Egyptian Journal of Aquatic Research (2014) 40, 235–242

H O S T E D BY
National Institute of Oceanography and Fisheries

Egyptian Journal of Aquatic Research

http://ees.elsevier.com/ejar
www.sciencedirect.com

FULL LENGTH ARTICLE

Removal of cadmium from aqueous solution using

marine green algae, Ulva lactuca
Mohamed M. Ghoneim a, Hanaa S. El-Desoky a, Khalid M. El-Moselhy b,*
,
Adel Amer b, Emad H. Abou El-Naga b, Lamiaa I. Mohamedein b,
Ahmed E. Al-Prol b

a
Chemistry Department, Faculty of Science, Tanta University, 31527 Tanta, Egypt
b
National Institute of Oceanography and Fisheries, Suez Branch, 182, Suez, Egypt

Received 26 May 2014; revised 25 August 2014; accepted 25 August 2014

Available online 6 October 2014

KEYWORDS Abstract The present study aimed to evaluate the efficiency of marine algae for removal of metals
Ulva lactuca; from the aqueous solution. The green alga, Ulva lactuca, collected from the intertidal zone of the
Marine algae; Suez Bay, northern part of the Red Sea was used to reduce cadmium levels from the aqueous
Biosorption; solutions. The biosorption mechanisms of Cd2+ ions onto the algal tissues were examined using
Cadmium; various analytical techniques: Fourier-transform infrared spectroscopy (FT-IR) and Scanning elec-
Isotherm models tron microscopy (SEM). Results indicated that at the optimum pH value of 5.5; about 0.1 g of U.
lactuca was enough to remove 99.2% of 10 mg L1 Cd2+ at 30 C in the aqueous solutions. The
equilibrium data were well fitted with the Langmuir and Freundlich isotherms. The monolayer
adsorption capacity was 29.1 mg g1. The calculated RL and ‘n’ values have proved the favorability
of cadmium adsorption onto U. lactuca. The desorption test revealed that HCl was the best for the
elution of metals from the tested alga. In conclusion, the seaweed U. lactuca was the favorable alter-
native of cadmium removal from water.
ª 2014 Hosting by Elsevier B.V. on behalf of National Institute of Oceanography and Fisheries.

Introduction into the environment through wastewater streams are electro-

plating, smelting, paint pigments, batteries, fertilizers, mining
Environmental pollution due to toxic heavy metals is a signifi- and alloy industries (Iqbal and Edyvean, 2005).
cant worldwide problem due to their incremental accumulation Cadmium is one of the toxic heavy metals with a greatest
in the food chain and continued persistence in the ecosystem potential hazard to humans and the environment. It causes
(Aneja et al., 2010). The removal and recovery of toxic heavy kidney damage, bone diseases and cancer. Chronic exposure
metal ions from wastewaters are of great importance from an to elevated levels of cadmium is known to cause renal dysfunc-
environmental viewpoint. The major sources of Cd(II) release tion, bone degeneration and liver damage (Iqbal et al., 2007).
Conventional techniques for removing heavy metals from
* Corresponding author. industrial effluents include chemical precipitation, chemical
E-mail address: [email protected] (K.M. El-Moselhy). reduction, adsorption, ion exchange, evaporation and
http://dx.doi.org/10.1016/j.ejar.2014.08.005
1687-4285 ª 2014 Hosting by Elsevier B.V. on behalf of National Institute of Oceanography and Fisheries.
236 M.M. Ghoneim et al.

membrane processes, while the biosorption process offers Effect of biomass amount
potential advantages such as low operating cost, minimization This part of the experiment was performed to verify the effect
of chemical or biological sludge, high efficiency of heavy metal of biosorbent weight on the sorption process. Different weights
removal from diluted solutions, regeneration of biosorbents, of biosorbents (0.05, 0.1, 0.2 and 0.4 g) were mixed and shaken
possibility of metal recovery and being environmentally with 10 mL solution of 10 mg Cd/L at 30 C, pH 5.5 for
friendly (Ahluwalia and Goyal, 2007). 120 min (Ajaykumar et al., 2008).
Biosorption is an innovative technology using living or
dead biomasses to remove toxic metals from aqueous solu- Initial cadmium concentration
tions. Various biomasses such as bacteria, yeast, fungi and alga
The extent of removal of heavy metals from aqueous solution
for biosorption of metal ions have been widely used (Vieira
depends strongly on the initial metal concentration. In order to
and Volesky, 2000). Among the biological materials, marine
assess, different Cd concentrations of 3, 5, 7, 10, 25, 50, 75 and
alga have high metal binding capacities due to the presence
100 mg/L were examined at constant parameters, pH 5.5 with
of polysaccharides, proteins or lipid in the cell wall structure
0.1 g of biosorbent added into 10 ml solutions at 30 C (Meral
(Davis et al., 2003). The mechanism of biosorption is mainly
Karaca, 2008).
based on physical adsorption (electrostatic attraction–Vander-
waal forces of attraction) and/or chemical adsorption (cova-
lent binding between negative charge of cell surface and Effect of temperature
cationic ions (Vijayaraghavan and Yun, 2008). The physio- Biosorption process was carried out at different values of
chemical phenomena besides being rapid are reversible temperature (20, 25, 30 and 35 C), at constant pH 5.5, 0.1 g
(Darnall et al., 1986). biosorbent weight, volume of 10 ml of 10 mg Cd/L for
The main objective of this study was to evaluate the 120 min (Ajaykumar et al., 2008).
biosorption performance of locally marine macroalga Ulva
lactuca for the removal of cadmium ions from aqueous solu- Metal removal efficiency
tions, as well as to study the effect of pH, biomass amount,
time, initial metal concentration and temperature on the treat-
Biosorption capacity (qe), the amount of metal adsorbed per
ment process. Langmuir and Freundlich isotherm equations
gram of biosorbent, can be calculated at equilibrium in mg/g
were employed to quantify the biosorption equilibrium. In
as follows:
addition to study the efficiency of different elutants to desorp
the cadmium from the algae tissues. qe ¼ ðC0  Ce ÞV=m ð1Þ

where C0 is the initial concentration of metal ions in the solu-

Materials and methods tion (mg/L), Ce is the equilibrium concentration of metal ions
in the solution (mg/L), V is the volume of solution (in L) and m
Materials is the mass of biosorbent applied (in g) (Hashim and Chu,
2004). Metal uptake can also be displayed by the percentage
Preparation of cadmium of metal removal given by (Zhang et al., 1998; Volesky, 1992):
The analytical grade salt Cd(NO3)2 was used to prepare stock Metal removal ð%Þ ¼ 100ðC0  Ce Þ=C0 ð2Þ
solution (1000 mg L1) of Cd2+. The desired concentrations
were prepared by dilution of the stock solution with deionised
water. The initial pH was adjusted with concentrated HCl or Cadmium measurement
NaOH. The initial metal concentration (10 mg L1) was mea-
sured using a flame atomic absorption spectroscopy (Perkin The collected samples from different experiments were filtered
Elmer AAnalyst 100). Samples were diluted before the with filter paper (47 lm) and Cd2+ concentration was mea-
required analysis to set the calibration linear range. sured by an Atomic Absorption Spectrometer (Perkin Elmer
AAnalyst 100). The analyses were carried out at the wave-
Preparation of adsorbent lengths of 228.8 nm.
U. lactuca (green alga) was collected from the Suez Bay shore.
The collected alga was washed with excess tap water and Characterization of biomass
finally with distilled water to remove salt and particulate
materials from the surface, dried at room temperature, then Fourier-transform infrared analysis (FTIR)
ground as powder using an electrical mill and sieved to uni- Dry U. lactuca samples (before and after cadmium biosorp-
form particle sizes (0.210 mm). tion) were examined with a Model Tensor – 27. Bruker FTIR
within the wave number 200–5000 cm1 under ambient condi-
Methods tions. This technique was used to elucidate the chemical char-
acteristics relevant to metallic ion sorption by the algal
Effect of pH biomass (Raize et al., 2004).
During the experiment of pH effect, the parameters of temper-
ature, solution volume, biosorbent amount, initial metal ion Scanning electron microscopy (SEM)
concentration, and shaking time were fixed at 30 C, 10 mL, Dry U. lactuca samples (before and after cadmium biosorption)
10 mg L1, 0.1 g and 120 min, respectively. Effects of pH were were glued and coated with gold. The coated samples were put
tested at pH 2, 3, 4, 5, 5.5, 6 and 8 (Karaca, 2008). into a JEOL, JSM-52500 LV SEM, Japan and different sections
Cadmium removal from aqueous solution using green algae 237

in the samples were examined. This technique was used to exam- is increased in the solution, so metal ions react with OH- ions
ine the algal cell surface (Saravanan et al., 2011). and are precipitate as a metal hydroxide at high pH value
(Farooq et al., 2010).
Isotherm studies At higher pH, the removal was also low compared with the
optimum condition. This can be explained as the binding site
Biosorbent (0.1 g) was added to 10 mL of metal solutions with may not activate in basic conditions (Memon et al., 2008).
different initial cadmium concentrations varying from 3 to Dursun (2006) concluded that, pH of the solution influences
100 mg/L. The solution was controlled at pH 5.5, 30 C and both metal binding sites on the cell surface and the chemistry
for 2 h (Ajaykumar et al., 2008). of metal in solution.

Desorption of metals Effect of biomass amount

It was observed that the amount of Cd2+ ions adsorbed varied
Desorption studies were performed in a way that, 0.1 g of with varying algae amounts (Fig. 2). The results recorded
biosorbent was shaken with 10 mL of 10 mg/L cadmium ion removal percentages of 86.6%, 99.2%, and 98.7% and
solution for 5–30 min. After shaking and filtration steps, bio- 98.1% at weights of 0.05, 0.1, 0.2 and 0.4 g, respectively. It
sorbed metals were tried to be desorbed in separate experi- seems that the highest biosorption uptake was found at the
ments with 1 M HCl, 1 M H2SO4, 1 M HNO3 and distilled biomass weight of 0.1 g. High biosorbent amounts are known
water. Finally, the concentration of the metal ions in the fil- to cause cell agglomeration and a consequent reduction in
trate was determined by AAS. The eluted metal was deter- intercellular distance and produce ‘screen effect’ among a
mined and the elution efficiency by desorption agent can be dense layer of cells, leading to the ‘protection’ of binding sites
defined as follows: from metal ions (Pons and Fuste, 1993). The obtained data
Elution efficiency ð%Þ ¼ 100ðCs Vs Þ=ðqe mÞ ð3Þ were in agreement with those of Esposito et al. (2001) and
El-Sikaily et al. (2011), who reported lower biosorbed metal
where Cs is the concentration of metal ions in the desorbed percentage (q) at high adsorbent concentrations.
solution (mg/L), Vs is the volume of solution in the desorption
(L), m is the mass of biosorbent used in desorption studies (g) Effect of initial Cd2+ concentration
and qe is defined in Eq. (1) (Nessim et al., 2011).
The present data illustrated that, as the initial metal ion con-
centration increases the percentage of Cd2+ ions adsorption
Results and discussion
increases (Fig. 3). Removal percentage starts from 55% for
3 mg/L and increases up to 99.6% at 10 mg/L Cd2+ then
Factors affecting biosorption of Cd2+
decreases (steady state) as the initial heavy metal concentration
increases. The increase in adsorption is a result of an increase
Effect of pH in the driving forces, i.e. concentration gradient. At lower con-
In order to demonstrate the effect of pH on biosorption of centrations, all Cd2+ ions present in solution could interact
Cd(II) ions by algae, pH ranges of 2–8 were used and illus- with the binding sites and thus the percentage adsorption
trated in Fig. 1. Biosorption of heavy metal ions is dependent was increased gradually as Cd2+concentration increases
on the pH of solution as it affects biosorbents surface charge, While, at higher concentrations than 10 mg/L Cd2+, slightly
degree of ionization, and the species of biosorbent (Ahmady- lower adsorption yield is mainly attributed to the saturation
Asbchin et al., 2008). The present results showed that, the of adsorption sites. This is due to an increase in the number
metal removal percentage was increased up to pH 5.5 and then of ions competing for available binding sites in the biomass
decreased. In contrast, when the pH was increased, a partial (Puranik and Paknikar, 1999).
desorption of protons occurs allowing the sorption of Cd(II)
onto the sites left by protons at the surface of biomass and Effect of temperature
the biosorption reached the maximum (91.9%) around pH
5.5. According to this, it may be suggested that there was a Effect of solution temperature (20, 25, 30 and 35 C) on the
clear competition for the biomass sorption sites between Cd(II) biosorption of Cd2+ ions was investigated. Fig. 4 shows that
and proton.The decrease in biosorption at higher pH values when temperature was increased from 20 C to 30 C, the
(pH > 5.5) may be attributed to that the amount of OH- ions uptake of Cd2+ ions by U. lactuca was increased from

100
90 100
80
Cd removal (%)

95
70
Cd removal (%)

60 90
50
85
40
30 80
20
75
10
0 70
0 1 2 3 4 5 6 7 8 9 0 0.05 0.1 0.15 0.2 0.25 0.3 0.35 0.4 0.45
PH Biomass amount (g)

Figure 1 Effect of pH values on cadmium biosorption. Figure 2 Effect of biomass amount on removal of cadmium.
238 M.M. Ghoneim et al.

100 biosorption) (Sheng et al., 2004). Also, the bands at 1107 cm1
(before biosorption) and 1053 cm1 (after biosorption)
90 corresponded to the C–O stretching of alcohol or carboxylic
Cd removal (%)

acid (Ngah and Hanafiah, 2007). The values which appeared

80
in the region between 538 and 1030 are finger prints of the
70
symmetric bond.

60 Scanning electron microscopy (SEM)

50 The morphology of U. lactuca surface was analyzed by scan-

0 10 20 30 40 50 60 70 80 90 100 110
ning electron microscopy before and after cadmium loading
Concentration (mg/l)
(Fig. 6a and b). The cells before exposure were smooth and
Figure 3 Effect of initial cadmium ions concentration on the had certain dimensions, after their exposure to cadmium ions
biosorption. solution, they become destroyed and swollen, and their surface
becomes meanders. This may be due to cadmium ions precip-
itated around the cell surface and linked with their functional
63.14% to 87.3%. The temperature has two major effects on groups. Also, these changes were probably caused when the
the adsorption process. The first is that increasing the temper- samples were exposed to heavy metal solution; the metal ions
ature will increase the rate of adsorbate diffusion across the replaced some of the cations initially present in the cell wall
external boundary layer and in the internal pores of the adsor- matrix and created stronger crosslinking. Due to ion-exchange
bate particles because liquid viscosity decreases as the temper- mechanism, the heavy metal ions occupied the available free
ature constant increases. Second is that, the temperature binding sites (Saravanan et al., 2011).
affects the equilibrium capacity of the adsorbate depending
on whether the process is exothermic or endothermic (Al- Biosorption isotherm models
Qodah, 2006).
The sorption isotherms are the mathematical model which
FTIR
provides an explanation about the behavior of adsorbate species
between solid and liquid phases. Langmuir and Freundlich iso-
FTIR analysis was carried out in order to identify the different therm models (Langmuir, 1918 and Freundlich, 1906) were stud-
functional groups present in U. lactuca which were responsible ied for the investigation of biosorption of Cd2+ ions by U.
for the adsorption process (Fig. 5). The peaks appearing in the lactuca .The Langmuir isotherm assumes monolayer coverage
FTIR spectrum were assigned to various functional groups of metal ions over a homogeneous sorbent surface (Sheng
according to their respective wave numbers as reported in et al., 2004). The isotherm is presented by the following equation:
the literature. The shift in the band 3409 and 3414 cm1 indi-
cates changes in the hydroxyl and amino group positions dur- qe ¼ qmax bCe =ð1 þ bCe Þ ð4Þ
ing cadmium biosorption (Sheng et al., 2004). The peak where qe (mg/g) is the observed biosorption capacity at equilib-
observed at 2931 cm1 (before and after biosorption) was asso- rium, qmax (mg/g) is the maximum biosorption capacity corre-
ciated with the stretching vibrations of C–H bond of methyl, sponding to the saturation capacity (representing total binding
methylene and methoxy groups (Feng et al., 2008). Intense sites of biomass), Ce (mg/L) is the equilibrium concentration
band at 2285 cm1 (before biosorption) indicates C–H stretch- and b (L/mg) is a coefficient related to the affinity between
ing from CH2 groups (Solomon et al., 2012), that peak disap- the sorbent and sorbate (b is the energy of adsorption). The
peared after biosorption. The peaks at 1656 cm1 (before linear relationship can be obtained by plotting (1/qe) vs. (1/Ce):
biosorption) and 1640 cm1 (after biosorption), corresponded
1=qe ¼ 1=ðbqmax Ce Þ þ 1=qmax ð5Þ
to the C‚C stretching which might be attributed to the pres-
ence of lignin aromatic bond (Florido et al., 2009). The peaks In which b and qmax are determined from slope and inter-
at 1431 cm1 (before biosorption) reveal the presence of C–O cept, respectively. The different biosorbents can be compared
(Fourest and Volesky, 1996). The presence of amide in the by its respective qmax values which are calculated from fitting
structure of alga is confirmed by the peak at 1542 cm1 (after the Langmuir isotherm model to actual experimental data.

100
95
90
Cd removal ( %)

85
80
75
70
65
60
55
50
0 5 10 15 20 25 30 35 40
o
Temp ( C)

Figure 4 Effect of temperature on the biosorption of cadmium.

Cadmium removal from aqueous solution using green algae 239

Figure 5 FTIR spectrum of Ulva lactuca (a) before biosorption and (b) after biosorption of cadmium.

Freundlich isotherm is used for modeling the adsorption on log qe ¼ log Kf þ 1=n log Ce ð7Þ
heterogeneous surfaces. This isotherm can be described as
follows: The plots of non-linearized Langmuir and Freundlich
adsorption isotherms are shown in Figs. 7 and 8. The adsorp-
qe ¼ Kf C1=n
e ð6Þ
tion isotherm constants were determined by using non-linear
where Kf and n are the Freundlich constants related to the regression. The Langmuir and Freundlich adsorption con-
adsorption capacity and intensity of the sorbent, respectively stants evaluated from the isotherms with the correlation
(Freundlich, 1906). The Freundlich model can be easily linear- coefficients are also presented in Table 1. The best-fit equilib-
ized by plotting it in a logarithmic form: rium model was determined based on the linear regression
240 M.M. Ghoneim et al.

Figure 6 SEM micrograph (·5000) of Ulva lactuca cell wall (a) before and (b) after Cd2+ adsorption from aqueous solution.

is consistent with strong monolayer sorption on to specific

5
4.5 sites.
4 Accordingly, the essential characteristics of the Langmuir
3.5 isotherm parameter can be expressed in terms of a separation
3
factor or a dimensionless equilibrium parameter, RL according
1/qe

2.5
2 to the equation of Ahalya et al. (2005) and Kagaya et al. (2006)
1.5 as follows:
1
0.5 RL ¼ 1=ð1 þ bC0 Þ ð8Þ
0
0 0.2 0.4 0.6 0.8 1 1.2 1.4 where b is the Langmuir constant and C0 is the initial concen-
1/Ce tration of Cd2+ ions. The value of the separation parameter
RL provides important information about the nature of
Figure 7 Langmuir isotherm plot for cadmium ions. adsorption. The value of RL indicated the type of Langmuir
isotherm to be irreversible (RL = 0), favorable
(0 < RL < 1), linear (RL = 1) or unfavorable (RL > 1). RL
1 values between 0 and 1 indicate favorable absorption
0.8 (Mckay et al., 1982). From this study, The RL was found to
0.6
be 0.802053 (Table 1).
0.4
The experimental data obeyed also the Freundlich model, as
Log qe

0.2
confirmed by the high determination coefficient (R2 > 0.951)
0
(Table 1). As can be seen from the results, the n values were found
-0.2 -0.2 0 0.2 0.4 0.6 0.8 1 1.2 1.4
to be 1.0002. According to Kadirvelu and Namasivayam (2000),
-0.4
n values between 1 and 10 represent beneficial biosorption. The
-0.6
‘n’ value of Freundlich equation could give an indication on
-0.8
Log Ce the favorability of sorption. Kf can serve as an indicator for the
maximal metal cation uptake capacity of the algal biomass.
Figure 8 Freundlich isotherm plot for cadmium ions.
Desorption of metal ions

Table 1 Langmuir and Freundlich isotherm parameters for With the use of elutants it is necessary to evaluate both effi-
cadmium. ciency of desorption and preservation of biosorption capacity
Model Parameter of the biomass (Chu et al., 1997). The adsorbed metals on
Langmuir qmax b R2 RL
adsorbents cannot be completely reversible as reported by sev-
29.069 0.000545 0.984 0.802053 eral observations on the literature of workers (Farrah and
Freundlich n kf R2 Pickering, 1978; Brummer et al., 1988; Ainsworth et al.,
1.0002 0.2300 0.9517 1994). If desorbent fulfills the assigned criteria, it is possible
to recover metal ions in the form of concentrated solution
and to regenerate the biosorbent that can be used in another
correlation coefficient R2. The fitting of experimental data with biosorption cycle.
the Langmuir model was emphasized by high R2 values. The Desorption of Cd(II) ions by U. lactuca biomass was studied
correlation regression coefficient (R2 = 0.984) shows that the by using 1 M of HCl, H2SO4 and HNO3 as well as distilled
biosorption process is fit Langmuir model. The Langmuir fit water. The results of desorption are shown in Fig. 9, which
Cadmium removal from aqueous solution using green algae 241

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90 1994. Cobalt, cadmium, and lead sorption to hydrous iron oxide:
Recovery of removal ions (%)

80
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70
Ajaykumar, A.V., Al Hashimi, S., Hilal, N., 2008. Investigation of
60
50
kinetics and mechanism involved in the biosorption of heavy metals
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Brummer, G.W., Gerth, J., Tiller, K.G., 1988. Reaction kinetics of
Figure 9 Effect of various agents on desorption of cadmium
the adsorption and desorption of nickel, zinc and cadmium by
from Ulva lactuca biomass. goethite. I. Adsorption and diffusion of metals. J. Soil Sci. 39, 37–
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and H2SO4). The distilled water has a low amount of Cd2+ ions
Biosorption of cadmium by algal biomass: adsorption and desorp-
recovery (<28%). The highest amount of Cd2+ ions recovery tion characteristics. Water Sci. Technol. 35, 115–122.
was 84.1% using of 1 M HCl. While, for the other two elutants Darnall, D.W., Greene, B., Hosea, M., McPherson, R.A., Henzl, M.,
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