The removal of copper (II) ion by using mushroom biomass (Agaricus bisporus) and kinetic modelling

Desalination 255 (2010) 137–142

Contents lists available at ScienceDirect

Desalination j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / d e s a l

The removal of copper (II) ion by using mushroom biomass (Agaricus bisporus) and kinetic modelling N. Ertugay ⁎, Y.K. Bayhan Department of Environmental Engineering, Faculty of Engineering, Ataturk University, 25240 Erzurum, Turkey

a r t i c l e

i n f o

Article history: Received 26 October 2009 Received in revised form 24 December 2009 Accepted 7 January 2010 Available online 9 February 2010 Keywords: Biosorption Agaricus bisporus Copper (II) Kinetic Adsorption isotherms

a b s t r a c t The efficiency of Agaricus bisporus as an adsorbent for removing Cu2+ ions from synthetic wastewater has been studied. Batch adsorption experiments were carried out as a function of contact time, pH, zeta potential of particles, initial metal ion concentration and temperatures. Cu2+ uptake was very rapid during the first 5 min. Contact time was observed in 30 min. The extent of metal ion removed increased with increasing initial metal ion concentration. Maximum metal sorption was found to occur at initial pH 5.0. Adsorption equilibrium data was calculated for Langmuir, Freundlich, Dubinin–Radushkevich and Temkin isotherms at different temperatures. It was found that biosorption of Cu2+ was better suited to the Freundlich adsorption model than other adsorption models. To study the kinetics of adsorption, batch adsorption models were applied, using pseudo-first and second-order mechanisms at different initial concentrations of Cu2+. The best result came from the second-order mechanism. Thermodynamic parameters such as ΔG°, ΔH° and ΔS° were calculated. The thermodynamics of Cu2+ ion onto A. bisporus indicates the spontaneous and exothermic nature of the process. The activation energy of the biosorption (Ea) was determined as 118.86 kJ mol− 1 from the Arrhenius equation. © 2010 Elsevier B.V. All rights reserved.

1. Introduction In water bodies, the presence of heavy metals in incoming waste streams has harmful effects on human health and to the fauna and flora. Environmental legal standards have evolved and now the discharge of heavy metals into aquatic bodies and sources of potable water is rigorously controlled [1]. Copper is one of the most common toxic metals that finds its way to water sources from various industries, i.e. electroplating, mining, electrical and electronics, iron and steel production, non-ferrous metal industry, printing and photographic industries. As with other heavy metals, small amounts of copper are necessary for life functions. However, copper concentrations in humans have increased to toxic levels causing various diseases and disorders, such as liver damage [2]. According to U.S. Environmental Protection Agency (EPA) standards, the permissible limit of copper discharge in industrial effluents into water bodies is limited to 0.25 mg l− 1 [2]. There are several methods available to achieve the reduction of heavy metals in wastewater; including chemical precipitation, ion exchange, reverse osmosis, etc., but high costs restrict their widespread use [3]. To achieve wide-spread removal of heavy metals from water sources, a more efficient and low-cost process is needed. Recently, biosorption has attracted growing interest. Using inexpen-

⁎ Corresponding author. Fax: +90 442 2360957. E-mail address: [email protected] (N. Ertugay). 0011-9164/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.desal.2010.01.002

sive sorbents, biosorption can achieve high purity in treated wastewater. Studies on various types of non-living biomasses, such as algae [4,5], fungi [6], bacteria [7], yeast [8], nut hulls [9], and wood sawdust [10] have shown that biomaterials can be used for the removal of toxic metal ions from wastewater [11]. Most of these works has shown that natural products can be effective sorbents for heavy metals [12]. The object of this study is to investigate the possible use of Agaricus bisporus as an alternative biosorbent material for removal of Cu2+ ions from aqueous solutions. The effects of contact time, initial metal ion concentration, temperature of solution and pH on the removal of Cu2+, along with the zeta potential of particles were evaluated at different pH values. The thermodynamic parameters and the kinetics of Cu2+ adsorption of were also calculated and discussed.

2. Materials and methods 2.1. Preparation of biomass Fresh fungal biomass of A. bisporus purchased from a commercial company was used in this investigation as an adsorbent. The chemical characteristics of A. bisporus are shown in Table 1 [13]. Before use, it was washed with distilled water to remove dirt. Then, the fungal biomass was dried at 80 °C for 24 h, and granulated in a mortar to a very fine powder. The last step was to sieve the fungal biomass through a 140-mesh copper sieve.

138

N. Ertugay, Y.K. Bayhan / Desalination 255 (2010) 137–142

Table 1 The chemical characteristicsa of A. bisporus [13]. Water

Protein

Carbohydrate

Oil

Cellulose

Ash

90.8

2.76

2.85

0.24

0.90

1.00

a

The values were expressed as %.

where R (8.314 J mol− 1 K− 1) is the gas constant, and T is the absolute temperature. The Temkin isotherm assumes that the fall in sorption heat is linear rather than logarithmic, as implied in the Freundlich equation. The Temkin isotherm has generally, been applied in the following form [7]: RT lnðAT Ce Þ bT

ð4Þ

2.2. Preparation of Cu (II) solutions

qe =

Cu2+ solutions were prepared using CuSO4·5H2O. A stock solution (500 mg l− 1) of Cu2+ was prepared by dissolving the required quantity of CuSO4·5H2O in deionized distilled water. For all of the biosorption experiments, a Cu2+ solution containing 30–100 mg l− 1 was prepared and used. The pH of the solution was adjusted using H2SO4 and NaOH solutions.

where AT (l mg− 1) and bT are Temkin isotherm constants, R is the universal gas constant and T is the absolute temperature. There have been several reports [20,21] on the use of different kinetic models to describe experimental data of heavy metals adsorption on biomass. The pseudo-first-order rate Lagergren model is:

2.3. Batch biosorption experiments logðqe −qt Þ = log qe − The batch biosorption experiments were carried out in 250 ml erlenmeyer flasks containing 100 ml Cu2+ on a rotary shaker at 150 rpm at a temperature of 20 °C. The samples were taken at definite time intervals (at 3, 5, 10, 15, 20 and 30 min) and were filtered immediately to remove biomass with filter paper (Whatman 42). The Cu2+ in the remaining solution was then analyzed. The residual Cu2+ ions in the biosorption were determined spectrophotometrically at 460 nm using sodium diethyl dithiocarbamate reagent in 1.5 N NH3 as the complexing agent for Cu2+ [14]. Zeta potential was measured with a Zeta-Meter (ZETAMETER 3.0 + 542, USA).

k1 t 2:303

ð5Þ

where qe and qt are the amounts of adsorbed Cu2+ ions on the biosorbent at equilibrium and at time t (min.) respectively and k1 is the first-order biosorption rate constant (1 min− 1). The pseudo-second-order kinetic model is [22]: t 1 1 = + t qt qe k2 q2e

ð6Þ

where k2 is the rate constant of second-order sorption (g mg− 1 min− 1).

2.4. Equilibrium isotherms and kinetics of biosorption 2.5. Thermodynamics of biosorption Adsorption equilibrium data were calculated for Langmuir, Freundlich, Dubinin–Radushkevich, and Temkin isotherms at different temperatures. The Langmuir isotherm is valid for monolayer sorption onto the surface of a finite number of identical sites; expressed in the linear form as [15]: Ce 1 C + e = Q 0b qe Q0

ð1Þ

where Ce is the equilibrium concentration (mg l− 1) and qe is the amount adsorbed at equilibrium (mg g− 1). The Langmuir constant Q0 (mg g− 1) represents the monolayer adsorption capacity and b (l mg− 1) relates to adsorption heat. The Freundlich equation has been widely used and is applied for isothermal adsorption. The Freundlich isotherm describes heterogeneous surface energies in multilayer adsorption and is expressed in linear form as [16]: 1 log Ce n

log qe = log Kf +

ð2Þ

where qe is the concentration of the adsorbed solute (mg g− 1), Ce is the concentration of the solute in solution (mg l− 1), Kf (mg g1− (1/n) l1/n g− 1) relates to the adsorption capacity of the adsorbent, and 1/n represents the surface heterogeneity [17]. The Dubinin–Radushkevich isotherm (D–R) is more general than the Langmuir isotherm, because it does not assume a homogeneous surface or constant sorption potential [18]. The D–R Eq. [19] is: 2

ln qe = ln qm −βε

The thermodynamic parameters including change in free energy (ΔG°), enthalpy (ΔH°) and entropy (ΔS°) were determined using following equations:

Ce; ad Ce

ð7Þ

ΔG  = −RT ln Kc

ð8Þ

ΔG  = ΔH −TΔS 

ð9Þ

Kc =

where KC is the equilibrium constant, Ce,ad the amount of Cu2+ adsorbed on the adsorbent of the solution at equilibrium (mg l− 1), Ce is the equilibrium concentration of Cu2+ in the solution (mg l− 1), R is the gas constant, and T is the temperature in Kelvin [16]. 2.6. Activation energy The pseudo-second-order rate constant is expressed as a function of temperature by the following Arrhenius type relationship [8]. ln k2 = ln k0 −

Ea RT

ð10Þ

ð3Þ

where, β is a constant related to the mean free energy of adsorption per mole of the adsorbate (mol2 kJ− 2), qm is the theoretical saturation capacity, and ε is the Polanyi potential, which is equal to RT ln(1+ (1/Ce)),

where k2 is the rate constant pseudo-second-order of adsorption (g/(mg min)), ko is the independent temperature factor (g/(mg min)), R is the gas constant (8.314 J mol− 1 K− 1), and T is the solution temperature (K).

N. Ertugay, Y.K. Bayhan / Desalination 255 (2010) 137–142

139

3. Results and discussion 3.1. Effect of contact time on adsorption of Cu2+ by biomass of A. bisporus Depending on the system used, the contact time of the adsorbate with the adsorbent is of great importance [8]. As shown in Fig. 1, Cu2+ uptake was very rapid during the first five minutes. After 5 min, Cu2+ adsorption rates slowly declined. A second equilibrium was established 30 min following the first equilibrium step, while the biomass adsorbed Cu2+. Again, the results indicate that metal sorption was very efficient in the first few minutes of the process. As shown in Fig. 1, the qe value was 3.15 mg g− 1 after the thirtieth minute, while the value for the fifth minute was 2.5 mg g− 1. The difference is probably due to the active site availability near cells, as shown in the second stage with the gradual occupancy of active sites [23]. After the initial period, slow adsorption may be due to slower diffusion of the solute into the interior of the adsorbent. Rapid metal removal has significant practical importance, as it will facilitate the use of small adsorbent volumes, thus ensuring ensure efficiency and economy [2].

Fig. 2. Effect of initial pH on sorption of Cu2+ by A. bisporus (initial metal conc. = 50 mg l− 1, adsorbent conc. = 10 g l− 1, temperature = 20 °C, agitating rate = 150 rpm, contact time = 30 min).

positive metal ion charges, resulting in electrostatic interaction. The A. bisporus at pH 5.0 gave the greatest zeta potential value (Fig. 3). 3.3. Effect of initial Cu2+concentration

2+

3.2. Effect of pH on Cu

uptake

The pH of the aqueous solution is an important controlling parameter in the heavy metal adsorption process [24]. Thus, the role of hydrogen ion concentration was examined from solutions at different pH levels covering a range of 1.0–6.0. The form of Cu2+ can differ depending on forms of aqueous solution, whose stability, in turn, is dependent on system pH. It is apparent that the uptake is quite low at lower pH levels. As shown in Fig. 2, note that the adsorption efficiency increased from 19% at a pH 1.0 up to 63% at pH 5.0. At lower pH values, H3O+ ions compete with metal ions for exchange sites in the adsorbent. Cu2+ uptake decreased because the surface area of the adsorbent was more protonated. Competitive adsorption occurred between H+ protons and free Cu2+ ions and their hydroxide fixation sites [25]. As shown in Fig. 2, the uptake of Cu2+ was decreased at a pH level of 6.0. After pH > 6.0, Cu2+ ions were precipitated, due to hydroxide anions forming a Cu (OH)2 [24]. For this reason, the maximum effective pH value is 5.0. Zeta potential is the electrical potential at the surface of a particle. It can be determined by the measurement of particle velocity in the electric field. At pH levels of 3.0, 4.0, 5.0 and 6.0, the zeta potentials of A. bisporus were − 5.18, −5.2, − 12.2 and −8.12 mV, respectively. Zeta potential values could not be measured at pH 2.0 and 7.0 due to high ionic strength. All samples indicated negative charge values, which should be favorable to the attraction between active sites and

Fig. 1. Effect of contact time on the removal of Cu2+ (adsorbent conc = 10 g l− 1, temperature = 20 °C, agitating rate = 150 rpm, pH = 5.0).

The biosorption of Cu2+ ions was carried out at different initial Cu2+ion concentrations ranging from 30 to 100 mg l− 1 at pH 5.0, 150 rpm and 30 min of contact time using A. bisporus. The results are presented in Table 2, and they show that the equilibrium concentration of Cu2+increased with increasing adsorbate concentration. The study showed that the higher was the initial metal ion concentration, the more metal ion was absorbed per unit weight at equilibrium. Also, the study showed a decrease in the removal efficiency with increasing concentration. When the initial Cu2+concentration was increased from 30 to 100 mg l− 1, the removal decreased from 73.3% to 55.9%. The decrease was due to the saturation of the sorption sites on the adsorbent, as the concentration of the metal increased. However, higher biosorption yields were observed at lower metal concentrations [26]. A higher initial concentration provides an important initial force to overcome pollutant mass transfer resistances between the aqueous and solid phases, thus increases the uptake [27]. 3.4. Adsorption isotherms An adsorption isotherm is characterized by certain constant values, which express the surface properties and affinity of the

Fig. 3. The effect of pH on the zeta potential (initial metal conc. = 50 mg l− 1, adsorbent concentration = 0.5 g l− 1, temperature = 20 °C, agitating rate = 150 rpm, contact time = 30 min).

140

N. Ertugay, Y.K. Bayhan / Desalination 255 (2010) 137–142

The Kf value represents the degree of adsorption in Eq. (2). The increase of Kf values at higher temperatures shows that the adsorption rate decreases with the rise of temperature. The values of 0.1 < 1/ n < 1.0 show that adsorption of hydroquinone on the anion exchanger is favorable [28]. The values of Kf and n constants, and the correlation coefficient for the Freundlich isotherm are presented in Table 3. The calculated results at different temperatures of the Langmuir, Freundlich, Temkin and Dubinin–Radushkevich (D–R) isotherm constants are given in Table 3. The study found that the biosorption of Cu2+ on the A. bisporus biomass correlated well (R2 > 0.98) with the Freundlich equation, as compared to Langmuir, Temkin and Dubinin– Radushkevich (D–R) equation under the concentration range studied. The Freundlich type adsorption isotherm is an indication of surface heterogeneity of the adsorbent, while Langmuir type isotherm demonstrates surface homogeneity of the adsorbent. This leads to the conclusion that the surface of adsorbent is made up of small heterogeneous adsorption patches which are very much similar to each other in adsorption capability. Table 4 compares the results of this study with other similar studies. This study found that metal uptake differences in adsorption capacity are due to the individual properties of each adsorbent, such as structure, functional groups and surface area [29].

Table 2 Effect of initial Cu2+concentration on biosorption yield for A. bisporus (adsorbent conc. =0 g l− 1, temperature=20 °C, pH=5.0, agitating rate=150 rpm, contact time=30 min). Co (mg l− 1)

Ce (mg l− 1)

qe (mg g− 1)

30 50 75 100

8.00 18.50 29.00 44.10

2.20 3.15 4.60 5.59

Table 3 Constant parameters and correlation coefficients calculated for various adsorption models at different temperatures. Isotherm equations

20 °C

Langmuir Q0 (mg g− 1) b (l mg− 1) R2 Freundlich Kf (mg g− 1) 1/n R2 D–R isotherm qm (mg g− 1) β (mol2 kJ− 2) R2 Temkin AT (l g− 1) bT R2

30 °C

50 °C

9.107 0.034 0.9305

9.1157 0.0241 0.9294

11.441 0.0141 0.8153

0.664 0.5608 0.9815

0.4340 0.6278 0.9971

0.307 0.7002 0.9804

4.78 0.00001 0.8023

4.415 0.00002 0.8571

4.254 0.00002 0.8136

3 82.84 0.9494

4.34 124.94 0.9624

3.5. Thermodynamics of biosorption The change in Gibbs free energy (ΔG°) for biosorption of Cu2+ ions onto dried A. bisporus biomass was calculated from Eq. (8). ΔH° and ΔS° were calculated from the slope and intercept of plot of ΔG° against T (Eq. (9)). Thermodynamic parameters calculated as a function of temperature are listed in Table 5. The negative value of ΔH° confirms that the process was exothermic. Further, the free energy ΔG° of the process at all temperatures was negative and decreased with the increase in temperature. This result indicates that the process is spontaneous in nature and the spontaneity increases with the rise in temperature. This further supports the above mechanism [10]. The values found for ΔG° indicate that the extraction of heavy metals on clinoptilolite could be considered as a physical adsorption. As long as chemical adsorption is generally characterized by the range of free energy from 80 to 400 kJ mol− 1, the obtained negative values indicate that the extraction process is exothermic [31].

5.19 212.44 0.9524

Table 4 Maximum capacity, Kf for biosorption of Cu2+ by various adsorbents. Adsorbent

Kf

Reference

CFA–NaOH LS WS RS Fucus serratus Potato peels Agaricus bisporus

19.3 0.648 0.019 0.108 2.544 7.479 0.664

[3] [24] [24] [24] [4] [30] This study

Table 5 Thermodynamic parameters of biosorbent at initial concentration of 50 mg l− 1. Temperature (K)

ΔG° (kJ mol− 1)

ΔH° (kJ mol− 1)

ΔS° (J mol− 1 K− 1)

293 303 323

− 1.29 − 0.81 − 0.20

− 11.64a

− 35.50a

a

3.6. Kinetic studies The kinetics of biosorption of Cu2+ on A. bisporus were studied using two kinetic models: the pseudo-first-order and pseudo-secondorder [32–34]. The linear form plots of pseudo-second-order for the adsorption of different initial Cu2+ ions was obtained at the following temperatures: 20°, 30° and 50 °C. The kinetic parameters for the adsorption of Cu2+ onto A. bisporus are given in Table 6 and the pseudo-second-order plots are given in Fig. 4. Plots for the pseudo-first-order equation (Eq. (5)) are not shown because the correlation coefficients for the pseudo-first-order model are lower than that of the pseudo-second-order model (Eq. (6)).

These values are valid for all temperatures.

adsorbent. It can also be used to compare the adsorptive capacities of the adsorbent for different pollutants. The values of Q0 and b constants and the correlation coefficient for the Langmuir isotherm (Eq. (2)) are presented in Table 3.

Table 6 Comparison of the first and second-order adsorption, and calculated and experimental qe values for different initial Cu2+ concentrations (adsorbent conc. = 10 g l− 1, pH = 5.0, temperature = 20°C, agitating rate = 150 rpm, contact time = 30 min). First-order kinetic model

Second-order kinetic model

Co (mg l− 1)

qe,exp (mg g− 1)

k1 (l min− 1)

qe,cal (mg g− 1)

r2

k2 (g mg min− 1)

qe,cal (mg g− 1)

r2

h (mg g min− 1)

30 50 75 100

2.20 3.15 4.60 5.59

0.165 0.095 0.035 0.108

1.357 1.113 1.130 2.453

0.964 0.857 0.801 0.772

0.162 0.051 0.016 0.010

2.359 3.287 4.852 5.882

0.998 0.995 0.994 0.991

0.901 0.551 0.376 0.345

N. Ertugay, Y.K. Bayhan / Desalination 255 (2010) 137–142

Fig. 4. The plot of the pseudo-second-order adsorption kinetics of Cu2+ on A. bisporus biomass at different initial concentration (adsorbent conc. = 10 g l− 1, pH = 5.0, temperature = 20 °C, agitating rate = 150 rpm, contact time = 30 min).

As seen from Table 6, the pseudo-first-order model is not suitable for modeling the adsorption of Cu2+ onto A. bisporus. In contrast, the application of a pseudo-second-order model leads to much better regression coefficients, all greater than 0.99. Furthermore, the qe values are experimental, as indicated in Table 6. Thus, the pseudosecond-order kinetic model is well suited to model the sorption curves of Cu2+ onto A. bisporus.

141

higher temperatures [36]. Consequently, the study found that the biosorption process was affected by temperature and that the optimum working range was 20 °C for A. bisporus. The magnitude of activation energy explains the type of sorption. Two main types of adsorption can occur, physical or chemical. In physical adsorption, the equilibrium is usually attained rapidly and easily reversible, because the energy requirements are small. The activation energy for physical adsorption is usually not more than 4.2 kJ mol− 1, because the forces involved in physical adsorption are weak. Chemical adsorption is specific and involves forces much stronger than physical adsorption. Therefore, activation energy for chemical adsorption is of the same magnitude as the heat of chemical reactions [34]. A plot of ln k2 versus 1/T gives a straight line, and the corresponding activation energy was determined (50 mg l− 1) from the slope of linear plot (Eq. (10)). The activation energy for the biosorption of Cu2+ A. bisporus was found to be 118.86 kJ mol− 1 (Fig. 6). From the value of activation energy, it appears that the biosorption of Cu2+ on A. bisporus is a chemical adsorption process. This is confirmed from the fact that the activation energy for chemical adsorption is usually more than 4–6 kJ mol− 1 [8].

4. Conclusions 3.7. The effect of temperature and the activation energy To determine the effect of temperature on the biosorption of Cu2+, experiments were also conducted at 20°, 30° and 50 °C. The equilibrium uptake of Cu2+ ions to the A. bisporus biomass (qe) was affected by temperature (T). The sorption of Cu2+ by A. bisporus decreased progressively with the increase in temperature from 20° to 50 °C, as shown in Fig. 5, indicating that the sorption process of A. bisporus biomass was exothermic. The increase in temperature decreases the physical forces responsible for sorption. However, the temperature has two main effects on the sorption process. An increase in temperature is known to increase the diffusion rate of the sorbate across the external boundary layer and within the pores. This could be the result of decreasing solution viscosity. Furthermore, changing the temperature will modify the equilibrium capacity of the sorbent for a particular sorbate [33]. The decrease in adsorption capacity of A. bisporus biomass at higher temperatures (above 20 °C) may be attributed to the deactivation of the adsorbent surface or the destruction of some active sites on the adsorbent surface due to bond rupture [35]. This decrease can be attributed to the deformation of electrode surfaces at

Fig. 5. Equilibrium Cu2+ uptake capacities of A. bisporus at different temperatures (adsorbent conc. = 10 g l− 1, pH= 5.0, agitating rate = 150 rpm, contact time = 30 min).

The study showed that the biosorption process was a function of the adsorbate concentration, pH, and temperature of solution. The sorption capacity was found to increase with the increase of solute concentration. The highest Cu2+ biosorption by A. bisporus biomass was obtained as 73.3% at a pH level of 5.0. The equilibrium of the metal ion sorption is reached within about 30 min. Biosorption of Cu2+ is better suited to the Freundlich adsorption model than calculated under other adsorption models. The adsorption dependence of Cu2+ on temperature was investigated and the thermodynamic parameters ΔS°, ΔH° and ΔG° were calculated. Thermodynamic studies confirmed that the process was spontaneous and exothermic. The pseudo-first-order and pseudo-second-order kinetic models were used to describe the kinetic data for initial Cu2+ and adsorbent concentrations and the rate constants were evaluated. The results indicated that the pseudo-second-order equation provided the best correlation for the adsorption data. The value of adsorption energy, Ea, gives an idea of the nature of adsorption. The activation energy of the Cu2+ adsorption was calculated using the Arrhenius equation. From the value of activation energy, the results of the study conclude biosorption of Cu2+ by A. bisporus was chemical sorption. It can be said that A. bisporus biomass as an alternative biosorbent material has been useful for removal of Cu2+ ions from aqueous solutions.

Fig. 6. Arrhenius plot.

142

N. Ertugay, Y.K. Bayhan / Desalination 255 (2010) 137–142

References [1] E. Malkoc, Y. Nuhoglu, Potential of tea factory waste for chromium(VI) removal from aqueous solutions: thermodynamic and kinetic studies, Separation and Purification Technology 54 (2007) 291–298. [2] B. Zhu, T. Fan, D. Zhang, Adsorption of copper ions from aqueous solution by citric acid modified soybean straw, Journal of Hazardous Materials 153 (2008) 300–308. [3] T.C. Hsu, C.C. Yu, C.M. Yeh, Adsorption of Cu2+ from water using raw and modified coal fly ashes, Fuel 87 (2008) 1355–1359. [4] S. Ahmady-Asbchin, Y. Andre`s, C. Ge´rente, P. Le Cloirec, Biosorption of Cu (II) from aqueous solution by Fucus serratus: surface characterization and sorption mechanisms, Bioresource Technology 99 (2008) 6150–6155. [5] V.J.P. Vilar, C.M.S. Botelho, Boaventura, A.R. Rui, Copper removal by algae Gelidium, agar extraction algal waste and granulated algal waste: kinetics equilibrium, Bioresource Technology 99 (2008) 750–762. [6] X.-m. Li, D.-x. Liao, X.-q. Xu, Q. Yang, G.-m. Zeng, W. Zheng, L. Guo, Kinetic studies for the biosorption of lead and copper ions by Penicillium simplicissimum immobilized within loofa sponge, Journal of Hazardous Materials 159 (2008) 610–615. [7] M. Işık, Biosorption of Ni(II) from aqueous solutions by living and non-living ureolytic mixed culture, Colloids and Surfaces. B, Biointerfaces 62 (2008) 97–104. [8] Z. Baysal, E. Cınar, Y. Bulut, H. Alkan, M. Dogru, Equilibrium and thermodynamic studies on biosorption of Pb(II) onto Candida albicans biomass, Journal of Hazardous Materials 161 (2009) 62–67. [9] A.F. Tajar, T. Kaghazchi, M. Soleimani, Adsorption of cadmium from aqueous solutions on sulfurized activated carbon prepared from nut shells, Journal of Hazardous Materials 165 (2009) 1159–1164. [10] M. Ajmal, A.H. Khan, S. Ahmad, A. Ahmad, Role of sawdust in the removal of copper (II) from industrial wastes, Pergamon PII: S0043-1354(1998) 00067-0. [11] A. Grimm, R. Zanzi, E. Bjönbom, A.L. Cukierman, Comparison of different types of biomasses for copper biosorption, Bioresource Technology 99 (2008) 2559–2565. [12] O. Demirbas, A. Karadağ, M. Alkan, M. Doğan, Removal of copper ions from aqueous solutions by hazelnut shell, Journal of Hazardous Materials 153 (2008) 677–684 (E). [13] P. Kumari, P. Sharma, S. Srivastava, M.M. Srivastava, Biosorption studies on shelled Moringa oleifera Lamarck seed powder: removal and recovery of arsenic from aqueous system, International Journal of Mineral Processing 78 (2006) 131–139. [14] Y. Nuhoğlu, E. Malkoc, A. Gürses, N. Canpolat, The removal of Cu(II) from aqueous solutions by Ulothrix zonata, Bioresource Technology 85 (2002) 331–333. [15] E. Malkoc, Y. Nuhoglu, Determination of kinetic and equilibrium parameters of the batch adsorption of Cr(VI) onto waste acorn of Quercus ithaburensis, Chemical Engineering and Processing 46 (2007) 1020–1029. [16] S. Erentürk, E. Malkoc, Removal of lead(II) by adsorption onto Viscum album L.: effect of temperature and equilibrium isotherm analyses, Applied Surface Science 253 (2007) 4727–4733. [17] R. Crisafully, M.A.L. Milhome, R.M. Cavalcante, E.R. Silveira, D.D. Keukeleire, R.F. Nascimento, Removal of some polycyclic aromatic hydrocarbons from petrochemical wastewater using low-cost adsorbents of natural origin, Bioresource Technology 99 (2008) 4515–4519. [18] M. Akcay, Characterization and adsorption properties of tetrabutylammonium montmorillonite (TBAM) clay: thermodynamic and kinetic calculations, Journal of Colloid and Interface Science 296 (2006) 16–21.

[19] O. Gok, A. Özcan, B. Erdem, A.S. Özcan, Prediction of the kinetics, equilibrium and thermodynamic parameters of adsorption of ions onto 8-hydroxy quinoline immobilized bentonite, Colloids and Surfaces. A, Physicochemical and Engineering Aspects 317 (2008) 174–185. [20] M.D. Mashitah, Y.Y. Azila, S. Bhatia, Biosorption of cadmium (II) ions by immobilized cells of Pycnoporus sanguineus from aqueous solution, Bioresource Technology 99 (2008) 4742–4748. [21] X.-F. Sun, S.-G. Wang, X.-W. Liu, W.-X. Gong, N. Bao, B.-Y. Gao, H.-Y. Zhang, Biosorption of malachite green from aqueous solutions onto aerobic granules: kinetic and equilibrium studies, Bioresource Technology 99 (2008) 3475–3483. [22] C.L. Mack, B. Wilhelmi, J.R. Duncan, J.E. Burgess, A kinetic study of the recovery of platinum ions from an artificial aqueous solution by immobilized Saccharomyces cerevisiae biomass, Minerals Engineering 21 (2008) 31–37. [23] S. Singh, B.N. Rai, L.C. Rai, Ni (II) and Cr (VI) sorption kinetics by microcystis in single and multi metallic system, Process Biochemistry 36 (2001) 1205–1213. [24] H. Aydın, Y. Bulut, C. Yerlikaya, Removal of copper (II) from aqueous solution by adsorption onto low-cost adsorbents, Journal of Environmental Management 87 (2008) 37–45. [25] A. Benhammou, A. Yaacoubi, L. Nibou, B. Tanouti, Adsorption of metal ions onto Moroccan stevensite: kinetic and isotherm studies, Journal of Colloid and Interface Science 282 (2005) 320–326. [26] E. Malkoc, Ni(II) removal from aqueous solutions using cone biomass of Thuja orientalis, Journal of Hazardous Materials B137 (2006) 899–908. [27] Z. Aksu, S. Tezer, Biosorption of reactive dyes on the green alga Chlorella vulgaris, Process Biochemistry 40 (2005) 1347–1361. [28] F. Zha, S. Li, Y. Chang, Preparation and adsorption property of chitosan beads bearing b-cyclodextrin cross-linked by 1, 6-hexamethylene diisocyanate, Carbohydrate Polymers 72 (2008) 456–461. [29] A. Özer, D. Özer, A. Özer, The adsorption of copper(II) ions on to dehydrated wheat bran (DWB): determination of the equilibrium and thermodynamic parameters, Process Biochemistry 39 (2004) 2183–2191. [30] T. Aman, A.A. Kazi, M.U. Sabri, Q. Bano, Potato peels as solid waste for the removal of heavy metal copper(II) from waste water/industrial effluent, Colloids and Surfaces. B, Biointerfaces 63 (2008) 116–121. [31] M. Sprynskyy, Solid–liquid–solid extraction of heavy metals (Cr, Cu, Cd, Ni and Pb) in aqueous systems of zeolite-sewage sludge, Journal of Hazardous Materials 161 (2009) 1377–1383. [32] M. Dundar, C. Nuhoglu, Y. Nuhoglu, Biosorption of Cu(II) ions onto the litter of natural trembling poplar forest, Journal of Hazardous Materials 151 (2008) 86–95. [33] R. Djeribi, O. Hamdaoui, Sorption of copper(II) from aqueous solutions by cedar sawdust and crushed brick, Desalination 225 (2008) 95–112. [34] H. Ucun, Y.K. Bayhan, Y. Kaya, Kinetic and thermodynamic studies of the biosorption of Cr(VI) by Pinus sylvestris Linn, Journal of Hazardous Materials 153 (2008) 52–59. [35] H.D. Ozsoy, H. Kumbur, B. Saha, J. Hans van Leeuwen, Use of Rhizopus oligosporus produced from food processing wastewater as a biosorbent for Cu(II) ions removal from the aqueous solutions, Bioresource Technology 99 (2008) 4943–4948. [36] S. Kılınç Alpat, S. Alpat, B. Kutlu, O. Ozbayrak, H.B. Buyukısık, Development of biosorption-based algal biosensor for Cu(II) using Tetraselmis chuii, Sensors and Actuators B 128 (2007) 273–278.