Journal of Environmental Chemical Engineering 4 (2016) 4587 –4599

Contents lists available at ScienceDirect

Journal of Environmental Chemical Engineering

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

Research paper

Biosorption of lead ions from the aqueous solution by Sargassum filipendula:

Equilibrium and kinetic studies
Ayushi Verma, Shashi Kumar, Surendra Kumar*
Department of Chemical Engineering, Indian Institute of Technology Roorkee, Roorkee, 247 667, Uttarakhand, India

ARTICLE INFO ABSTRACT

Article history:
+2
Received 3 August 2016 The removal of Pb ions by Sargassum filipendula was studied using batch process. The biosorbent characterization was
Received in revised form 5 October 2016 +2
carried out by FESEM-EDX and FTIR techniques. Central composite design was used to optimize Pb ions biosorption
Accepted 23 October 2016 Available online 24 process by varying four different independent process parameters (temperature, pH, biosorbent dosage, and initial
October 2016 +2
concentration of Pb ions). The adequacy of response surface model was checked by analysis of variance (ANOVA). The
+2
optimum process parameters for the removal of Pb ions were found as temperature (34.8 C), pH (4.99), initial concentration
Keywords:
(152.10 mg/L) and biosorbent dosage (0.49 g/L) at which 96% of removal were achieved. The predictive capabilities of six
Biosorption
types of kinetic models and six types of adsorption isotherm models were examined for S. filipendula. For this study, Fritz
Heavy metals +2
Central composite design isotherm model and Bangham kinetic model were found as best fitted models for the biosorption of Pb ions. Desorption
Isotherms studies showed that after four consecutive biosorption-desorption cycles 77.53% and 90.84% of desorption and biosorption
+2
Kinetics efficiency were achieved, respectively. The studied thermodynamic parameters showed that biosorption of Pb ions on S.
filipendula were feasible, spontaneous, and endothermic in nature. Thus, in view of experimental observations it can be
+2
concluded that S. filipendula can be used as an efficient biosorbent for Pb ions biosorption from the aqueous solution.

ã 2016 Published by Elsevier Ltd.

1. Introduction
In recent years, pollution caused through heavy metals is a global problem
due to their toxicity and bioaccumulation in food chain causing a serious
health and ecological problems [1]. Most of the heavy metals released from
various industries are found to be non-biodegradable, which may cause a
significant danger to human health. Among different heavy metals (As, Pb, Cr,
Cu, Co, Zn, Hg, and Ni) lead is a highly toxic metal even at very low
concentrations; lead causes brain damage in children. Lead can cause many
human health effects like damage to kidney, brain, reproductive system, liver,
and central nervous system. Severe exposure to lead results in abortion,
sterility, stillbirths and neo-natal deaths. Therefore, it is important to remove
lead from industrial wastewater and discharges.
+2
In industrial effluents as shown in Table 1, Pb ions concentration
approaches to as high as 200–500 mg/L; this concentration is very high in
comparison to standards described by WHO. The maximum limits of
discharge for lead ion in
* Corresponding author.
E-mail addresses: skumar.iitroorkee@gmail.com, skumar@iitr.ac.in (S. Kumar).
wastewater is 0.05 mg/L and sewage slurry applied to agriculture land is 420
mg/L as set by the Environment protection Agency [8,9]. Thus, the
concentration of lead-ion in wastewaters must be reduced to a level of 0.05
mg/L before discharging to waterbodies [10,11]. There are various
+2
conventional methods used for the removal of Pb ions from industrial
wastewater. These methods are ion exchange, precipitation, filtration, reverse
osmosis, membrane separation, evaporation, electrochemical treatment, and
adsorption by activated carbon. But these conventional methods possess
+2
several disadvantages as they are expensive, ineffective when Pb ions are
present in low concentration and generates large amount of secondary waste
(sludge) which is difficult to treat [12–15]. In comparison to the conventional
+2
physico-chemical methods, biosorption is revealed to be promis-ing for Pb
ions removal from industrial wastewater because of its low cost, high
+2
adsorption efficiency at low Pb ions concentration, sludge free method with
high efficiency and affinity, short operation time, possibility of metal recovery,
and biosorbent regeneration [16,17].
+2
Biosorption involves the passive uptake of Pb ions by inactive/ dead
biological materials like bacteria, fungi, and algae. The main mechanisms
+2
responsible for Pb ions accumulation by biosorb-ents involve ionic
interactions and complex formation between

http://dx.doi.org/10.1016/j.jece.2016.10.026
2213-3437/ã 2016 Published by Elsevier Ltd.
4588 A. Verma et al. / Journal of Environmental Chemical Engineering 4 (2016) 4587–4599

Table 1
+2
Level of Pb ions in wastewater of various industries.
S. No. Industry +2 Reference
Pb ions concentration in wastewater (mg/L)
1 Chemical manufacturing plant, Glubczyce (Poland) 326.4 [2]
2 NM 200–500 [3]
3 Oil 125–150 [4]
4 Battery manufacturing plant 5–15 [5]
5 Electroplating 116.42 [6]
6 Industrial plant 19.1 [7]

NM: Not mentioned.

+2 2.2. Characterization techniques

Pb ions and ligands present on biosorbent surface. The marine algae are
proved to be more effective for metal binding activity because of their low
cost, high capacity of metal biosorption, and renewable nature [18–20]. To determine the surface morphology of biosorbent and its composition,
Marine algae, usually known as seaweeds, are abundantly available in many FESEM-EDX (FESEM QUANTA 200 FEG from FEI Netherland) analytical
+2
parts of the world and it can be obtained economically from the ocean at a instrument was used. The biosorbent before and after biosorption of Pb ions
large scale was subjected to analysis by the instrument.
+2
[21]. They can efficiently remove very low concentration of Pb ions
ranging from few ppm to several hundred ppm [22]. There are three types of FTIR spectra for both raw form and lead treated S. filipendula were
algae, red (Rhodophyta), brown (Phaeophyta), and green (Chlorophyta). obtained by KBr pellets method using Fourier Transform Infrared
Among these, brown algae are proved to be more efficient for biosorption of Spectrometer (Thermo Scientific, India), which was used for IR spectral
+2
Pb ions because of their acidic polysaccharide content which are present in studies of biosorbent. For these studies, the dry sample was mixed with KBr
their cell wall. The effectiveness of biosorption to remove Pb ions depends
+2 in 1:10 ratio and made into pellets to observe the functional groups existing in
on the pH of the solution, effluent composition, biosorbent concentration, the S. filipendula.
reaction temperature and kinetics [23–25]. Compared to different types of
marine alga, biosorptive performance shown by Sargassum genus of brown 2.3. Preparation of metal solution
+2
alga is proved to be the best due to its high biosorption capacity for Pb ions
at a low equilibrium concentra-tion [26]. This genus of brown alga is widely The stock solution of 1000 mg/L was prepared by dissolving 1.56 g Pb
distributed in most of the tropical countries and is available in large quantities (NO3)2 in deionized water. The test solutions of various concentrations were
as a waste seaweed biomass [27–30]. The main constituents of Sargassum sp. +2
prepared by diluting the stock solution. The initial pH of Pb ions solution
brown alga are polysaccharides alginate, usually Ca and Na alginates [31–
+2
was controlled by using 0.1 M NaOH and 0.1 M HNO3.
33]. Thus it has a high efficiency to accumulate Pb ions in comparison to
alga of other genera [34].
2.4. Batch biosorption experiments

The main objective of this work was to remove lead ions from aqueous
solution by using dried form of dead marine algae, S. filipendula. The
experiments were planned to be conducted according to design of
experiments using Response Surface Methodology (RSM). The effect of
+2
temperature, pH, initial Pb ions concentration and biosorbent dosage were
examined. The isotherm and kinetic models were fitted to experimental data.
Thermodynamic study (determination of DG and DS ) was carried out to
judge the feasibility of the process. Desorption study was also done to
ascertain the regeneration capacity of the biosorbent. All the results of
biosorption capacities of different brown seaweeds, isotherms, kinetic, and
thermodynamic studies were compared with the reported results in the
literature to make the present study complete.
2. Materials and methods
2.1. Biomass preparation
The dried form of S. filipendula was purchased from Aushadh Agri
Science Private Limited, Gujarat (India) at the rate of Rs 80/kg dry wt. The
+2 +
impurities and ions such as Ca or Na present on the surface of biosorbent,
which can affect the biosorption process, were removed by washing the
biomass with abundant quantity of deionized water several times. After that, it
was dried at 80 C for 24 h and kept in the desiccator. The dried alga was then
grounded in a blender. The grounded alga was sieved through 212 mm sieve
and the undersize fraction thus obtained was used as biosorbent for
biosorption process.
All the batch biosorption experiments were conducted to observe the
+2
effects of several experimental parameters like temperature, pH, initial Pb
ions concentration, biosorption time, and biosorbent dosage on the removal of
lead. The biosorption experiments were conducted in Erlenmeyer flasks of
250 mL by agitating specified amount of biosorbent in 50 mL of lead solution
with different process parameters for 85 min at 150 rpm in an incubator-
shaker (Metrex Scientific Instruments Private Limited, India). The
optimization of lead biosorption was studied by varying important reaction
+2
parameters such as pH (2.0–5.0), temperature (25–35 C), initial Pb ion
concentration (100–300 mg/L), and biosorbent dosage (0.2–0.5 g/L). In all
the experiments, samples were collected after a regular interval of time. In
+2
order to determine the concentration of Pb ions in the solution, the treated
solution was filtered with Whatman No. 1 filter paper. The filtrate was
+2
examined for residual Pb ions concentration using Flame Atomic
Absorption Spectrophotometer (GBC Avantha, Germany) and quantified
against known standard solution of lead. Whenever it was necessary, the
samples were diluted with distilled water to improve accuracy of estimation.
All the experi-ments were conducted in triplicate and the results were
statistically analyzed. The results were expressed in terms of% removal of
+2
Pb ions, as given below by the equation:
(1)
% Removal = ((Co Ce)/Co) 100
The biosorption capacity qe of a biosorbent is the amount of metal
biosorbed per unit amount of biosorbent (mg/g) at equilibrium. It can be
obtained by using Eq. (2):
qe = (Co Ce) V/m (2)
 A. Verma et al. / Journal of Environmental Chemical Engineering 4 (2016) 4587–4599 4589

+2 The total 30 batch experiments (16 + 8 + 6) designed from CCD were

The amount of biosorbed Pb ions per unit mass of biosorbent at any
time t (qt, mg/g) was obtained by using the following equation:
(3)
qt = (Co Ct) V/m
In Eqs. (1)–(3) Co is initial concentration of metal ion, Ce is equilibrium
concentration of metal ion and C t is concentration of metal ion at any time t in
the solution (mg/L), V is volume of solution (L), m is mass of biosorbent (g).
+2
The experiments for kinetic study of Pb ions biosorption on S.
filipendula were performed at 35 C by using five different initial
+2
concentrations of Pb ions: 100, 150, 200, 250, and 300 mg/L. In each flask,
a fixed amount of biosorbent (0.5 g/L) was added. The pH of solution was
adjusted at 5.0 by adding 0.1 M NaOH or 0.1 M HNO 3 as necessary. After
specified time interval, the samples were withdrawn and filtered immediately
to stop the biosorption process. The filtrate samples were analyzed by using
+2
AAS to estimate the remaining concentration of Pb ions in the solution, Ct.
+2
In order to determine Pb ions biosorption isotherms at different
temperatures, experiments were performed at four different temperatures (20,
25, 30 and 35 C) by varying initial concentration from 100 to 300 mg/L with
constant biosorbent dosage of 0.5 g/L. These experimental data with different
values of Ce for each run were fitted to six isotherm models and model
2
parameters with the value of R were obtained by using curve fitting tool of
MATLAB 2013 on Window XP. The normalized standard deviation between
experimental and predicted values for each isotherm model was determined to
discriminate amongst the competing models.
The thermodynamic study has been carried out to assess the feasibility of
+2
Pb ions biosorption on S. filipendula. For this purpose, the biosorption of
+2
Pb ions was performed at four different temperatures: 20, 25, 30 and 35 C
by keeping all the other biosorption process parameters constant such as
+2
biosorbent dosage (0.5 g/L), initial concentration of Pb ions (150 mg/L) and
pH (5.0).
2.5. Experimental design
RSM is a well-known mathematical technique which is used to design the
experiments, develop models and evaluate the effects of variables on a
response variable of interest. The aim is to optimize this response and to
obtain optimum values of variables [35]. In order to statistically design the
experiments and calculate the interactive effects of four independent
parameters (pH, tempera-ture, biosorbent dosage, and initial metal
concentration) for optimizing the biosorption of lead on S. filipendula, a full
factorial central composite design (CCD) with a quadratic model was used
k noticed when S. filipendula samples were exposed to Pb (NO 3)2 solution.
[36]. In general, the total number of runs required for CCD are (2 + 2k +
k Some of the cations initially present on cell wall matrix were replaced with
N0), where k is number of variables, 2 are factorial points, 2k are axial points
and N0 is number of experiments carried out at the center [37]. The lower and
higher levels of four parameters are given in Table 2.
conducted in triplicate with six replicates of the center points and the average
value was reported. CCD model with the response under different operating
conditions are given in Table 3. The experimental design and the analysis of
data were done by using ‘Design Expert’ software (Version 9.0, Stat-Ease,
Inc., Minneapolis, USA).
In order to correlate responses with four independent variables, a second
degree polynomial equation, given below, was used:
k k 2 k k
Y ¼ bo þ S i¼1 bixi þ S i¼1 biixi þ S i¼1 S j>1 bij xixj ð4Þ
where Y is predicted response (dependent variable), bo is constant coefficient,
xi and xj are variables, bi, bii and bij are interaction coefficients for linear,
quadratic, and second order terms, respectively.
The optimum value of selected variables was achieved by resolving the
regression equation and by examining the 3D response graph. The adequacy
of each model was checked by Analysis of Variance (ANOVA) and the quality
2
of polynomial model fitness was indicated by correlation coefficient (R ) [38–
40].
2.6. Desorption/regeneration method
The recycling of biosorbent is a most important step from economical
point of view. Hence biosorption-desorption process were carried out up to 4
+2
cycles by adding 0.5 g of Pb ions loaded S. filipendula in 50 mL of 0.2 M
HCl for each cycle. A single cycle sequence comprises of biosorption
followed by desorption. In order to reuse the biomass for next cycle, the
biomass was washed with 0.2 M HCl solution and distilled water,
consecutively. The desorption efficiency was given by the following equation:
Amount of desorbed metal ion
Desorption efficiency ð%Þ ¼ Amount of biosorbed metal ion 100
ð5Þ
3. Results and discussion
3.1. Characterization of S. filipendula
3.1.1. FESEM – EDX analysis
Fig. 1(a) shows the raw form of S. filipendula before biosorption. Fig.
+2
1(b) shows that after biosorption of Pb ions the pores and surface of S.
filipendula were covered and the surface became smooth. It is evident that the
structure of S. filipendula has changed after biosorption.
+2
EDX analysis of biosorbent before and after biosorption of Pb ions
+2
confirms this observation as shown in Fig. 2(a & b). A peak of Pb ions was
+2
Pb ions and created a strong cross linkage. EDX image shows that the main
component of S. filipendula cell wall was C along with small amounts of Mg,
Na, S, Ca, and K.

3.1.2. FTIR analysis

The FTIR study was carried out to detect the functional groups present on
Table 2 the biosorbent surface and their interaction with metal ions. Fig. 3 shows the
Range and level of the independent variables. peaks corresponding to functional groups of S. filipendula biomass before and
Independent variables Range and levels (coded) after biosorption of lead ions. Table 4 shows the change in vibrational
+2
a 1 0 +1 +a frequency of functional groups of S.filipendula after biosorption of Pb ions.
Temperature, C (A) 20 25 30 35 40
1
Initial concentration, mg/L (B) 75 150 225 300 375 The biosorption peak at 3407.9 cm corresponds to stretching of OH
Biosorbent Dosage, g/L (C) 0.05 0.2 0.35 0.5 0.65 1 1
group shifted to 3405.9 cm , 2925.35 cm corresponds to stretching of OH
pH (D) 2 3 4 5 6 1 1
group and C H group shifted to 2924.3 cm , 1633.89 cm corresponds to
stretching of C¼C
4590 A. Verma et al. / Journal of Environmental Chemical Engineering 4 (2016) 4587–4599

Table 3
+2
Experimental design based on CCD and its response for Pb ions removal.

Run Temperature Initial concentration Biosorbent dosage pH Removal (%)

( C) (mg/L) (g/L)
Experimental Predicted
1 25 150 0.2 3 33.98 33.33
2 35 150 0.2 3 41.64 43.85
3 25 300 0.2 3 16.48 17.78
4 35 300 0.2 3 34.9 29.46
5 25 150 0.5 3 61.84 64.47
6 35 150 0.5 3 78.56 80.65
7 25 300 0.5 3 33.67 36.00
8 35 300 0.5 3 54.17 53.33
9 25 150 0.2 5 42.68 45.58
10 35 150 0.2 5 57.33 52.83
11 25 300 0.2 5 29.26 25.00
12 35 300 0.2 5 33.97 33.40
13 25 150 0.5 5 80.59 83.85
14 35 150 0.5 5 96.50 96.76
15 35 300 0.5 5 50.49 50.34
16 35 300 0.5 5 65.94 64.41
17 20 225 0.35 4 40.96 37.22
18 40 225 0.35 4 57.95 61.80
19 30 75 0.35 4 92.34 87.93
20 30 375 0.35 4 35.50 40.03
21 30 225 0.05 4 12.78 17.23
22 30 225 0.65 4 83.71 79.38
23 30 225 0.35 2 31.18 29.31
24 30 225 0.35 6 50.64 52.63
25 30 225 0.35 4 53.53 53.21
26 30 225 0.35 4 51.53 53.21
27 30 225 0.35 4 54.53 53.21
28 30 225 0.35 4 53.59 53.21
29 30 225 0.35 4 52.53 53.21
30 30 225 0.35 4 53.53 53.21

+2
Fig. 1. FESEM images for Pb ions biosorption on S. filipendula (a) Before biosorption (b) After biosorption.

1 1
group shifted to 1628.96 cm , 1426.39 cm corresponds to C H group
stretching and C¼C group bending shifted to 1417.63 cm
1
and 606.88 cm
1 3.2. Effect of contact time
1 1
corresponds to C Cl group shifted to 622.57 cm . The peaks at 1245.13 cm
1 It was noticed experimentally that initially biosorption rate was very high
and 1048.13 cm corresponds to C O groups stretching are shifted to 1250.90
1 1 1
and 80% removal efficiency has been achieved within initial 15 min.
cm and 1049.47 cm . The new peak at 3140.54 cm corresponds to OH Thereafter the biosorption rate was gradually decreased with time until it
group stretching appears. The change in vibrational frequency of functional reaches the equilibrium (Fig. 4). It is due to the fact that initially large surface
+2
groups after biosorption of Pb ions shows that these groups are involved in area of biosorbent was available for biosorption of metal ions but after a
biosorption process certain time period accessibility of active sites on biosorbent surface
[41]. decreases which slows down the rate of biosorption [13]. The equilibrium
 A. Verma et al. / Journal of Environmental Chemical Engineering 4 (2016) 4587–4599 4591

+2
Fig. 2. EDX images for Pb ions biosorption on S. filipendula (a) Before biosorption (b) After biosorption.

+2
time for Pb ions biosorption onto S. filipendula was 40 min at which
+2
Before biosorption 96.54% removal efficiency of Pb ions was achieved.
0.6
After biosorption +2
0.5 3.3. Experimental design and factorial model for Pb ions biosorption
process
Absorbance

0.4
In the experimental design, the selected range and level of variables were
0.3 +2
selected on the basis of literature reported for Pb ions biosorption by other
brown algae. The optimized conditions of higher biosorption efficiency for
0.2 +2
Pb ions were analyzed by using CCD under RSM. The matrix of four
0.1 variables pH, initial concentration, biosorbent dosage, and temperature of
+2
Pb ions were varied at 5 levels (-2, 1, 0, +1, +2). The higher and lower
0.0 3500 3000 2500 2000 1500 1000 500 levels of variables were symbolized as ‘+’ and ‘-’, respectively. Removal
+2
efficiency (%) of Pb ions obtained from the experiments at the end of
4000 equilibrium time for each experiment is presented in Table 3. The
Wavenumber (cm -1) mathematical expression of relationship of four independent variables with
response is given as:
+2
Fig. 3. FTIR image of S. filipendula surface before and after biosorption of Pb ions.
4592 A. Verma et al. / Journal of Environmental Chemical Engineering 4 (2016) 4587–4599

+2
where Y is percent removal of Pb ions and A, B, C and D are coded values of
+2
temperature ( C), initial concentration (mg/L) of Pb ions, biosorbent dosage
2 2 2 2
(g/L), and pH, respectively. A , B , C and D are the measure of main effect
+2
of variables such as temperature ( C), initial concentration (mg/L) of Pb ions,
biosorbent dosage (g/ L), and pH, respectively. Whereas, AB, BC, CD and AD
+2
represent interaction effect of temperature and initial concentration of Pb
+2
ions, initial concentration of Pb ions and biosorbent dosage,

Table 5
ANOVA results for response surface quadratic model.

Table 4
+2
IR vibration wavenumber and functional groups observed on untreated and Pb ions treated S. filipendula biomass.
1 Functional groups
Wavenumber (cm )
Unloaded biomass Metal ion loaded biomass
3407.9 3407.15 OH stretching
– 3140.54 OH stretching
2925.35 2924.43 CH & OH stretching
1633.89 1628.96 C¼C stretching
1426.39 1417.63 C H stretching & C¼C bending
1245.13 1250.9 C O stretching
1048.13 1049.47 C O stretching
606.88 622.57 C Cl stretching

biosorbent dosage and pH, temperature and pH, respectively. The

120 six runs were replicated for central point.
100 The statistical significance and interaction of factors are
fi
determined by ANOVA. Table 5 shows the regression coef cient
80 and analysis of variance of second-order polynomial models. The
p-value (P < 0.0001) and F-value (53.94) shows that the model is
 60 significant. The “Lack of fit F-value” of 21.36 shows that Lack of fit is
Removal40 that the deviation between experimental and predicted values is
significant. A low value of coefficient of variance (CV) 7.73 indicates
%
low. The goodness of fit of the model is tested by coefficient of

20 2 2
determination (R ). The R value close to 1.0 show that the model is
0 2
more significant. For this model R value is found to be 0.98 which
0 20 40 60 80 100 shows that more than 98% of the experimental data are compatible
2
Time (min) with predicted data. The value of predicted R (0.88) is in reasonable
+2 2
Effect of contact time on biosorption of Pb ions by S. filipendula (pH 5.0, agreement with adjusted R value (0.96). Adequate precision
Fig. 4. measures the ratio of signal to noise. A ratio greater than 4 is
+2
temperature 35 C, biosorbent dosage of 0.5 g/L, initial concentration of Pb ions desirable [42]. In this work, the ratio was 28.41 which indicate an
150 mg/L).
adequate signal. The value of Prob. > F less than 0.050 indicates that
+2
Y = + 53.21 + 6.15A 5.83D + 0.29AB + 1.42AC 0.82 the model terms are significant. Here, for biosorption of Pb ions A,
2 2
11.98B + 15.54C + 2 2 2 B, C, D, B , D and BC were significant model terms. The p-value
AD
3.23BC 1.26BD + 1.78CD 0.92A + 2.69B 1.23C 3.06 2 2
D2 (6) greater than 0.10 shows that model terms A , C , AB, AC, AD and BD
are not significant. Fig. 5 shows that the predicted response values
of reduced quadratic model are well in agreement with actual ones in the
+2
range of operating variables. The 3D graphs for Pb ions removal efficiency
are presented in Fig. 6. The pH of the solution plays a significant role in the
protonation of functional group present on biosorbent surface. Fig. 6 (a)
+2
illustrates the effect of pH on removal efficiency of Pb ions. It is noticed
+2
that removal efficiency of Pb ions increases with the increase in pH from 3
to 5. At low pH, the biomass surface becomes positively charged due to

Source Sum of square df Mean square F value p-value Remarks

Model 11832.02 14 845.14 53.94 <0.0001 Significant
A-Temperature 906.51 1 906.51 57.86 <0.0001 Significant
B-Initial concentration 3442.09 1 3442.09 219.69 <0.0001 Significant
C-Dosage 5793.31 1 5793.31 369.76 <0.0001 Significant
D-pH 815.97 1 815.97 52.08 <0.0001 Significant
AB 1.35 1 1.35 0.086 0.7735
AC 32.04 1 32.04 2.04 0.1732
AD 10.69 1 10.69 0.68 0.4217
BC 167.06 1 167.06 10.66 0.0052 Significant
BD 25.35 1 25.35 1.62 0.2227
CD 50.91 1 50.91 3.25 0.0916
2
A 23.39 1 23.39 1.49 0.2406
2
B 198.88 1 198.88 12.69 0.0028 Significant
2
C 41.23 1 41.23 2.63 0.1256
D2 256.8 1 256.8 16.39 0.0011 Significant
Residual 235.02 15 15.67
Lack of fit 229.64 10 22.96 21.36 0.0017 Significant
Pure error 5.38 5 1.08
Total 12067.03 29

R2 = 0.9805; Adjusted R2 = 0.9623; Predicted R2 = 0.8897; Adequate precision = 28.415.

 A. Verma et al. / Journal of Environmental Chemical Engineering 4 (2016) 4587–4599 4593

+2
120 positively charged metal ions. At pH greater than 5, precipitation of Pb ions
occurs as lead hydroxides [43].
(%)
100
The biosorbent dosage has a great impact on biosorption process at a
60 specified initial metal ions concentration. The effect of biomass dosage on
remo val

+2
80 removal efficiency of Pb ions has been studied by changing biosorbent
Predicted

40 dosage from 0.2 to 0.5 g/L and the results are presented in Fig. 6(a). It is
+2
observed that Pb ions removal efficiency increases with increase in dosage
of S. filipendula. This trend is due to the availability of more active sites
20 available on S. filipendula surface [45].

0 +2
The effect of initial concentration on Pb ions removal efficiency has
been studied in the range 150–300 mg/L. The results are shown in Fig. 6(b).
0 20 40 60 80 100 120 +2
The removal efficiency of Pb ions decreases on increasing the initial
Actual removal (%) +2
concentration of Pb ions. It could be possible that all biosorbents have
+2 certain number of active binding sites which are accessible for binding of
Fig. 5. Correlation of actual versus predicted removal of Pb ions by S. filipendula.
metal ions at low initial concentration while at high initial concentration the
binding sites become saturated [46].
which repulsion for binding of metal ions occurs [43,44]. With rise in pH of
+ +2
the solution, the concentration of H ions decreases and negatively charged Fig. 6(c) illustrates the effect of temperature on Pb ions removal
ligands like phosphate, carboxyl, and amino groups present on biomass efficiency. It has been noticed that there is an increase in removal efficiency of
+2
surface is exposed because of deprotonation of metal binding sites which can Pb ions with rise in temperature from 25 to 35 C indicating that the reaction
interact with +2
for Pb ions biosorption is

100 100

80 80

60 60
Removal (%)

Remova
40 40
l (%)
20 20

0
0
5 0.5 5 300

4.5 0.44 4.5 270

4 0.38 4 240
0.32 210
3.5 0.26
pH Biosorbent dosage (g/L) pH 3.5 180 Initial concentration (mg/L)
3 0.2 3 150

(c) (d)

100
25 35 150 300
80
A:Temperature = 34.8529 B:initial concentration = 152.107

60

40
Remova
l (%) 20
0.2 0.5 3 5
0
C:dosage = 0.499904 D:pH = 4.99992
Desirability = 1.000

5 35
4.5 33
4
29
31
12.78 96
3.5 27
pH Temperature (degree celsius) removal = 96.0077
3 25

+2
Fig. 6. (a) Interactive effect of pH and biosorbent dosage (b) Interactive effect of pH and initial concentration of Pb ions (c) Interactive effect of pH and temperature (d) Desirability ramp for
numerical optimization of four independent variables and the responses.
4594 A. Verma et al. / Journal of Environmental Chemical Engineering 4 (2016) 4587–4599

endothermic in nature. On increasing temperature, the thickness of layer that 3.5.3. Elovich model
surrounds the biosorbent decreases. This results in the decrease of external This model is expressed as follows [51]:
layer resistance. Micro-pores become widen and deepen which provide more ð13Þ
dqt ¼ aexpð bqt Þ
surface area for biosorption and the increased availability of active sites in the
dt
biosorbent [47].
Simplifying Eq. (13) in form of Eq. (14) by considering ab >> 1 and with
3.4. Optimization using the desirability function initial conditions t = 0, qt = 0; t = t, qt = qt one obtains [52]:
1 1 ð14Þ
To obtain the maximum point for desirability function, numerical
qt ¼ b lnðabÞ þ b lnðtÞ
optimization was done by fixing the values of reaction parameters within their
+2
ranges and maximizing the removal efficiency of Pb ions [38]. It can be where both a and b are constants and their values are determined from
seen in Fig. 6(d), that the best local maximum value is noticed at initial the linear plot of qt vs. ln t. The constant a (mg/g. min) indicates initial rate of
+2
solution pH of 4.99, temperature of 34.85 C, initial Pb ion concentration of biosorption, b (g/mg) is associated with the extent of surface coverage and
+2 +2
152.10 mg/L, and biosorbent dosage of 0.5 g/L. In this condition, Pb ions activation energy for chemisorption and q t (mg/g) is amount of Pb ions
removal efficiency and the desirability value are found to be 96.0% and 1.0, biosorbed at time t (min).
respectively. This optimum condition has been tested experimentally and
results reveal that removal efficiency is 96.5%. The high degree of agreement
between the predicted optimum conditions and repeated experimental results 3.5.4. Bangham model (Pore diffusion model)
shows that RSM can be used as an efficient and reliable tool to evaluate and Bangham model was used to determine whether the bio-sorption of Pb
+2
+2
optimize the effects of biosorption parameters on Pb ions removal efficiency ions on S. filipendula is pore diffusion or not. The equation for this model is
using S. filipendula. given below:
ln ln Co komþ aolnðtÞ ð15Þ
¼ ln
Co qt m V
3.5. Biosorption kinetics are constants which are calculated from the
where ao (<1) and ko
intercept and slope of the straight line plot of
The biosorption mechanism and rate controlling step are investigated by
h i
ln ln Co qt m vs: l nðtÞ[53].
Co
using six kinetic models as discussed below:

3.5.5. Intraparticle diffusion model

3.5.1. Pseudo first order +2
This model is expressed as follows [48–50]: In intraparticle diffusion there is a migration of Pb ions from liquid
phase to the solid phase. According to Weber and Morris
dqt ¼ k1ðqe qt Þ ð7Þ theory, equation for this model is given below [53,54]:
dt 0.5 (16)
qt = Kid t + C
Integration of Eq. (7) with initial conditions, t = 0, qt = 0; t = t, qt = qt gives: 0.5
where C is constant, Kid is intraparticle diffusion rate constant (mg/ g min ).
0.5
ð8Þ If the plot of qt vs. t shows a linear relationship then biosorption process
ln ðqe qt Þ ¼ ln qe k1:t involves the intraparticle diffusion. In intra-particle diffusion the uptake is
0.5
qe ¼ 1 ðÞ proportional to t instead of time t. The values of Kid and C are obtained
0.5
from the slope and intercept of plot q t vs. t , respectively. The value of
ln qe qt k:t 9 intercept C is proportional to boundary layer thickness. It implies that larger
the intercept more will be the boundary layer effect. The value of C equal to
1
where k1 (min ) is pseudo first order biosorption rate constant. zero shows that the intraparticle diffusion is the rate controlling step.

The value of k1 is calculated from the slope of plot of ln qe qt vs:t:

qe

3.5.2. Pseudo second order

3.5.6. Modified freundlich model
This model is expressed as follows [49,50]: Kuo and Lotse [53,55] developed the Modified Freundlich equation for
dqt
2 ð10Þ
kinetics of biosorption. This model is expressed as follows:
dt ¼ k2ðqe qt Þ
1
Integration of Eq. (10) with initial conditions, t = 0, qt = 0; t = t, qt = qt gives: ð17Þ
qt ¼ ðk3CoÞt m1

1 ð18Þ
t 1 1 t ð11Þ
¼ 2 þ
q k2 q e q lnðtÞ
t e lnqt ¼ lnk3Co þ
m1
1 1 Þqe 2 1 ð12Þ
where k3 is uptake rate constant (L/g min), t is contact time (min), m 1 is Kuo-
ð
¼ Lotse constant. The values of k3 and m1 are used to find out the effect of ionic
qt qe k2t strength and surface loading in biosorption process.
where k2 (g/mg min) is pseudo second order biosorption rate constant. The
The best fitted kinetic model is chosen on the basis of correlation
value of k2 is evaluated from the slope of plot of
ð
1 1
Þvs: :
1
coefficient (R2) and normalized standard deviation
qtqet
 A. Verma et al. / Journal of Environmental Chemical Engineering 4 (2016) 4587–4599 4595

(Dq%) estimated according to Eq. (19). at a constant temperature, there is no contact between the biosorbed
molecules and all vacant sites on biosorbent surface, and all active sites are of
Normalized standard deviationðDq%Þ same intensity [56,57,60]. The Langmuir isotherm model equation is as
vffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi follows:
ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
ffiffiffiffiffiffiffiffiffiffiffiffiffi qe ¼ qobCe ð20Þ
100u X
½

q q =q &2 19 1 þ bCe
eðexpÞ eðpredÞ eðexpÞ
N

where qo (mg/g) is maximum biosorption capacity i.e. the maximum amount

u

¼ t
In Eq. (19), qeðexpÞ is the experimental qe and qeðpredÞ is the corresponding
predicted qeaccording to the equation under study with the best fitted
parameters, N is the number of measurements. Lower the values of Dq%, the
2
better are the fit of experimental data. The values of parameters, R and Dq%
for all the kinetic models are evaluated and given in Table 6 (values for
Pseudo first order and Pseudo second order have not been mentioned as their
2 2
R values are very much lower). The R values for Bangham, Elovich,
Modified Freundlich, and Intra particle diffusion models are greater than 0.90
while the value of normalized standard deviation (Dq%) is low (1.36) in case
of Bangham model in comparison to other kinetic models (Table 6).
According to these results, it can be concluded that Bangham model gives a
+2
good correlation for Pb ions biosorption on S. filipendula.
3.6. Biosorption isotherm model study
ð Þ
+2
of Pb ions biosorbed per gram of S. filipendula to form a complete
monolayer on surface, b (L/mg) is biosorption equilibrium constant.
3.6.2. Freundlich isotherm
+2
This model is applicable to multilayer biosorption of Pb ions on a
heterogeneous surface [57,61]. The equation for this model is given below:
qe ¼ kf Ce
1=n ð21Þ
where kf and n are Freundlich constants which represent the biosorption
capacity and biosorption intensity, respectively [62]. According to this model,
the value of 1/n should lie between 0 and 1 for good biosorption. The
limitation of this isotherm model is that it does not obey Henry’s law at low
concentration and doesn’t reach a maximum biosorption at high
concentration.

Biosorption isotherm describes the relationship between amount of 3.6.3. Redlich-Peterson isotherm
biosorbate biosorbed per unit mass of biosorbent qe (mg/g) at equilibrium and This model involves the features of both Langmuir and Freundlich
biosorbate concentration in the bulk phase at equilibrium Ce (mg/L). isotherm equations [57,61]. The equation for this model is given below:
Biosorption isotherm gives the evidence about biosorption capacity of
biosorbent or amount of biosorbent required to adsorb a unit mass of K1Ce ð22Þ
qe ¼
biosorbate [61]. The experimental data are assessed using six different b
isotherm models namely Langmuir, Freundlich, Radke-Prausnitz, Redlich- 1 þ K 2 Ce
Peterson, Fritz and Toth isotherm models. Out of these isotherms, Langmuir
where K1 and K2 are Redlich-Peterson isotherm constants and b is Redlich-
and Freundlich both are two parameter models, Radke-Prausnitz, Toth, and
Peterson isotherm exponent which lies between 0 and 1. For b = 1 this model
Redlich-Peterson are three parameter models, and Fritz is four parameter b
model. is converted to Langmuir isotherm, for K 2 Ce >> 1, it becomes Freundlich
b
isotherm, and for K2 Ce << 1 it obeys Henry’s law.

3.6.1. Langmuir isotherm

This model relies on the assumptions that a monolayer of biosorbate is
biosorbed above homogenous surface of biosorbent

Table 6
+2
Kinetic models parameter for Pb ion biosorption using S. filipendula.
Kinetic model Parameters Initial concentration (mg/L) Dq%
100 150 200 250 300
Elovich qe (mg/g) 198 289.22 336.32 363.78 393.6 1.94
qt (mg/g) 200.789 297.903 330.11 371.584 393.675
5 3 4 3 2
a 1.628 10 8.364 10 1.86 10 2.297 10 6.24 10
b 0.067 0.033 0.0324 0.022 0.0169
0.98 0.92 0.94 0.95 0.95
R2
Bangham qe (mg/g) 198 289.22 336.32 363.78 393.6 1.36
q (mg/g) 196.831 291.083 329.069 370.407 396.725
t

ao 0.355 0.3792 0.219 0.2491 0.289

ko 89.32 68.392 67.139 46.06 31.04
0.94 0.90 0.93 0.95 0.968
R2
Intraparticle diffusion model qe (mg/g) 198 289.22 336.32 363.78 393.6 5.72
qt (mg/g) 206.093 309.757 344.461 389.363 418.86
0.5 6.73 13.96 14.92 21.24 27.96
Kid (mg min /g)
C 147.81 188.86 215.25 205.42 176.72
2 0.90 0.89 0.98 0.94 0.95
R
Modified Freundlich qe (mg/g) 198 289.22 336.32 363.78 393.6 2.79

qt (mg/g) 201.995 300.78 331.897 375.72 403.58

k
3 1.403 1.190 1.037 0.781 0.566
m
1 11.862 8.825 9.182 6.605 4.995
 2 0.98 0.93 0.95 0.96 0.97
R
4596 A. Verma et al. / Journal of Environmental Chemical Engineering 4 (2016) 4587–4599

3.6.4. Radke-Prausnitz isotherm 450

This model equation is expressed as follows: 400
qe ¼ q KC ð 23 Þ 350
o ea
300 Langmuir
1 þ qoCe

(mg/g)
250 Freundlich
150
Radke-Prausnitz
where qo is Radke-Prausnitz maximum biosorption capacities (mg/ g), K is 200
Redlich-Peterson
Radke-Prausnitz equilibrium constant and a is Radke-Prausnitz model

e
Toth
exponent. At low concentration, Radke- Prausnitz isotherm reduces to a linear

q
100 Fritz
isotherm and at high concentration it changes to Freundlich isotherm [61]. 50 Experimental
0
0 20 40 60 80 100 120
3.6.5. Toth isotherm Ce (mg/L)
This model is the modified form of Langmuir isotherm which is applicable
+2
to heterogenous biosorption [57]. This isotherm follows Henry’s law at low Fig. 7. Comparison of different isotherm models for biosorption of Pb ions on S.
+2 filipendula.
Pb ions concentration. The Toth isotherm equation is expressed as follows:

1 ð24Þ
qe ¼ qe Ce where a1 and a2 are Fritz parameters, b1 and b2 are Fritz equation exponents.
n 1=n Fritz isotherm has higher degree of flexibility to fit the experimental data as it
a þ Ce 1 1 contains more parameters than any other equation isotherm. Therefore, Fritz
where a (mg/L) is Toth isotherm constant and n 1 is dimensionless constant isotherm described the high level of accuracy and able to fit experimental data
generally n1 <1. over a wide range of concentration. Fritz isotherm is a hybrid of Langmuir
and Freundlich isotherms. It contains the heterogeneity factor (b1 and b2) that
3.6.6. Fritz isotherm report for the biosorbent heterogeneity and show a high level of irreversibility
This model equation is expressed as follows [57]: which characterizes diffusion in the micro-pores [58,59].
b
aC
1 e
1
The value of parameters for each isotherm model with their correlation
qe ¼ b2 ð25Þ 2
coefficient (R ) and normalized standard deviation (Dq %) are shown in Table
1 þ a2Ce
7. Fig. 7 shows the comparison of different isotherm models with
experimental results. The shape of isotherm models can be used to find out
2
favorable biosorption system. For Fritz model, the value of R is greater than
0.99 and Dq% is very small for all the temperatures. This shows that Fritz
+2
model is the best fitted isotherm model for Pb ions biosorption on S.
Table 7
+2
Isotherm model constants for Pb ions biosorption onto S. filipendula at different temperatures.
filipendula.
Isotherm model Parameters Temperature ( C)

20 25 30 35
Langmuir q 455.68 427.635 376.907 367.942 3.7. Thermodynamic study
o
b 0.021 0.0412 0.178 1.024
2 0.983 0.986 0.979 0.923
R The nature of biosorption process and feasibility, are assessed by
Dq% 4.466 3.794 2.209 5.89 thermodynamic study. The equilibrium constant changes with temperature on
Freundlich kf 43.023 75.308 152.69 215.342
the basis of which Gibbs free energy change ( DG ), entropy change (DS )
+2
n 2.339 3.033 5.245 7.720 and enthalpy change (DH ) are estimated. The biosorption of Pb ions is a
R2 0.957 0.929 0.929 0.96 reversible process, which represents a heterogenous equilibrium.
Dq% 7.5 8.542 5.574 5.396
Radke- Prausnitz q 0.009 0.013 0.247 3.139
+2 (26)
Pb (solution) + biosorbent $ Pb biosorbent
K 912.914 1051.8 318.721 263.832
a 1.133 1.179 0.963 0.918
2 0.984 0.994 0.996 0.988
R
Dq% 3.91 2.202 2.334 2.168
Redlich- Peterson K1 8.589 13.645 78.726 828.258

0.009 0.013 0.247 3.139

0
K2
b 1.138 1.179 0.963 0.918
295 300 305 310
2 0.984 0.994 0.996 0.988
-1 290
R
-2
Dq% 3.91 2.177 2.334 2.168
°(kJ/mol)

Toth 385.889 368.906 384.317 473.129

-3
qe
-5 y = -0.443x + 128.34
a 329.596 385.194 4.176 0.314 -4
G

n1 1.478 1.724 0.901 0.321 -6 R² = 0.9771

2 0.985 0.996 0.996 0.981
R
Dq% 3.58 1.531 2.312 2.89
Fritz a1 69.8132 176.738 2.297 242.445 -7

6 -8
a2 1.1448 10 331.774 0.011 0.2245
b1 0.322 0.145 0.3270 0.100 -9
b2 4.733 2.210 3.145 13.896 Temperature (K)
2
R 0.996 0.999 0.999 0.994
Dq% 2.10 0.442 0.732 1.505 Fig. 8. Plot of DG vs. T for the estimation of thermodynamic parameters for biosorption of Pb +2
ions by S. filipendula.
 A. Verma et al. / Journal of Environmental Chemical Engineering 4 (2016) 4587–4599 4597

Table 8
+2
Comparison of thermodynamic parameters for Pb ions adsorption with different adsorbents.
Adsorbent T ( C) DG0 DH0 DS0 Reference
(kJ/mol) (kJ/mol) (J/mol.K)
Solanum melongena 30, 40, 50 8.74 to 7.98 3.698 0.039 [64]
Peanut shells 20, 30, 40 24.25 to 25.00 16.68 25.16 [4]
Sargassum ilicifolium 20, 25, 30 2.6 to 3.6 0.027 0.102 [65]
Cucumis melo 20, 30, 40 23.22 to 29.97 75.67 337 [66]
Caulerpa 20, 30, 40 17.9 to 19.7 8.28 0.0893 [67]
lentillifera 17.24 to 18.15 11.82
Rice husk ash 25, 40, 50, 75 18.26 [68]
Olive tree pruning waste 25, 40, 60 23.46 to 23.84 19.8 11.34 [69]
Sargassum filipendula 20, 25, 30, 35 1.75 to 8.52 0.128 0.443 This study

Thermodynamic constants were evaluated by the following equations: 3.8. Desorption and reuse efficiency

D G0 = - RT ln Ke
DG0 = D H0 T D S0
where Ke is equilibrium constant, calculated as ratio of equilibrium metal
concentration on the biosorbent surface, Ca and in the solution Ce (Ke =
3 significant loss of their biosorption capacities.
Ca/Ce), R is universal gas constant (8.314 10 kJ/mol K) and T is temperature
0 0
in Kelvin. From Fig. 8 the values of DH (128.34 kJ/mol) and DS (0.443
0
J/mol K) are evaluated from intercept and slope of a plot of DG vs. T
according to Eq. (26). The evaluated thermodynamic parameters are listed in
0
Table 8. The positive value of DH indicates endothermic nature of physical
biosorption [63]. It is evident that the extent of metal ion biosorption
increases with the increase in the temperature of process. The negative value
0 ions is presented. The removal efficiency of different biosorbents for Pb
of DG shows the feasibility and spontaneous nature of biosorption [49,60].
Few reported results in the literature on thermodynamic study for other
+2
adsorbent – Pb ions systems are listed in Table 8. It can be clearly observed
from this table that the temperature for every system favors the extent of
0 on biomass surface depends on the number of active binding sites present
adsorption as DG tends to become more negative. The increase in
biosorption with temperature can be either due to increase in the number of
metal binding sites which are accessible for biosorption on surface of
biosorbent or due to decrease in boundary layer thickness surrounding the
biosorbent, which intern reduces the mass transfer resistance of biosorbate
0
[70]. The positive values of DS indicate the enhancement in random-ness of
biosorbed species at solid and liquid interface with progress of biosorption.
+2
Four consecutive cycles of biosorption and desorption of Pb ions were
(27)
+2
carried out in a batch system to find the reusability of S. filipendula for Pb
(28)
ions biosorption (Fig. 9). After four cycles, the biosorption and desorption of
+2
Pb ions was decreased by 5.7% and 15.68%, respectively. Hence, S.
filipendula has shown the better reusability during four consecutive cycles of
+2
biosorption and desorption for Pb ions. The results indicate that S.
+2
filipendula can be reused in Pb ions biosorption studies without any
3.9. Comparison with other seaweeds
A comparative table (Table 9) on the basis of brief review of different
+2
kinetic models, isotherm models, and uptake capacity of brown algae for Pb
+2
ions varies due to different properties of adsorbents like structural, functional
groups, and surface area. In addition to these properties, the degree of
biosorption can also be affected by reaction parameters like temperature, pH,
and presence of other competing cations. The amount of metal ions that binds
+2
[71]. The value of biosorption capacity for Pb ions in this work is
significantly greater than (ffi285 mg/g) other reported biosorbents. Thus, S.
+2
filipendula can be used as an efficient biosorbent for Pb ions uptake.

4. Conclusions

+2
A batch experimental study for the biosorptive removal of Pb ions on S.
filipendula algae has been presented. The RSM has been used to obtain the
+2
optimum conditions for biosorption of Pb ions from the aqueous solution by
S. filipendula. The optimum parameters for biosorption have been obtained as
+2
pH (4.99), temperature (34.8 C), initial concentration of Pb ions (152
120 Desorption efficiency Adsorption efficiency mg/L), and biosorbent dosage (0.49 g/L) at which 96% removal efficiency has
+2
100 been achieved. The removal efficiency of Pb ions is increased with
increasing biosorbent dosage and reaction temperature while decreased with
%Efficiency

80 +2 +2
rise in initial concentration of Pb ions. The percentage of Pb ions removal
is decreased at both low and high pH. Therefore, further biosorption studies
60 +2
have been performed at pH of 5. The biosorption experimental data of Pb
40 ions removal using S. filipendula have been very well fitted with Fritz
isotherm and Bangham kinetic model. Thermodynamic studies has shown that
+2
20 the reaction for biosorption of Pb ions is spontaneous, feasible and
endothermic in nature. After four consecutive cycles of biosorption-
0 +2
desorption, 77.53% of Pb ions has been recovered. The observations of this
1 2 3 4 study indicates that S. filipendula can be
No. of cycles

Fig. 9. Biosorption-desorption efficiency vs. the number of cycles.

4598 A. Verma et al. / Journal of Environmental Chemical Engineering 4 (2016) 4587–4599

Table 9
+2
Comparison of adsorption isotherm, kinetics, and uptake capacity of brown algae for Pb ions.
Biosorbent pH T +2 Adsorption Isotherms Kinetic model Reference
Initial Pb
( C) ions capacity
concentration (mg/g)
Padina sp. 5 22 662 122.6 Langmuir – [72]
Sargassum 5 25 75–100 38.2 – Pseudo first order, [73]
muticum Pseudo second order
Cytoseira baccata 4.5 35 10–2000 134.68 Langmuir, Freundlich – [74]
Gelidium algae 5 25 100 64 Langmuir, Langmuir-Freundlich Pseudo first order, [75]
Pseudo second order
Chlamydomonas 5 25 100 96.3 Langmuir, Freundlich Pseudo first order, [44]
reinhardtii Pseudo second order
Sargassum 3.7 25 200 195 Langmuir, Freundlich Pseudo first order, [65]
illicifolium Pseudo second order
Nizimuddiniazan 5.5 25 165.5 50.41 Langmuir, Toth, Freundlich, Sips, Khan, Dubinin- Pseudo first order, [61]
ardini Radushkavich, Temkin, Redlich-Peterson, Radke- Pseudo second order
Prausnitz
Sargassum 5 35 150–300 285.65 Langmuir, Fritz, Toth Freundlich, Radke- Pseudo first order, Pseudo second order, This
filipendula Prausnitz, Redlich-Peterson Elovich, Bangham, Modified Freundlich study
Intraparticle diffusion

+2
used effectively as a biosorbent for the removal of Pb ions from industrial
wastewater.
Acknowledgements
The authors are thankful to the Ministry of Human Resource
Development, New Delhi, India for providing financial support (Fellowship to
Ayushi Verma), and Institute Instrumentation Center, Indian Institute of
Technology Roorkee, India for making its analytical instruments available for
the research work.
References
[1] A. Iyer, K. Mody, B. Jha, Biosorption of heavy metals by a marine bacterium, Mar. Pollut.
Bull. 50 (2005) 340–343.
[2] S. Wierzba, Biosorption of lead (II) zinc (II) and nickel (II) from industrial wastewater by
Stenotrophomonas maltophilia and Bacillus subtilis, Pol. J. Chem. Technol. 17 (2015)
79–87.
[3] M. Arbabi, S. Hemati, M. Amiri, Removal of lead ions from industrial wastewater: a
review of removal methods, Int. J. Epidemiol. 2 (2) (2015) 105 – 109.
[4] S. Tasar, F. Kaya, A. Ozer, Biosorption of lead (II) ions from aqueous solution by peanut
shells: equilibrium, thermodynamic and kinetic studies, J. Environ. Chem. Eng. 2 (2)
(2014) 1018–1026.
[5] K. Dermentzis, E. Valsamidou, D. Marmanis, Simultaneous removal of acidity and lead
from acid lead battery wastewater by aluminum and iron electrocoagulation, J. Eng. Sci.
Technol. 5 (2) (2012) 1–5.
[6] A.A. Mengistie, T. Siva Rao, A.V. Prasada Rao, M. Singanan, Removal of lead (II) ions
from aqueous solutions using activated carbon from Militia ferruginea plant leaves, Bull.
Chem. Soc. Ethiop. 22 (3) (2008) 349–360.
[7] M.A.O. Badmus, T.O.K. Audu, B.U. Anyata, Removal of lead ion from industrial
wastewaters by activated carbon prepared from periwinkle shells (Typanotonus fuscatus),
Turk. J. Eng. Env. Sci. 31 (2007) 251–263.
[8] N.C. Brady, R.W. Ray, The Nature and Properties of Soil, fourteenth ed., Prentice-Hall,
1999, 2016.
[9] C.N. Deepa, S. Suresha, Biosorption of lead (II) from aqueous solution and industrial
effluent by using leaves of Araucaria cookii: application of response surface methodology,
J. Environ. Sci. Toxicol. Food Technol. 8 (7) (2014) 67–79.
[10] J. Goel, K. Kadirvelu, C. Rajagopal, V.K. Garg, Removal of lead (II) by adsorption using
treated granular activated carbon: batch and column studies, J. Hazard. Mater. 125 (2005)
211–220.
[11] J.J. Moreno-Barbosa, C. Lo’pez-Velandia, A. Pilar Maldonado, L. Giraldo, J.C. Moreno-
Piraja’n, Removal of lead (II) and zinc (II) ions from aqueous solutions by adsorption
onto activated carbon synthesized from watermelon shell and walnut shell, Adsorption 19
(2013) 675–685.
[12] S. Moussous, A. Selatnia, A. Merati, G.A. Junter, Batch cadmium (II) biosorption by an
industrial residue of macrofungal biomass (Clitopilus scyphoides), Chem. Eng. J. 197
(2012) 261–271.
[13] D. Das, G. Basak, V. Lakshmi, N. Das, Kinetics and equilibrium studies on removal of
zinc (II) by untreated and anionic surfactant treated dead biomass of yeast: batch and
column mode, Biochem. Eng. J. 64 (2012) 30–47.
[14] N.S.M. Tahiruddin, S.Z. Ab Rahman, Adsorption of lead in aqueous solution by a mixture
of activated charcoal and peanut shell, World J. Sci. Technol. 1 (2013) 102–109.
[15] N.H. Yarkandi, Removal of lead (II) from waste water by adsorption, Int. J. Curr.
Microbiol. App. Sci. 3 (2014) 207–228.
[16] N. Dasy, R. Vimla, P. Karthika, Biosorption of heavy metals – an overview, Int. J.
Biotechnol. 7 (2008) 159–169.
[17] W. Huang, Z. Liu, Biosorption of Cd (II)/Pb (II) from aqueous solution by biosurfactant-
producing bacteria: isotherm kinetic characteristic and mechanism studies, Colloids Surf.
B 105 (2013) 113–119.
[18] Y.G. Bermudeza, I.L.R. Ricoa, E. Guibalb, M.C. de Hocesc, M.A. Martin-Larac,
Biosorption of hexavalent chromium from aqueous solution by Sargassum muticum
brown alga: application of statistical design for process optimization, Chem. Eng. J. 183
(2012) 68–76.
[19] P. Lodeiro, R. Herrero, M.E. Sastre de Vicente, The use of protonated Sargassum muticum
as biosorbent for cadmium removal in a fixed-bed column, J. Hazard. Mater. B137 (2006)
244–253.
[20] V.K. Gupta, A. Rastogi, Biosorption of lead (II) from aqueous solutions by non- living
algal biomass Oedogonium sp. and Nostoc sp. – a comparative study, Colloids Surf. B 64
(2) (2008) 170–178.
[21] R. Jalali, H. Ghafourian, Y. Asef, S.J. Davarpanah, S. Sepehr, Removal and recovery of
lead using nonliving biomass of marine algae, J. Hazard. Mater. 92 (2002) 253–262.
[22] J.P. Chen, Decontamination of Heavy Metals: Processes, Mechanisms, and Applications,
CRC Press, 2012.
[23] Y. Wanga, Y. Lia, F.J. Zhao, Biosorption of chromium (VI) from aqueous solutions by
Sargassum thunbergii Kuntze, Biotechnol. Biotec. Equip. 28 (2014) 259 –265.
[24] S.H. Abbas, I.M. Ismail, T.M. Mostafa, S.H. Abbas, Biosorption of heavy metals: a
review, J. Chem. Sci. Tech. 3 (2014) 74–102.
[25] O. Abdia, M. Kazemia, A review study of biosorption of heavy metals and comparison
between different biosorbents, J. Mater. Environ. Sci. 6 (2015) 1386–1399.
[26] C.C.V. Cruz, A.C.A. da Costa, C.A. Henriques, A.S. Luna, Kinetic modeling and
equilibrium studies during cadmium biosorption by dead Sargassum sp. biomass,
Bioresour. Technol. 91 (2004) 249–257.
[27] A.C.A. Costa, A.P.M. Tavares, F.P. Franca, The release of light metals from a brown
seaweed (Sargassum sp.) during zinc biosorption in a continuous system, Electron. J.
Biotechnol. 4 (2001) 1–5.
[28] D.M. Vieira, A.C.A. da Costa, C.A. Henriques, V.L. Cardoso, F.P. de Franca, Biosorption
of lead by the brown seaweed Sargassum filipendula – batch and continuous pilot studies,
Electron. J. Biotechnol. 10 (2007) 368–375.
[29] B. Volesky, N. Kuyucak, Biosorbent for Gold. US Patent no. 4,769,233 (1988).
[30] B. Volesky, S. Schiewer, Biosorption metals, in: M.C. Flickinger, S.W. Drew
(Eds.), Encyclopaedia of Bioprocess Technology: Fermentation, Biocatalysis, and
Bioseparation, John Wiley and Sons, Inc, USA, 1999, pp. 433–453.
[31] E. Fourest, B. Volesky, Alginate properties and heavy metal biosorption by marine algae,
Appl. Biochem. Biotechnol. 67 (1997) 33–44.
[32] D. Jeba Sweetly, K. Sangeetha, B. Suganthi, Biosorption of heavy metal lead from
aqueous solution by non-living biomass of Sargassum myriocystum, Int. J. Appl. Innov.
Eng. Manag. 3 (2014) 39–45.
[33] B. Southichak, K. Nakano, M. Nomura, N. Chiba, O. Nishimura, Marine macroalga
Sargassum horneri as biosorbent for heavy metal removal: roles of calcium in ion
exchange mechanism, Water Sci. Technol. 58 (2008) 697 –704.
[34] A.C.A. da Costa, F.P. de Franca, Cadmium uptake by biosorbent seaweeds: adsorption
isotherms and some process conditions, Separ. Sci. Technol. 31 (1996) 2373–2393.
[35] A. Morshedi, M. Akbarian, Application of response surface methodology: design of
experiments and optimization: a mini review, Ind. J. Fund. Appl. Life Sci. 4 (2014) 2434–
2439.
[36] D.C. Montgomery, Introduction to Statistical Quality Control, fourth edition, Wiley, New
York, 2011.
 A. Verma et al. / Journal of Environmental Chemical Engineering 4 (2016) 4587–4599
[37] M.A. Ahmad, N.S. Afandi, O.S. Bello, Optimization of process variables by response
surface methodology for malachite green dye removal using lime peel activated carbon,
Appl. Water Sci. 284 (2015) 1–11.
[38] S. Chowdhury, P.D. Saha, Scale-up of a dye adsorption process using chemically modified
rice husk: optimization using response surface methodology, Desalin. Water Treat. 37
(2012) 331–336.
[39] N. Chaisongkroh, J. Chungsiriporn, C. Bunyakan, Modeling and optimization of ammonia
treatment by acidic biochar using response surface methodology, Songklanakarin J. Sci.
Technol. 34 (2012) 423–432.
[40] M. Jain, V.K. Garg, K. Kadrivelu, Investigation of Cr (VI) adsorption onto chemically
treated Helianthus annus: optimization using response surface methodology, Bioresour.
Technol. 102 (2011) 600–605.
[41] P. Pavasant, R. Apiratikul, V. Sungkhum, P. Suthiparinyanont, S. Wattanachira, T.F.
+2 +2 +2 +2
Marhaba, Biosorption of Cu , Cd Pb , and Zn using dried marine green macroalga
Caulerpa lentillifera, Bioresour. Technol. 97 (2006) 2321–2329.
[42] S. Kamsonlian, B. Shukla, Optimization of process parameters using Response Surface
Methodology (RSM): removal of Cr (VI) from aqueous solution by wood apple shell
activated carbon (WASAC), Res. J. Chem. Sci. 3 (2013) 31 –37.
[43] B. Yu, Y. Zhang, A. Shukla, S.S. Shukla, K.L. Dorris, The removal of heavy metals from
aqueous solutions by sawdust adsorption- removal of lead and comparison of its
adsorption with copper, J. Hazard. Mater. B 84 (2001) 83 –94.
[44] I. Tuzun, G. Bayramoglu, E. Yalcin, G. Basaran, G. Celik, M.Y. Arica, Equilibrium and
kinetic studies on biosorption of Hg (II), Cd (II) and Pb (II) ions onto microalgae
Chlamydomonas reinhardtii, J. Environ. Manag. 77 (2005) 85–92.
[45] N.T. Abdel-Ghani, M. Hefny, G.A.F.E. Chaghaby, Removal of lead from aqueous solution
using low cost abundantly available adsorbents, Int. J. Environ. Sci. Tech. 4 (2007) 67–73.
[46] S. Sugashini, S. Gopalakrishnan, Studies on the performance of protonated cross linked
chitosan beads (PCCB) for chromium removal, Res. J. Chem. Sci. 2 (2012) 55–59.
[47] M.A. Hashem, Adsorption of lead ions from aqueous solution by okra wastes, Int. J. Phys.
Sci. 2 (2007) 178–184.
[48] S. Lagergren, Zur theorie der sogenannten adsorption gelo ster stoffe. Kungliga Svenska
Vetenskapsakademiens Handlingar, 24 (1898) 1–39.
[49] R. Apiratikul, P. Pavasant, Batch and column studies of biosorption of heavy metals by
Caulerpa lentillifera, Bioresour. Technol. 99 (2008) 2766–2777.
[50] B. Yasemin, T. Zeki, Removal of heavy metals from aqueous solution by sawdust
adsorption, J. Environ. Sci. 19 (2007) 160–166.
[51] M.J.D. Low, Kinetics of chemisorption of gases on solids, Chem. Rev. 60 (1960) 267–
312.
[52] S.H. Chien, W.R. Clayton, Application of Elovich equation to the kinetics of phosphate
release and sorption on soils, Soil Sci. Soc. Am. J. 44 (1980) 265 –268.
[53] Y. Onal, Kinetics of adsorption of dyes from aqueous solution using activated carbon
prepared from waste apricot, J. Hazard. Mater. 137 (2006) 1719–1728.
[54] W. Wang, X. Wang, X. Wang, L. Yang, Z. Wu, S. Xia, J. Zhao, Cr (VI) removal from
aqueous solution with bamboo charcoal chemically modified by iron and cobalt with the
assistance of microwave, J. Environ. Sci. 25 (9) (2013) 1726– 1735.
[55] S. Kuo, E.G. Lotse, Kinetics of phosphate adsorption and desorption by hematite and
gibbsite, Soil Sci. 116 (1973) 400–406.
[56] Y.S. Ho, G. McKay, The kinetics of sorption of divalent metal ions onto sphagnum moss
peat, Water Res. 34 (2000) 735–742.
[57] R.K. Singh, S. Kumar, S. Kumar, A. Kumar, Development of parthenium based activated
carbon and its utilization for adsorptive removal of p-cresol from aqueous solution, J.
Hazard. Mater. 155 (2008) 523–535.
4599
[58] X. Yang, B. Al-Duri, Kinetic modeling of liquid-phase adsorption of reactive dyes on
activated carbon, J.Colloid Interface Sci. 287 (2005) 25 –34.
[59] X. Yang, B. Al-Duri, Application of branched pore diffusion model in the adsorption of
reactive dyes on activated carbon, Chem. Eng. J. 83 (2001) 15–23.
[60] P. Bhatt, R.K. Vyas, P. Pandit, M. Sharma, Adsorption of reactive blue and direct red dyes
on PAC: equilibrium kinetics and thermodynamic studies, Nat. Env. Poll. Tech. 12 (2013)
397–405.
[61] M.M. Montazer-Rahmati, P. Rabbani, A. Abdolali, A.R. Keshtkar, Kinetics and
equilibrium studies on biosorption of cadmium lead, and nickel ions from aqueous
solutions by intact and chemically modified brown algae, J. Hazard. Mater. 185 (2011)
401–407.
[62] M.F. Carvalho, A.F. Duque, I.C. Goncalves, P.M.L. Castro, Adsorption of fluorobenzene
onto granular activated carbon: isotherm and bioavailability studies, Bioresour. Technol.
98 (2007) 3424–3430.
[63] M. Xu, H. Wang, D. Lei, D. Qu, Z. Yujia, W. Yili, Removal of Pb (II) from aqueous
solution by hydrous manganese dioxide: adsorption behavior and mechanism, J. Environ.
Sci. 25 (3) (2013) 479–486.
[64] G. Yuvaraja, N. Krishnaiah, M.V. Subbaiah, A. Krishnaiah, Biosorption of Pb (II) from
aqueous solution by Solanum melongena leaf powder as a low-cost biosorbent prepared
from agricultural waste, Colloids Surf. B. 114 (2014) 75 – 81.
[65] R. Tabaraki, A. Nateghi, S. Ahmady-Asbchin, Biosorption of lead (II) ions on Sargassum
ilicifolium: application of response surface methodology, Int. Biodeter. Biodegr. 93 (2014)
145–152.
[66] S.T. Akar, S. Arslan, T. Alp, D. Arslan, T. Akar, Biosorption potential of the waste
2+
biomaterial obtained from Cucumis melo for the removal of Pb ions from aqueous
media: equilibrium kinetic, thermodynamic and mechanism analysis, Chem. Eng. J. 185–
186 (2012) 82–90.
[67] R. Apiratikul, M. Madacha, P. Pavasant, Kinetic and mass transfer analyses of metal
biosorption by Caulerpa lentillifera, Desalination 278 (2011) 303 –311.
[68] M.G.A. Vieira, A.F. de Almeida Neto, M.G.C. da Silva1, C.N. Carneiro, A.A. Melo Filho,
Adsorption of lead and copper ions from aqueous ef fluents on rice husk ash in a dynamic
system, Braz. J. Chem. Eng. 31 (2014) 519–529.
[69] G. Blazquez, M.A. Martin-Lara, G. Tenorio, M. Calero, Batch biosorption of lead (II)
from aqueous solutions by olive tree pruning waste: equilibrium, kinetics and
thermodynamics study, Chem. Eng. J. 168 (2011) 170–177.
[70] R. Coskun, C. Soykan, M. Sac, Adsorption of copper (II), nickel (II) and cobalt (II) ions
from aqueous solution by methacrylic acid/acrylamide monomer mixture grafted poly
(ethylene terephthalate) fiber, Sep. Purif. Technol. 49 (2006) 107– 114.
[71] M.A. Hashim, K.H. Chu, Biosorption of cadmium by brown green, and red seaweeds,
Chem. Eng. J. 97 (2004) 249–255.
[72] P.X. Sheng, Y.P. Ting, P. Chen, L. Hong, Sorption of lead, copper, cadmium, zinc and
nickel by marine algal biomass: characterization of biosorptive capacity and investigation
of mechanisms, J. Colloid Interface Sci. 275 (2004) 131 –141.
[73] O.M.M. Freitas, R.J.E. Martins, C.M. Delerue-Matos, R.A.R. Boaventura, Removal of Cd
(II), Zn (II) and Pb (II) from aqueous solutions by brown marine macro algae: kinetic
modelling, J. Hazard. Mater. 153 (2008) 493–501.
[74] P. Lodeiro, J.L. Barriada, R. Herrero, M.E.S. de Vicente, The marine macroalga Cystoseira
baccata as biosorbent for cadmium (II) and lead (II) removal: kinetic and equilibrium
studies, Environ. Pollut. 142 (2006) 264–273.
[75] V.J.P. Vilar, C.M.S. Botelho, R.A.R. Boaventura, Influence of pH, ionic strength and
temperature on lead biosorption by Gelidium and agar extraction algal waste, Process
Biochem. 40 (2005) 3267–3275.