (I) of the solution. Supplementary Figure 1 presents graphs of the fraction of Cr(VI) species, as a function of solution pH from 0 to 10, for total Cr(VI) concentrations of 0.77 and 3.85 mmol L -1 . At a total Cr(VI) concentration of 0.77 mmol L -1 (I = 0.05 mol L -1 ), the HCrO4 -species (fraction of ~0.9) predominates over the Cr2O7 2-species (fraction of ~0.1) in the pH range from 1 to 5. At pH 1.0, the HCrO4 -species (fraction of ~0.85) still predominates over Cr2O7 2-(fraction of ~0.10) and H2CrO4 (fraction of ~0.05). Contrarily, as the solution pH increased from 5 to 8, the CrO4 2-fraction increased from ~0.10 to 1.0, predominating over HCrO4 -(which decreased from ~0.9 to 0) and Cr2O7 2-(which decreased from ~0.1 to 0). At low pH (pH < 4), the nitrogen atoms of the imine, pyridine, and remaining amine groups on C1 are protonated, resulting in strong electrostatic attraction between the positively charged C1 surface and the negatively charged oxyanions of Cr(VI) (HCrO4 - and Cr2O7 2-) (Figure 1b). This explains the higher value of qe for Cr(VI) adsorption at pH 3.5 (Figure 3a). At pH lower than 3.5, competition between HCrO4 -and Cr2O7 2-for C1 surface sites, together with repulsive lateral interactions between adsorbed Cr(VI) species, could have contributed to decreasing the value of qe for Cr(VI) adsorption.

Anions with higher charge density and multivalent anions are more strongly adsorbed by electrostatic attraction [START_REF] Lv | Factors influencing the removal of fluoride from aqueous solution by calcined Mg-Al-CO3 layered double hydroxides[END_REF]. The charge/radius (Z/r) ratio of Cr2O7 2-(2/2.92) [START_REF] Haynes | CRC Handbook of Chemistry and Physics[END_REF] is higher than that of HCrO4 -(1/2.42) [START_REF] Motzer | Chemistry, Geochemistry, and Geology of Chromium and Chromium Compounds[END_REF], suggesting that Cr2O7 2-is preferentially adsorbed on the C1 surface in the pH range from 2 to 4, in the presence of HCrO4 -. As the solution pH was increased from 3.5 to 8, the nitrogen atoms of the imine, pyridine, and remaining amine groups on C1 were gradually deprotonated, hence decreasing the electrostatic attraction between the C1 surface and the oxyanions of Cr(VI) (HCrO4 -, CrO4 2-, and Cr2O7 2-). At pH higher than 7 (pHPZC = 7.6 ± 0.8), the adsorption of Cr(VI) species (HCrO4 -and CrO4 2-) was close to zero, because the C1 surface was almost deprotonated.

Therefore, the subsequent studies of adsorption of Cr(VI) and Cu(II) species on C1 were carried out at the pH values of maximum adsorption. As pointed out by Wan [START_REF] Ngah | Adsorption of dyes and heavy metal ions by chitosan composites: A review[END_REF], the solubility and swelling properties of raw chitosan are the main existing bottlenecks for its application as an adsorbent. On the other hand, C1 stability (solubility and swelling) was not affected in the pH range studied. This is an advantage of C1 in comparison to raw chitosan, which was soluble in the acidic pH values tested in the present study.

Adsorption of Cu(II) and oxyanions of Cr(VI) on C1, as a function of contact time

Figures 3b and3c show the change in adsorption capacity (qt), as a function of contact time, for the adsorption of Cu(II) and oxyanions of Cr(VI) on C1, respectively. In Table 3 are and Cu(II) on C1. As can be seen in Figures 3b and3c, qe was reached at 240 and 360 min for the adsorption of Cu(II) and oxyanions of Cr(VI) on C1, respectively.

According to [START_REF] Plazinski | Modeling of sorption kinetics: the pseudosecond order equation and the sorbate intraparticle diffusivity[END_REF], the PSO model can be interpreted in terms of surface reaction models or in terms of the intraparticle diffusion model. The first consider that the transfer of adsorbate throughout the solution/solid interface is the slowest step in the entire adsorption process. The second considers that the overall adsorption rate is controlled by the rate of adsorbate diffusion within the pores of the adsorbent [START_REF] Plazinski | Modeling of sorption kinetics: the pseudosecond order equation and the sorbate intraparticle diffusivity[END_REF]. On the other hand, the PFO model can be interpreted considering that the adsorption kinetics is determined by the rate of diffusional transport of a solute [START_REF] Plazinski | Theoretical models of sorption kinetics including a surface reaction mechanism: A review[END_REF] as suggested by [START_REF] Boyd | The exchange adsorption of ions from aqueous solutions by organic zeolites[END_REF]. This model is a film diffusion model represented by an equation with the same analytical form as the PFO model

Table 3

The mechanisms of adsorption of Cu(II) and oxyanions of Cr(VI) on C1 were evaluated from the Boyd and intraparticle diffusion plots. These graphs are available in the Supplementary Material (Supplementary Figures 2 and3). The intraparticle diffusion plots for the adsorption of oxyanions of Cr(VI) and Cu(II) on C1 showed two and three stages, respectively. The straight lines representing the first stages did not intersect the origin (C ≠ 0), indicating that the adsorption was influenced by the diffusion of the ions through the thin solvent layer surrounding the C1 particles. Two stages were observed for Cu(II) adsorption, reflecting a shift from film diffusion (first stage) to intraparticle diffusion (second stage), after 10 min.

The Boyd plots for adsorption of Cu(II) and oxyanions of Cr(VI) on C1 were linear for f < 0.85 and presented intercept values close to zero, suggesting that external mass transfer of solute through the thin solvent layer affected the adsorption of both ions on C1. The effective diffusion coefficients (Di) (Table 3) for adsorption of Cu(II) and oxyanions of Cr(VI) on C1 were of the same order of magnitude (10 -11 m 2 min -1 ), with Cr(VI) ions diffusing 4-fold faster than Cu(II) ions from the bulk solution to the C1 external surface. Although Cr(VI) ions are heavier than Cu(II) ions, the diffusion of Cr(VI) ions was faster than the diffusion of Cu(II) ions. This behavior may be explained by the larger hydrated ion size (α) of the Cu(II) ion (αCu 2+ = 419 pm, αHCrO 4 -= 375 pm, [START_REF] Nightingale | Phenomenological theory of ion solvation. Effective radii of hydrated ions[END_REF].

Adsorption of Cu(II) and oxyanions of Cr(VI) on C1, as a function of initial solute concentration

Adsorption isotherms are of fundamental importance for providing relevant information about adsorption systems. The isotherm represents the adsorption behavior of a solute on an adsorbent, according to increasing solute concentration, at constant temperature and pH. The adsorption isotherm is also used to estimate the maximum adsorption capacity (Qmax) of a solute on an adsorbent. Various isotherm models have been proposed for fitting the equilibrium data in the form of a plot of qe against Ce. Some model equations have two or more adjustable parameters, such as those of the [START_REF] Langmuir | The adsorption of gases on plane surfaces of glass, mica and platinum[END_REF], [START_REF] Sips | On the structure of a catalyst surface[END_REF], and Redlich and Peterson (1959) (R-P) models.

Figures 3d and3e present plots of qe against Ce for the adsorption of Cu(II) and oxyanions of Cr(VI) on C1, respectively. The isotherm models that best described the adsorption of Cu(II) on C1 were the Langmuir and Sips models. The values of the adjustable parameters obtained by modeling the equilibrium data using the Langmuir, R-P, and Sips models are presented in Table 3. These models presented higher R 2 values and lower χ 2 red values (Table 3). The parameter n of the Sips isotherm reflects the heterogeneity of an adsorption system. The value of n for Cu(II) adsorption on C1 was close to unity, suggesting that the Sips isotherm model could be reduced to the Langmuir isotherm model. The Langmuir model is based on premises that are not valid for the system investigated in the present study. Nevertheless, Langmuir model is as a suitable mathematical descriptor to estimate the maximum adsorption capacity. Aspects related to the heterogeneity of the adsorption sites will be discussed in more in-depth in thermodynamic studies (subsection 4.2.4).

The Sips model provided the best description of the adsorption of oxyanions of Cr(VI) on C1, with higher R 2 values and lower χ 2 red values (Table 3). Since the value of n was much smaller than unity, the Sips isotherm model could not be reduced to the Langmuir isotherm model for Cr(VI) adsorption.

Considering that Cu(II) and Cr(VI) were adsorbed on the same adsorbent (C1), the results suggested that: 1) Cu(II) adsorption occurred on homogeneous sites, and 2) Cr(VI) adsorption did not occur on homogeneous sites. Hypothesis 1 is compatible with the formation of inner-sphere complexes, which requires a particular electronic configuration of the adsorbent (specific sites) and the adsorbate. Hypothesis 2 is compatible with the adsorption of different Cr(VI) species.

The value of Qmax for adsorption of oxyanions of Cr(VI) on C1 was 2-fold higher than the value of Qmax for adsorption of Cu(II) on C1. A possible explanation for this result is that adsorption of Cu(II) on the C1 surface may have been occurred by the formation of bidentate inner-sphere complexes with nitrogen atoms of imine and pyridine groups (Figure 1b) [START_REF] Brown | Sorption at mineral-water interfaces: Macroscopic and microscopic perspectives[END_REF][START_REF] Sposito | The Chemistry of Soils[END_REF]. On the other hand, within the Cr(VI) concentration range studied (0.15-7 mmol L -1 ), HCrO4 -species prevailed over Cr2O7 2- species. This suggests the possible formation of outer-sphere complexes between two HCrO4 -species and positively charged nitrogen atoms of imine and pyridine groups (Figure 1b) [START_REF] Brown | Sorption at mineral-water interfaces: Macroscopic and microscopic perspectives[END_REF][START_REF] Sposito | The Chemistry of Soils[END_REF]. C1 presented a higher Qmax than other bioadsorbents reported in the literature [START_REF] Chen | Study on adsorption of Cu(II)-Cr(VI) binary system by carbonized Eupatorium adenophorum[END_REF][START_REF] Dong | A novel method for amino starch preparation and its adsorption for Cu(II) and Cr(VI)[END_REF]. For example, [START_REF] Chen | Study on adsorption of Cu(II)-Cr(VI) binary system by carbonized Eupatorium adenophorum[END_REF] [START_REF] Dong | A novel method for amino starch preparation and its adsorption for Cu(II) and Cr(VI)[END_REF]. In a previous study, [START_REF] Almeida | Application of a new bifunctionalized chitosan derivative with zwitterionic characteristics for the adsorption of Cu 2+ , Co 2+ , Ni 2+ , and oxyanions of Cr 6+ from aqueous solutions: Kinetic and equilibrium aspects[END_REF] reported the synthesis of an efficient adsorbent by quaternization of the amine group of chitosan and esterification of -OH groups with EDTA dianhydride. This chitosan derivative showed Qmax values of 0.698 and 1.91 mmol g -1 for adsorption of Cu(II) (pH 4.5, 25 ºC) and Cr(VI) (pH 2.0, 25 ºC), respectively. Table 4 shows different adsorbent materials that have been applied for the removal of both Cu(II) and Cr(VI) from aqueous solution.

The Langmuir constant, b, reflected the affinity of the C1 adsorption surface sites for oxyanions of Cr(VI) or Cu(II). The value of b was much higher for adsorption of Cu(II) than for adsorption of Cr(VI), which was in agreement with the hypotheses raised.

As discussed previously, Cr(VI) can form various species in aqueous solution (Supplementary Figure 1), depending on the chemical conditions of the solution. The speciation of Cr also depends on the redox conditions (solution Eh). The reduction of Cr(VI) to Cr(III) can occur under specific conditions that depend on the presence of light irradiation or substances that can promote reduction. For example, [START_REF] Fida | Preparation and characterization of bifunctional Ti-Fe kaolinite composite for Cr(VI) removal[END_REF] employed a bifunctional Ti-Fe kaolinite composite with adsorption and photocatalytic properties to remove Cr(VI) from water. According to [START_REF] Fida | Preparation and characterization of bifunctional Ti-Fe kaolinite composite for Cr(VI) removal[END_REF], the reduction of Cr(VI) to Cr(III) was promoted by visible light irradiation, associated with TiO2 and the Fe(III)/Fe(II) redox cycle. [START_REF] Wang | A novel cellulose hydrogel coating with nanoscale Fe 0 for Cr(VI) adsorption and reduction[END_REF] reported the use of nanoscale Fe 0 with a cellulose hydrogel coating for Cr(VI) reduction and adsorption. According to [START_REF] Wang | A novel cellulose hydrogel coating with nanoscale Fe 0 for Cr(VI) adsorption and reduction[END_REF], the cellulose hydrogel firstly promoted physical adsorption, transferring Cr(VI) from the solution to the Fe 0 particles, where it was immobilized by electrostatic attraction.

The Cr(VI) was then reduced to Cr(III) by Fe 0 from the adsorbent.

Nevertheless, in the present study, the results did not indicate the occurrence of reduction of Cr(VI) to Cr(III). This reduction is also strongly dependent on the solution pH, according to the following chemical equation:

(10) - + - 3 + 4 2 HCrO + 7H + 3e Cr + 4H O à àÜ á àà
Therefore, the reduction of Cr(VI) to Cr(III) consumes H3O + , consequently increasing the solution pH. However, there was no increase of the solution pH in any of the adsorption studies. Furthermore, the absence of change in the behavior of the curves of adsorption capacity for Cr(VI) as a function of contact time (Figure 3c) and equilibrium solute concentration (Figure 3e) provided additional evidence that there was no reduction of Cr(VI) to Cr(III). It should also be noted that the formation of Cr(III) would be observed by the appearance of a green coloration in the solution and on the adsorbent surface after adsorption. This was not observed. Therefore, there was no experimental evidence of the reduction of Cr(VI) to Cr(III), under the experimental conditions studied.

Thermodynamic analysis (subsection 4.2.4) provided further elucidation of the nature of the interactions involved in the Cr(VI) or Cu(II) adsorption on C1. For example, the values of ΔadsH plotted against qe, for the adsorption of Cr(VI) on C1 (Figure 4), were much lower than the values expected for oxidation-reduction processes. Additionally, the energies were of the same order of magnitude as those obtained for Cu(II) adsorption.

Therefore, these results support the hypothesis that there was no Cr(VI) reduction.

Adsorption thermodynamics analysis

ITC measurements were performed in order to obtain more information about the nature of the interactions governing the adsorption of Cu(II) and oxyanions of Cr(VI) on C1.

ITC is a sensitive technique that provides the amount of energy released or absorbed in an isothermal thermodynamic process. Figure 4 shows the curves of ΔadsH plotted against qe, for the adsorption of oxyanions of Cr(VI) and Cu(II) on C1 at 25 ºC.

Figure 4

The adsorption processes of oxyanions of Cr(VI) and Cu(II) on C1 were exothermic over the range of surface coverage of C1 studied, changing from -30.3 ± 0.2 to -15.6 ± 0.1 kJ mol -1 for Cr(VI) species and from -30.6 ± 0.6 to -10.8 ± 0.9 kJ mol -1 for Cu(II). The ΔadsH values were more negative for oxyanions of Cr(VI) than for Cu(II), indicating that the balance of the interactions involving the adsorption of Cr(VI) species was more favorable. As qe increased, the adsorptions of oxyanions of Cr(VI) and Cu(II) became less enthalpically favorable, suggesting the existence of heterogeneous adsorption processes in both cases. Additionally, the slopes of the ΔadsH versus qe curves (dΔadsH/dqe) were very different, indicating different interactions for the adsorption of oxyanions of Cr(VI) and Cu(II) on C1.

In order to better understand these results, the ΔadsH value observed for each qe value could be considered as the sum of the following independent terms: (11) where, ΔadsH C1-M is the change in the enthalpy of adsorption (negative) due to the formation of interactions between the metal ion species and the adsorption sites on C1;

ΔadsH des is the change in the enthalpy of adsorption (positive or negative) associated with the desolvation processes of the metal ion species and the adsorbent surface sites for the formation of inner/outer-sphere complexes; and ΔadsH M-M is the change in the enthalpy of adsorption (positive or negative) associated with the absorption and release of energy when interactions between the metal ion species are formed on the C1 surface and disrupted in the solution, respectively, during the adsorption process.

At the first adsorbed amount value in the ΔadsH versus qe curves, when the surface coverage and the concentration of the metal ion species in the bulk solvent were low, the As qe increased, repulsive lateral interactions between the adsorbed ions increased, due to the decreased distance between the adsorbed metal ion species on the C1 surface, contributing to positive values for ΔadsH M-M . At the same time, due to the heterogeneity of the adsorbent surface, the magnitudes of both ΔadsH des and ΔadsH C1-M were changed, contributing to the increase of ΔadsH (less negative values).

The C1 adsorbent possessed different functional groups containing nitrogen atoms (imine, pyridine, and remaining amine groups), which implied the existence of adsorption sites with different adsorption molar enthalpy changes. When the surface coverage increased, adsorption sites with lower adsorption molar enthalpy change were occupied by the ions, increasing the ΔadsH C1-M value. Additionally, for the pH range evaluated, especially pH 5.5, some of the functional groups on C1 were partially protonated (pKa,imine = 5-7, pKa,pyridine = 5.2), which provided a wider variety of functional groups for Cu(II) adsorption. Greater heterogeneity of the C1 surface for Cu(II) adsorption could explain the higher slope of the ΔadsH versus qe curve for the adsorption of this species.

In order to evaluate the thermodynamically driven forces for the adsorption of the metal ion species and corroborate the hypothesis mentioned previously, adsorption thermodynamic parameters were obtained under the standard conditions. The values of ΔadsGº, ΔadsHº, and TΔadsSº were -26 ± 2, -33.0 ± 0.8, and -7 ± 3 kJ mol -1 for Cu(II) and -21 ± 3, -35.2 ± 0.2, and -14 ± 3 kJ mol -1 for Cr(VI), respectively. For Cr(VI), it was considered that HCrO4 -predominated over Cr2O7 2-(α = 375 pm, γe = 0.415, and ΔadsGº = -23 ± 3 kJ mol -1 , at pH 3.6), with an equilibrium concentration of 3.85 mmol L -1

and Ie of 0.06 mol L -1 (Supplementary Figure 1b). The values of ΔadsGº obtained in the present study were similar to those reported by [START_REF] Almeida | Application of a new bifunctionalized chitosan derivative with zwitterionic characteristics for the adsorption of Cu 2+ , Co 2+ , Ni 2+ , and oxyanions of Cr 6+ from aqueous solutions: Kinetic and equilibrium aspects[END_REF] for Cr(VI) (-21 ± 1 kJ mol -1 ) and Cu(II) (-20 ± 6 kJ mol -1 ).

The change in the free energy of adsorption (ΔadsGº) was negative for adsorption of Cu(II)

and oxyanions of Cr(VI) on C1, indicating that under the standard conditions, the transfer processes of both species from the bulk solution to the adsorbent surface were favorable and that oxyanions of Cr(VI) and Cu(II) were concentrated on the C1 adsorbent surface under the equilibrium condition. The ΔadsHº and ΔadsSº parameters were negative, indicating that the adsorption was enthalpically driven and entropically unfavorable.

However, the entropy loss for the adsorption of oxyanions of Cr(VI) was much higher.

The change in the standard entropy of adsorption is mainly due to the rotational, translational, and electrostatic contributions from the free metal ions in the bulk solution and the ion pairs formed on the C1 adsorbent surface (Marcus, 1987a). The main change in the entropy of the system arises from i) decrease of the degrees of freedom of the metal ion species, due to their transfer from the bulk solution to the C1 surface, and ii) increase of the degrees of freedom of water molecules when they are released from the solvation shells of the ions and the C1 surface sites to the bulk solution, because of the formation of inner/outer-sphere complexes. As the ΔadsSº value was negative, the entropy gain related to the process of release of water molecules did not exceed the entropy loss related to the process of formation of ion pairs, i.e. inner/outer-sphere complexes on the C1 adsorbent surface. The lower loss of entropy for Cu(II) adsorption was probably due to the release of a greater number of water molecules more strongly bound to the metal ion solvation shell, for the formation of inner-sphere complexes with the C1 adsorption sites, as well as the difference associated with the contribution of the rotational entropy of this type of complex (Marcus, 1987a).

Bicomponent adsorption of Cu(II) and oxyanions of Cr(VI) on C1

The presence of both oxyanions of Cr(VI) and Cu(II) cations in aqueous solution may lead to the formation of CuCrO4 precipitate. Therefore, the solubility (S, mmol L -1 ) of CuCrO4 was calculated using Eq. ( 12).

(

where, Ksp is the solubility product constant of CuCrO4 (Ksp = 3.6 × 10 -6 (Harris, 2010)), Ka1 and Ka2 are the ionization constants of acidic species of Cr(VI) (Eqs. ( 15)-( 16)), and

( )

1 2 sp S K ab = + 2 + 3 3 a2 a1 a2 [H O ] [H O ] 1 K K K a = + + 2 3 4 1 2 3 4 1 [HO ] [HO ] [HO ] [HO ] b b b b b - - - - = + + + +
β1, β2, β3, and β4 are the formation constants of Cu(II)-hydroxy complexes (Eqs. ( 17)-( 20)

). Here, the dimerization of chromate to dichromate (Eq. ( 21)) was not considered, because all the dichromate salts are soluble in water. Bicomponent adsorption studies (presented in the next sections) were performed using pH values and concentrations of Cu(II) and oxyanions of Cr(VI) at which CuCrO4 precipitation does not occur.

( In contrast, when the value of qmulti/qmono is > 1, the adsorption of a solute i is favored by the presence of a solute j. When the value of qmulti/qmono is 1, the presence of a solute

) (16) 15
i a1 + 1 2 4 2 4 3 a 1 H CrO + H O HCrO + H O 1.8 10 K K - - = à à àÜ á à àà a2 2 7 4 2 4 3 a 2 HCrO + H O CrO + H O 3.1 10 K K - - + - = à à àÜ á à àà ( ) 1 2 6 1 Cu OH Cu OH 3.162 10 b b + + - + = à à à Ü á à à à ( ) 2 2 1 1 2 2 Cu 2OH Cu OH 6.310 10 b b + - + = à à à Ü á à àà ( ) 3 2 1 4 3 3 Cu 3OH Cu OH 3.162 10 b b - + - + = à à à Ü á à à à ( ) 4 2 2 1 5 4 4 Cu 4OH Cu OH 3.981 10 b b - + - + = à à à Ü á à àà 2 4 2 7 2 2 HCrO Cr O H O 2.05 D K D log K - -+ = à à àÜ á à àà
does not affect the adsorption of a solute j. The values of qmulti/qmono (0.6-0.8) for Cr(VI) adsorption from pH 3.6 to 4.5 were lower than unity, showing that the presence of Cu(II) disfavored the adsorption of Cr(VI) on C1. However, from pH 5.0 to 5.5, where the CrO4 2- concentration begins to increase, the presence of Cu(II) favored Cr(VI) adsorption (qmulti/qmono = 1.5, at pH 5.0). This was indicative of cooperative adsorption between oxyanions of Cr(VI) and Cu(II). The values of qmulti/qmono (17.9-1.2) for Cu(II) adsorption from pH 3.6 to 4.5 were higher than unity, showing that the presence of oxyanions of Cr(VI) favored Cu(II) adsorption. This also indicated cooperative adsorption between Cu(II) and oxyanions of Cr(VI). However, from pH 5.0 to 5.5, the presence of oxyanions of Cr(VI) disfavored the Cu(II) adsorption (qmulti/qmono = 0.5, at pH 5.0).

The Cu(II) ions were probably adsorbed on the C1 surface by the formation of innersphere complexes, while oxyanions of Cr(VI) were adsorbed on the C1 surface by the formation of outer-sphere complexes. These two types of adsorption, known as localized (specific, (Cu(II)) adsorption and delocalized (nonspecific, oxyanions of Cr(VI)) adsorption, allowed the formation of a Stern layer on the C1 surface. As the solvated Cu(II) ions did not form complexes with oxyanions of Cr(VI) adsorbed on the C1 surface, and vice-versa, they approached the C1 surface and were attached by delocalized (nonspecific) adsorption [START_REF] Sposito | The Chemistry of Soils[END_REF]. Therefore, a hypothesis for the cooperative adsorption between oxyanions of Cr(VI) and Cu(II) ions was the formation of a diffuse ion swarm, involving ions fully dissociated from the C1 surface functional groups and free to approach nearby adsorbed species on the C1 surface [START_REF] Sposito | The Chemistry of Soils[END_REF]. This type of interaction only involves electrostatic bonding.

The highest simultaneous adsorption capacity (1.96 mmol g -1 ) for oxyanions of Cr(VI) and Cu(II) was observed at pH 4.5. Therefore, a pH of 4.5 was considered as the optimum for simultaneous adsorption of both solutes on C1. The competitive model of [START_REF] Corsel | The role of intrinsic binding rate and transport rate in the adsorption of prothrombin, albumin, and fibrinogen to phospholipid bilayers[END_REF] was adopted to describe the multicomponent adsorption kinetics. Although the PFO and PSO models can be used to model the individual adsorption kinetic curves in a competitive adsorption of metal ions in aqueous solution, these models cannot describe the interactions between ions. On the contrary, the competitive adsorption model developed by [START_REF] Corsel | The role of intrinsic binding rate and transport rate in the adsorption of prothrombin, albumin, and fibrinogen to phospholipid bilayers[END_REF] can be used to model both adsorption kinetic curves simultaneously, allowing the understanding of the interactions between ions, i.e., how the adsorption of a species i affects the adsorption of a species j and vice versa. This model includes the intrinsic adsorption (k(Γ) app on) and desorption (k(Γ) app off) rate constants, which employ the adsorption capacity normalized by the specific area of the adsorbent (Γ). The model considers the deviations from ideal behavior assumed by the Langmuir model. The kinetic model of [START_REF] Corsel | The role of intrinsic binding rate and transport rate in the adsorption of prothrombin, albumin, and fibrinogen to phospholipid bilayers[END_REF], which is based on first-order reaction kinetics, employs a generalized diffusion equation.

It enables inclusion of the effect of the surrounding bulk medium (unstirred layer) [START_REF] Teodoro | Synthesis and application of a new carboxylated cellulose derivative. Part II: Removal of Co 2+ , Cu 2+ and Ni 2+ from bicomponent spiked aqueous solution[END_REF].

In previous studies, the Corsel model (Corsel et al., 1986) was employed to model the kinetics of the competitive adsorption of metal cations [START_REF] Teodoro | Synthesis and application of a new carboxylated cellulose derivative. Part II: Removal of Co 2+ , Cu 2+ and Ni 2+ from bicomponent spiked aqueous solution[END_REF] and cationic dyes [START_REF] Fideles | Trimellitated sugarcane bagasse: A versatile adsorbent for removal of cationic dyes from aqueous solution. Part II: Batch and continuous adsorption in a bicomponent system[END_REF] on lignocellulosic materials. [START_REF] Teodoro | Synthesis and application of a new carboxylated cellulose derivative. Part II: Removal of Co 2+ , Cu 2+ and Ni 2+ from bicomponent spiked aqueous solution[END_REF] The kinetic parameters estimated by the [START_REF] Corsel | The role of intrinsic binding rate and transport rate in the adsorption of prothrombin, albumin, and fibrinogen to phospholipid bilayers[END_REF] are presented in Table 5.

Figure 5b presents a graph of Γ(t) plotted against t. The equilibrium time (te,multi) for simultaneous adsorption of Cu(II) and oxyanions of Cr(VI) was 180 min, while the equilibrium times (te,mono) for monocomponent adsorption of Cu(II) and oxyanions of Cr(VI) were 240 and 360 min, respectively. This suggested that the presence of Cu(II) decreased the equilibrium time for adsorption of oxyanions of Cr(VI), and vice-versa. This result could be an indication of cooperative adsorption between Cr(VI) and Cu(II), due to electrostatic interaction between these ions. A possible cooperative effect in the adsorption of Cu(II) and Cr(VI) was also reported by [START_REF] Shen | A new insight on the adsorption mechanism of amino-functionalized nano-Fe3O4 magnetic polymers in Cu(II), Cr(VI) co-existing water system[END_REF], who studied the use of amino-functionalized nano-Fe3O4 magnetic polymers for adsorption of Cu(II) (100 mg L -1 ) and Cr(VI) (200 mg L -1 ) co-existing in a water system. It was concluded that there might be cooperative adsorption processes, although competitive adsorption was observed at higher concentrations of Cr(VI) and Cu(II).

The association constant (K) is related to the affinity of a solute i for the surface adsorption sites of an adsorbent, in the presence of a solute j. The value of K is calculated by the ratio of the adsorption (k+1) and desorption (k-1) rate constants, k+1/k-1 [START_REF] Teodoro | Synthesis and application of a new carboxylated cellulose derivative. Part II: Removal of Co 2+ , Cu 2+ and Ni 2+ from bicomponent spiked aqueous solution[END_REF]. The value of K was higher for Cr(VI) adsorption than for Cu(II) adsorption, indicating that the affinity of the C1 surface sites for oxyanions of Cr(VI), in the presence of Cu(II), was higher than the affinity of the C1 surface sites for Cu(II) ions, in the presence of oxyanions of Cr(VI). This behavior was not expected, because the value of b for monocomponent adsorption of Cu(II) (17 ± 1 L mmol -1 ) was much higher than that for monocomponent adsorption of oxyanions of Cr(VI) (3.8 ± 0.5 L mmol -1 ). This confirmed the non-ideal behavior of the adsorption of Cu(II) ions in the presence of oxyanions of Cr(VI), and vice-versa.

The interaction constants α and β for the adsorption and desorption of a solute at an adsorbent, respectively, provide useful information about lateral interactions between adsorbed species in multicomponent systems [START_REF] Teodoro | Synthesis and application of a new carboxylated cellulose derivative. Part II: Removal of Co 2+ , Cu 2+ and Ni 2+ from bicomponent spiked aqueous solution[END_REF]. Positive values of α indicated that oxyanions of Cr(VI) or Cu(II) ions did not tend to adsorb near other adsorbed species on the C1 surface, which could be explained by repulsive potentials around species adsorbed on the surface. The value of α was higher for Cr(VI) adsorption than for Cu(II) adsorption, suggesting that oxyanions of Cr(VI) tended not to adsorb near Cu(II) ions already adsorbed on C1 surface sites. In contrast, positive values of β indicated that oxyanions of Cr(VI) or Cu(II) ions tended to desorb from the C1 surface when it became progressively saturated. The higher value of β for Cr(VI) adsorption, compared to Cu(II) adsorption, showed that oxyanions of Cr(VI) tended to desorb from the C1 surface faster than Cu(II) ions. According to [START_REF] Cuypers | Adsorption kinetics of protein mixtures. A tentative explanation of the Vroman effect[END_REF], the greater the sum of the interaction constants (γ = α + β), the greater the effect of a solute i on the adsorption of a solute j. At pH 4.5, the oxyanions of Cr(VI) had a greater influence on Cu(II) adsorption, compared to the influence of Cu(II) adsorption on the adsorption of oxyanions of Cr(VI). This was in agreement with the results obtained for the simultaneous adsorption (at pH 4.5) of oxyanions of Cr(VI) (qmulti/qmono = 0.8) and Cu(II) (qmulti/qmono = 2.6).

In the bicomponent adsorption, oxyanions of Cr(VI) presented a 3-fold higher effective diffusion coefficient (Di), compared to Cu(II) ions. The thickness of the unstirred water layer (δ) surrounding the C1 particles seemed to have a significant effect on the adsorption of Cu(II) ions and oxyanions of Cr(VI) on C1. The diameter of a water molecule is 0.278 nm [START_REF] Zou | water shell" model for the dielectric properties of hydrated silica-filled epoxy nano-composites[END_REF], so the estimated thickness of the unstirred water layer was ~62 water molecules.

Table 5

Adsorption of Cu(II) and oxyanions of Cr(VI) on C1, as a function of initial metal ion concentration

Multicomponent isotherms are useful for describing the adsorption behavior of a mixture of solutes on an adsorbent. These isotherms can also assist in elucidating the influence of a solute i on the adsorption capacity of a solute j, as well as the selectivity of an adsorbent for a specific solute in a mixture of N solutes.

The ideal adsorbed solution theory model (IAST) was proposed by [START_REF] Myers | Thermodynamics of mixed-gas adsorption[END_REF] for describing the adsorption of a mixture of gases. Later, [START_REF] Radke | Thermodynamics of multi-solute adsorption from dilute liquid solutions[END_REF] extended this model to the liquid phase. However, IAST is not suitable for describing the adsorption of solutes that present antagonistic or synergistic interactions (non-ideal behavior). The real adsorbed solution theory (RAST) was proposed by [START_REF] Costa | Adsorption of binary and ternary hydrocarbon gas mixtures on activated carbon: Experimental determination and theoretical prediction of the ternary equilibrium data[END_REF]. This model is an extension of the IAST model for describing the adsorption of solutes that present non-ideal behavior.

The RAST model was also successfully employed to model experimental equilibrium data for adsorption of the binary systems Cu(II)/Co(II), Cu(II)/Ni(II), and Co(II)/Ni(II) on a carboxylated cellulose derivative [START_REF] Teodoro | Synthesis and application of a new carboxylated cellulose derivative. Part II: Removal of Co 2+ , Cu 2+ and Ni 2+ from bicomponent spiked aqueous solution[END_REF] as well as the bicomponent adsorption of auramine-O and safranin-T on trimellitated sugarcane bagasse [START_REF] Fideles | Trimellitated sugarcane bagasse: A versatile adsorbent for removal of cationic dyes from aqueous solution. Part II: Batch and continuous adsorption in a bicomponent system[END_REF].

Figure 5c shows the bicomponent isotherm for simultaneous adsorption of Cu(II) and oxyanions of Cr(VI) on C1. The values of Qmax for adsorption of Cu(II) and oxyanions of Cr(VI) on C1 were 1.13 ± 0.01 and 0.98 ± 0.01 mmol g -1 , respectively. The sum of the Qmax values was 2.11 ± 0.03 mmol g -1 . The sums of the qe values (at pH 4.5) for monoand bicomponent adsorption of oxyanions of Cr(VI) and Cu(II), as a function of solution pH, were 1.9 ± 0.1 and 1.96 ± 0.03 mmol g -1 , respectively. This indicated that there was a slight increase in the total adsorption capacity for bicomponent adsorption, compared to monocomponent adsorption.

The bicomponent isotherm profiles showed that the qe values for adsorption of Cu(II) and oxyanions of Cr(VI) on C1 increased progressively with increasing equilibrium Cr(VI) and Cu(II) concentrations, until reaching a plateau. on C1. The values of γ for Cr(VI) and Cu(II) were higher than unity, indicating that the Cr(VI) or Cu(II) ions (Supplementary Figure 4). The concentrations of Cu(II) ions or oxyanions of Cr(VI) on the C1 surface were not constant along the line. Figure 7c shows an SEM-EDX image of the C1 surface loaded with both Cr(VI) and Cu(II) ions present in an equimolar mixture, revealing non-uniform distributions of Cr(VI) and Cu(II) ions along the C1 surface. In addition, there appeared to be a number of vacant adsorption sites on the C1 surface loaded with both Cr(VI) and Cu(II) ions, when compared to SEM-EDX images of C1 loaded with either Cr(VI) (Figure 7a) or Cu(II) (Figure 7b) ions. Since the total adsorption capacity of C1 for Cr(VI) and Cu(II) ions did not decrease (as pointed out in Section 4.3.3), this was suggestive of cooperative adsorption between oxyanions of Cr(VI) and Cu(II) on C1. This was in agreement with the hypothesis discussed in Section 4.2.2, concerning the formation of a diffuse ion swarm.

Figure 7

Desorption and reuse of spent adsorbent

In Table 3 are presented the Edes values for the desorption of oxyanions of Cr(VI) and Cu(II) from C1 using aqueous solutions of Na2CO3 (1.0 mol L -1 ) and triethylenetetramine (0.01 mol L -1 ), respectively. The value of Edes for Cu(II) (~96%) was higher than for Cr(VI) (~49%). The Cu(II) ions were almost completely desorbed from C1, because the complex formed between Cu(II) and triethylenetetramine (trien) is highly stable.

Transition metals such as Cu(II) bind to the amine functions, forming polydentate complexes of high stability [START_REF] Navarro | Role of anions on heavy metal sorption of a cellulose modified with poly(glycidyl methacrylate) and polyethyleneimine[END_REF]. The formation constant (K1) of the trien-Cu(II) complex has a high value, with log K1 of 20.4 at 25 ºC [START_REF] Dean | Lange's Handbook of chemistry[END_REF].

The oxyanions of Cr(VI) were only partially desorbed from C1, presenting behavior different to that observed for Cu(II) desorption. The desorption of oxyanions of Cr(VI) was expected to occur by ion exchange, since the ions were adsorbed by electrostatic attraction (outer-sphere complexes). The size of HCrO4 -is 2.42 Å [START_REF] Sharma | The treatment of chromium wastewaters using the sorptive potential of leaf mould[END_REF], while the size of CO3 2-is 1.85 Å [START_REF] Chen | Study of the corrosion mechanism of the in situ grown Mg-Al-CO3 2hydrotalcite film on AZ31 alloy[END_REF]. Although the charge/radius (Z/r) ratio of HCrO4 -(1/2.42) is higher than that of CO3 2-(2/1.89), monovalent anions are easily exchanged by multivalent anions. Therefore, the use of a desorbent such as carbonate solution should enable the ion exchange of HCrO4 -by CO3 2-. On the other hand, the partial desorption of oxyanions of Cr(VI) from different adsorbents has been reported to be due to the phenomenon of aging [START_REF] Kuo | Sorption and desorption of chromate by wood shavings impregnated with iron or aluminum oxide[END_REF][START_REF] Moreira | Bifunctionalized chitosan: A versatile adsorbent for removal of Cu(II) and Cr(VI) from aqueous solution[END_REF].

According to [START_REF] Kuo | Sorption and desorption of chromate by wood shavings impregnated with iron or aluminum oxide[END_REF], oxyanions of Cr(VI) freshly loaded onto adsorbents can be easily desorbed.

In Table 3 are presented the values of Ere-ads for re-adsorption of oxyanions of Cr(VI) and Cu(II) on the spent C1 adsorbent. The value of Ere-ads for Cr(VI) re-adsorption was ~36%.

This was expected, due to the low Edes value for Cr(VI) desorption from C1. After desorption, a significant amount of oxyanions of Cr(VI) remained on the C1 surface, decreasing the number of free adsorption sites available for re-adsorption of Cr(VI) species. Although the Ere-ads value for Cr(VI) was considered low, this did not prevent the reuse of C1, since the material was still able to adsorb oxyanions of Cr(VI). On the other hand, the Ere-ads value for Cu(II) was ~100%, showing that the spent C1 adsorbent was able to adsorb the same amount of Cu(II) ions as in the first adsorption cycle. This demonstrated the excellent reuse potential of C1 for the adsorption of cations.

Conclusions

The imine and pyridine groups introduced on C1 were able to adsorb oxyanions of Cr(VI) by the formation of outer-sphere complexes (∆adsHº = -35.2 ± 0.2, T∆adsSº = -14 ± 3), while Cu(II) ions were adsorbed by the formation of inner-sphere complexes (∆adsHº = -33.0 ± 0.8, T∆adsSº = -7 ± 3), as shown by the thermodynamic parameters of adsorption.

C1 was able to simultaneously adsorb oxyanions of Cr(VI) and Cu(II) ions in the pH range 3.6-5.5, showing the versatility of this material for water treatment. The maximum adsorption capacities (at pH 4.5) of C1 for oxyanions of Cr(VI) and Cu(II) ions were 0.98 ± 0.01 and 1.13 ± 0.01 mmol g -1 , respectively. Although C1 was able to adsorb Cu(II) and Cr(VI) simultaneously (at pH 3.6-4.5), better adsorption performance was observed for single solute adsorption, with Qmax values of 3.8 ± 0.1 mmol g -1 (at pH 3.6) and 1.84 ± 0.03 mmol g -1 (at pH 5.5) for Cr(VI) and Cu(II), respectively. The reuse of C1 was investigated, with Cu(II) ions being almost completely desorbed (~96%) and fully re-adsorbed (~100%). For Cr(VI) ions, the desorption was incomplete (~49%), resulting in low re-adsorption (~36%). C1 was demonstrated to be an excellent adsorbent for cations of Cu(II), while its use for adsorption of oxyanions of Cr(VI) was limited by its partial reuse capacity.

  Cu(II) and oxyanions of Cr(VI), the ΔadsH versus equilibrium concentration of metal ion (Ce) curves (Figures not shown) were extrapolated to Ce → 0. The changes in the standard entropy of adsorption (ΔadsS°) for adsorption of oxyanions of Cr(VI) and Cu(II) were determined from the following classical thermodynamic relationship: oxyanions of Cr(VI) and/or Cu(II) was analyzed by energy-dispersive Xray (EDX) spectroscopy . The materials were dried in an oven at 80.0 ºC for 1 h, followed by pressing 100 mg portions of the samples denoted C1-Cu(II), C1-Cr(VI), and C1-Cu(II)-Cr(VI) in a hydraulic press (Model 181-1110, Pike Technologies) for 1 min, at

  presented the kinetic parameters obtained by modeling the adsorption of Cu(II) and oxyanions of Cr(VI) on C1, using the PFO and PSO models, as well as the Boyd and intraparticle diffusion models. The PSO kinetic model provided the best description of the adsorption of oxyanions of Cr(VI) (HCrO4 -and Cr2O7 2-) and Cu(II) on C1. The values of the R 2 and χ 2 red error functions were higher and lower, respectively, comparing the PSO model with the PFO model. In addition, the values of qe,est (estimated equilibrium adsorption capacity) calculated using the PSO model were closer to the qe,exp values (experimental equilibrium adsorption capacity) for the adsorption of oxyanions of Cr(VI)

  used carbonized crofton weed (Eupatorium adenophorum) and Dong et al. (2010) used a crosslinked amino starch for Cu(II) and Cr(VI) adsorption from aqueous solutions. Chen et al. (2016) reported Qmax values of 0.19 and 0.44 mmol g -1 for adsorption of Cr(VI) and Cu(II), respectively (pH 5.0, 25 ºC). The crosslinked amino starch reported by Dong et al. (2010) was produced by chemical modification of dialdehyde starch with ethylenediamine and presented Qmax values of 0.13 and 0.23 mmol g -1 for adsorption of Cu(II) and Cr(VI), respectively (pH 3.0-5.0, 30 ºC)

  ΔadsH M-M term was negligible and the ΔadsH values were determined by the magnitudes of the ΔadsH C1-M and ΔadsH des terms. Since the process was exothermic under this condition, there should be an important contribution of the interactions between the C1 adsorption sites and oxyanions of Cr(VI) or Cu(II), which released energy, because the desolvation of the functional groups containing nitrogen atoms and the metal ion species required a high amount of energy(Marcus, 1987b). Part of the desolvation energy was due to the dehydration of the metal ion species, with the displacement of water molecules from the solvation shells of the ions to bulk solution. Since Cu(II) could form inner-sphere complexes with the lone electron pairs of the nitrogen atoms on C1, the displacement of water molecules from the first solvation shell of these ions should result in a more endothermic ΔadsH des term for this metal ion, compared to the oxyanions of Cr(VI), which could form outer-sphere complexes. This could explain the less negative values of ΔadsH for Cu(II) adsorption.

  Figure5apresents a graph of qe plotted against solution pH (from 3.6 to 5.5) for the

  Figure 5

  studied the adsorption of the binary systems Cu(II)/Co(II), Cu(II)/Ni(II), and Co(II)/Ni(II) on a carboxylated cellulose derivative. Fidelis et al. (2019) studied the bicomponent adsorption of auramine-O and safranin-T on trimellitated sugarcane bagasse. In both studies, it was concluded that the Corsel model was more suitable for describing bicomponent adsorption systems, because it takes into consideration the competition between the adsorbate species for the adsorbent sites.

Figure

  Figure6ashows plots of qe,exp against qe,est for simultaneous adsorption of Cu(II) and

Figure

  Figure 6b presents a graph of the experimental values of γ, as a function of reduced

Figure 1 .

 1 Figure 1. Scheme illustrating (a) the synthesis of C1 from chitosan and pyridine-2carbaldehyde, and (b) the suggested mechanism for removal of Cu(II) and an oxyanion of Cr(VI) (HCrO4 -) by the C1 adsorbent.

Figure 2 .

 2 Figure 2. SEM images of chitosan (a and c) and C1 (b and d) at 60× and 3,000× magnifications.

Figure 3 .

 3 Figure 3. Profiles of the adsorption capacity, as a function of (a) solution pH for adsorption of Cu(II) and Cr(VI), (b) contact time for the adsorption of Cu(II), (c) contact time for the adsorption of Cr(VI), (d) equilibrium solute concentration for adsorption of Cu(II), and (e) equilibrium solute concentration for adsorption of Cr(VI). Experimental conditions: (a) [Cu(II)] = [Cr(VI)] = 0.77 mmol L -1 , 130 rpm, 25 ºC, 0.2 g L -1 C1, and 360 min contact time; (b) and (c) ([Cu(II)] = [Cr(VI)] = 0.77 mmol L -1 , 130 rpm, 25 ºC, 0.2 g L -1 C1, pH 5.5 for Cu(II), and pH 3.6 for Cr(VI)); and (d) and (e): 130 rpm, 25 ºC, 0.2 g L -1 C1, pH 5.5 and 360 min for Cu(II), and pH 3.6 and 240 min for Cr(VI).

Figure 4 .

 4 Figure 4. Changes in enthalpy of adsorption, as a function of qe, for adsorption on C1 of Cu(II) at pH 5.5 and oxyanions of Cr(VI) at pH 3.6, at 25 ºC.

Figure 5 .

 5 Figure 5. Profiles of the simultaneous adsorption of Cu(II) and Cr(VI) on C1: (a) adsorption capacity as a function of solution pH, (b) adsorption capacity normalized by the specific surface area (Γ(t)), as a function of contact time, and (c) equilibrium adsorption capacity (qe), as a function of equilibrium solute concentration. Experimental conditions: (a) 25 ºC, 130 rpm, [Cu(II)] = [Cr(VI)] = 0.77 mmol L -1 , 0.2 g L -1 C1, and 180 min contact time; (b) [Cu(II)] = [Cr(VI)] = 0.77 mmol L -1 , 130 rpm, 25 ºC, 0.2 g L -1 C1, pH 5.5 for Cu(II), and pH 3.6 for Cr(VI); and (c) 130 rpm, 25 ºC, 0.2 g L - 1 C1, pH 4.5, and 180 min contact time.

Figure 6 .

 6 Figure 6. Plots for simultaneous adsorption of oxyanions of Cr(VI) and Cu(II) on C1 of (a) experimental equilibrium adsorption capacity (qe,exp) against estimated equilibrium adsorption capacity (qe,est); (b) experimental activity coefficients of Cu(II) and Cr(VI), as a function of reduced spreading pressure, and (c) experimental activity coefficient of Cr(VI) plotted against experimental activity coefficient of Cu(II). Experimental conditions: (a) [Cu(II)]0 = [Cr(VI)]0 = 0.05-4.0 mmol L -1 , 180 min, 25 ºC, pH 4.5, 130 rpm, and 0.2 g L -1 C1.

Figure 7 .

 7 Figure 7. SEM-EDX images with surface mapping for (a) oxyanions of Cr(VI), (b) Cu(II), and (c) oxyanions of Cr(VI) and Cu(II) adsorbed on C1 ([Cu(II)] = [Cr(VI)] = 0.77 mmol L -1 , 130 rpm, 25 ºC, 0.2 g L -1 C1, 360 and 240 min contact times for individual adsorptions of Cu(II) and Cr(VI), respectively, and 180 min contact time for simultaneous adsorption of Cu(II) and Cr(VI)).

  Figure 1.

Figure 2a

 2a Figure 2a

Figure 2b

 2b Figure 2b

Figure 2c

 2c Figure 2c

Figure 2d

 2d Figure 2d

Figure 3a

 3a Figure 3a

Figure 3b

 3b Figure 3b

  Figure 3c

  57

  Figure 3e

  Figure 5b

Figure 5c

 5c Figure 5c

  Figure 6a

Figure 6b

 6b Figure 6b

  Figure 6c

Figure 7a

 7a Figure 7a

  Figure 7b

Figure 7c

  Figure 7c

Table 2

 2

	e
	des
	max	C1

Acknowledgments

The authors are grateful for research support provided by Universidade Federal de Ouro Preto (UFOP), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG, grant number CEX-APQ-01764-14), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq PVE grant number 400739/2014-3, CNPq grant number 422507/2018-0, ANR (ANR-11-BS07-030-01)), LabEx CHARMMMAT (ANR-11-LABEX-0039), and the University of Versailles St Quentin. The authors are also grateful to FAPEMIG for a Master's scholarship awarded to F. J. Gonçalves.

adsorptions of oxyanions of Cr(VI) and Cu(II) on C1 deviated from ideal behavior [START_REF] Erto | A Real Adsorbed Solution Theory model for competitive multicomponent liquid adsorption onto granular activated carbon[END_REF][START_REF] Teodoro | Synthesis and application of a new carboxylated cellulose derivative. Part II: Removal of Co 2+ , Cu 2+ and Ni 2+ from bicomponent spiked aqueous solution[END_REF].

Figure 6c presents a graph of the experimental values of γCr, as a function of the experimental values of γCu, for the simultaneous adsorption of oxyanions of Cr(VI) and Cu(II) on C1. Linear regression of the data resulted in a high R 2 value (> 0.98) and low values of χ 2 red (5.76 × 10 -5 ) and RSS (8.06 × 10 -4 ), indicating that the Wilson model equations [START_REF] Wilson | Vapor-Liquid equilibrium. XI. A new expression for the excess free energy of mixing[END_REF] could be used for estimating the adjustable parameters (c, ᴧ12, and ᴧ21) [START_REF] Teodoro | Synthesis and application of a new carboxylated cellulose derivative. Part II: Removal of Co 2+ , Cu 2+ and Ni 2+ from bicomponent spiked aqueous solution[END_REF].

Energy dispersive X-ray spectroscopy (EDX)

Figure 7 presents SEM-EDX images of the C1 surface loaded with Cu(II), oxyanions of Cr(VI), or both. Figures 7a and7b show that the distributions of adsorbed Cr(VI) and Cu(II) ions along the C1 surface were not homogeneous. This was confirmed by EDX microanalysis along lines with length of 1500 μm, drawn on the C1 samples loaded with