International Journal of Biological Macromolecules 75 (2015) 230238

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International Journal of Biological Macromolecules

journal homepage: www.elsevier.com/locate/ijbiomac

Chitosan/sporopollenin microcapsules: Preparation, characterisation

and application in heavy metal removal
I dris Sargn a, , Gulsin Arslan b
a
b

Selcuk University, Faculty of Science, Department of Chemistry, 42075 Konya, Turkey

Selcuk University, Faculty of Science, Department of Biochemistry, 42075 Konya, Turkey

a r t i c l e

i n f o

Article history:
Received 22 November 2014
Received in revised form 10 January 2015
Accepted 27 January 2015
Available online 3 February 2015
Keywords:
Chitosan
Sporopollenin
Heavy metal

a b s t r a c t
Use of natural polymers as biosorbents for heavy metal removal is advantageous. This paper reports a
study aiming to design a novel biosorbent from two biomacromolecules; chitosan, a versatile derivative
of chitin, and sporopollenin, a biopolymer with excellent mechanical properties and great resistance to
chemical and biological attack. Chitosan/sporopollenin microcapsules were prepared via cross-linking
and characterised by employing scanning electron microscopy, Fourier transform infrared spectroscopy
and thermogravimetric analysis. Sorption performance of the microcapsules and the plain chitosan beads
were tested for Cu(II), Cd(II), Cr(III), Ni(II) and Zn(II) ions at different metal ion concentration, pH, amount
of sorbent, temperature and sorption time. The adsorption pattern followed Langmuir isotherm model
and the sorption capacity of the chitosan/sporopollenin microcapsules was found to be Cu(II): 1.34,
Cd(II): 0.77, Cr(III): 0.99, Ni(II): 0.58 and Zn(II): 0.71 mmol g1 . Plain chitosan beads showed higher
afnity for the ions; Cu(II): 1.46, Cr(III): 1.16 and Ni(II): 0.81 mmol g1 but lower for Cd(II): 0.15 and
Zn(II): 0.25 mmol g1 . Sporopollenin enhanced Cd(II) and Zn(II) ions sorption capacity of the chitosan
microcapsules. Chitosan/sporopollenin microcapsules can be used in Cd(II) and Zn(II) metal removal.
2015 Elsevier B.V. All rights reserved.

1. Introduction
Water bodies are contaminated with heavy metal ions through
discharge of waste from many industries such as metal plating,
mining, textile and electric/electronic devices manufacturing [1,2].
The waste efuents from these industrial operations, untreated or
even treated, can have signicant amounts of heavy metal ions.
Heavy metal ions in aquatic systems and ground water pose risks
to the living organisms by accumulating in food chain due to their
mobility, stability and non-biodegradability [3]. When their detrimental effects and toxicity are considered, it is critical to remove
heavy metal ions to save diminishing water resources.
There have been increasing interest and efforts to improve conventional techniques to treat the metal contaminated efuents
efciently. Among the conventional physicochemical methods,
adsorption has been extensively employed because of its ease of
use, effectiveness and feasibility [1,4].
Selection of sorbent is a key parameter when sorbents for
heavy metal removal are designed. In addition to physicochemical

Corresponding author: Tel.: +90 332 223 3852; fax: +90 332 241 2499.
E-mail address: idrissargin@hotmail.com (I . Sargn).
http://dx.doi.org/10.1016/j.ijbiomac.2015.01.039
0141-8130/ 2015 Elsevier B.V. All rights reserved.

characteristics of a sorbent such as its selectivity towards certain

species and sorption capacity, its cost and production procedures
should be assessed. Many materials with natural or articial origin such as activated carbon, resins, y ash, oxides, silicates, clays,
zeolites, pine bark and cotton waste have been used as adsorbents
and reported in the literature [5,6]. These studies on sorbents have
demonstrated the need for more efcient, inexpensive and renewable adsorbents. Bio-based sorbents can full these needs; biomaterials are abundant in nature, and also many functional groups
for metal interaction are present on them or they can be easily
functionalised.
Chitin, a carbohydrate with nitrogen content, is the second most
abundant biopolymer in the biosphere. Chitosan, a derivative of
chitin produced via deacetylation of chitin in high alkaline conditions, is a biocompatible and biodegradable [7,8] polymer with high
afnity for metal ions [8,9]. The alkaline hydrolysis of chitin exposes
free amino groups (NH2 ) and gives the polymer unique cationic
nature [10]. The pendant amino groups of chitosan are primary
cause of its higher metal ion sorption capacity and its solubility in
aqueous solutions when compared to chitin. Amino and hydroxyl
groups (especially at the C-3 position) on chitosan can serve as
electrostatic interaction and complexation sites for metal cations
[11,12]. This makes chitosan an appropriate sorbent in heavy metal

I . Sargn, G. Arslan / International Journal of Biological Macromolecules 75 (2015) 230238

uptake [13]. Many workers have opted for chitosan composites as

sorbent and prepared chitosan composites from natural products
[14,15]. However, preparation of a chitosan-based biosorbent with
sporopollenin has not been reported in the literature.
Sporopollenin is a natural biomacromolecule present in the
outer wall (also called exine) of spores and pollens. This polymeric material is highly resistant to chemical and biological
attack and can retain its morphology in geological strata over
millions of years [16,17]. Many analytical techniques have been
performed to reveal its chemical nature; however, information
available on its chemical structure is still limited and needs clarifying. Nevertheless, some studies indicated that sporopollenin is
mainly an aliphatic polymer with phenolic and aromatic groups
or conjugated side chains [18]; it is considered as a macromolecule composed mainly of carotenoid and carotenoid esters
[19].
Sporopollenin particles extracted from Lycopodium clavatum
(common club moss) has excellent mechanical strength and
are reasonably monodisperse [20]. Recently, Fraser et al. (2014)
reported that sporopollenin from L. clavatum is also resistant
to heat and its chemistry does not alter until a threshold of
250300 C [21]. Many researchers have appreciated the unique
nature of the sporopollenin and have conducted works with
raw or functionalised form of it including metal removal studies
[2225].
Once dissolved in acidic solutions, chitosan can be transformed
into insoluble gel form via cross-linking; giving the polymer
structural stability in acidic media. Cross-linking also enables incorporation of ne particles into the polymeric matrice. Cross-linking
forms three dimensional sites within the networks; enhancing the
metal uptake [26]. Preparation of chitosan composite sorbents from
different sources has been reported earlier. Glutaraldehyde, which
forms Schiff bases with amines, is one of the cross-linking agents
used in synthesis and modication of these chitosan-based adsorbents [27].
In this paper, we describe the preparation of a novel biobased adsorbent combining physicochemical properties of both
chitosan and sporopollenin. The synthesised microcapsules were
characterised by employing scanning electron microscopy (SEM),
Fourier transform infrared spectroscopy (FT-IR) and thermogravimetric analysis (TGA). We attempted to provide insights into
how heavy metal ions; Cu(II), Cd(II), Cr(III), Ni(II) and Zn(II),
interact with chitosan/sporopollenin microcapsules and the crosslinked chitosan beads without sporopollenin. Also, we tried to
compare the metal ion uptake capacities of the sorbents. The
microcapsules exhibited higher efciency over the chitosan beads.
Sporopollenin grains entrapped in the chitosan polymeric matrice
signicantly improved the metal ion capture capacity of the
microcapsules. The chitosan/sporopollenin microcapsules can be
used in treatment of the waters contaminated with heavy metal
cations.

2. Experimental
2.1. Materials
Medium molecular weight chitosan was obtained from
SigmaAldrich. Sporopollenin from L. clavatum with 20 m particle size was purchased from Fluka Chemicals. Metal salts
(Cu(NO3 )2 3H2 O, Cr(NO3 )3 9H2 O, Ni(NO3 )2 6H2 O, Zn(NO3 )2 4H2 O)
were purchased from Merck, Cd(NO3 )2 4H2 O was obtained from
SigmaAldrich. Glutaraldehyde (25% in water, v:v) was obtained
from Merck. Double distilled water puried with Barnstead
(Dubuque, IA) ROpure LP reverse osmosis system was used in the
experiments.

231

2.2. Preparation of chitosan/sporopollenin microcapsules

Preparation of chitosan/sporopollenin microcapsules was carried out as follows: Chitosan solution was prepared by dissolving
3.00 g chitosan in 150 mL of acetic acid solution (2% v/v). The mixture was continuously stirred for 20 h. Subsequently, 1.500 g of
sporopollenin particles was added into the chitosan solution and
then the mixture was stirred for 3 h until homogeneity. The chitosan/sporopollenin mixture was transferred into a burette. This
mixture was dropped into the coagulation solution (a mixture of
200 mL of water, 300 mL of methanol and 60.0 g NaOH [28]). Resulting microcapsules were incubated in the coagulation solution for
24 h to achieve a complete gelation, giving a yellow-brownish
colour to the medium. Then, the microcapsules were recovered
and rinsed thoroughly with distilled water until the ltrate was
of neutral pH and free of coloured decomposition products of the
sporopollenin grains. Wet microcapsules (otherwise they could not
retain their spherical shape when dried) were recovered by ltration and transferred into cross-linking reaction solution (0.9 mL of
glutaraldehyde solution in 90 mL of methanol). The cross-linking
solution was reuxed at 70 C for 6 h. Finally, cross-linked microcapsules were recovered and washed thoroughly rst with ethanol
and then with water to remove any unreacted glutaraldehyde
molecules. The cross-linking treatment and the following washing
steps were performed in a fume hood to arrest any glutaraldehyde
vapour. The microcapsules were allowed to dry at room temperature. Plain chitosan beads were synthesised following the same
method but without adding sporopollenin grains to the chitosan
solution.

2.3. Microcapsule characterisation and analytical methods

The surface morphology of chitosan/sporopollenin microcapsules were investigated with Scanning electron microscope (EVO
LS 10 ZEISS). FT-IR spectra of chitosan/sporopollenin microcapsules
were obtained with a Perkin Elmer 100 FT-IR Spectrometer 2.5. Thermogravimetric analysis of chitosan/sporopollenin
microcapsules were done with a Setaram Thermogravimetric Analyzer/Setsys (EXSTAR S11 7300). Metal ion concentration in the
solutions was determined using a ame atomic absorption spectrophotometer (Contr AA 300, Analytik jena).

2.4. Metal sorption experiments

Metal sorption studies were done as follows: 0.1500 g of the
sorbent (chitosan/sporopollenin microcapsules or plain chitosan
beads) was placed into 25 mL of metal ion solution and agitated
for 4 h at 200 rpm. Then, the sorbent was ltered through a lter
paper. The effects of amount of sorbent (0.05000.2500 g), contact
time (60480 min.), metal ion solution pH (3.05.8), initial metal
ion concentrations (212 mg/L) and temperature (25, 35 and 45 C)
on sorption behaviour of the microcapsules and the chitosan beads
were studied. The amount of metal ions adsorbed by the sorbent
was determined from the difference of metal concentrations in the
initial and nal solutions employing following equation below:
qe =

(Ci Ce )V
W

(1)

where qe is the metal sorption capacity of the microcapsules or

chitosan beads (mmol g1 ), Ci and Ce are the initial and equilibrium
liquid-phase concentrations of metal ions (mmol L1 ), respectively;
V is the volume of metal solution (L), and W is the mass of the
sorbent interacted with metal ion solution in grams.

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3. Results and discussion

3.1. Characterisation of chitosan/sporopollenin microcapsules
3.1.1. SEM images
SEM images clearly demonstrated the almost spherical shape of
the microcapsules and the entrapment of the sporopollenin particles in chitosan polymeric matrice (Fig. 1). The images also showed
the effects chemical treatment on the surface morphology of the
sporopollenin grains. As depicted in Fig. 1, prior to introduction into
the chitosan network, the sporopollenin grains had high monodispersity and consistency of size. After coagulation and cross-linking
treatments, the grains could retain their structural integrity to some
extent; but their surface characteristics were partially disrupted;
and as a result, the cavities were compressed or disappeared.
As mentioned in the section 2.2, partial decomposition of
sporopollenin grains in the gelation solution, which was high
alkaline methanol solution, took place. Bubert et al. conducted studies on acidic methanolysis of sporopollenin of Typha angustifolia
[29]. They exposed the sporopollenin grains to HCl in methanol
stepwise; and they analysed the decomposition products using
spectroscopic techniques. They observed substantial weight losses
of the sporopollenin grains at the end of each step. Similarly, we
observed 16.8% mass loss on average upon drying the cross-linked
microcapsules with comparison to the chitosan beads without
sporopollenin. We can conclude that the higher mass losses
observed in preparation of the chitosan/sporopollenin microcapsules can be attributable to the decomposition of the sporopollenin
grains; indicating the act of methanolic alkali solution on sporopollenin grains incorporated in the chitosan microcapsules during the
gelation treatment. However, this phenomenon needs clarifying;
a detailed analysis of the decomposition products released from
the sporopollenin grains during the incubation in the basic media
should be done.
3.1.2. FT-IR spectra analysis
The analysis of the FT-IR spectra of sporopollenin (Fig. 2a),
methanol-NaOH treated sporopollenin (Fig. 2b), chitosan (Fig. 2c),
chitosan/sporopollenin microcapsules (Fig. 2d) and metal ion
loaded microcapsules (Fig. 3) could provide insights into the nature
of the metal ion-microcapsule interactions. As seen from Fig. 2,
after the basic methanolysis of the sporopollenin grains, the OHstretching vibrations at 3378 cm1 did not shift, but the 1709 cm1
band that can be assigned to carboxylic/ketone stretching shifted to
1706 cm1 with lesser intensity, and the sharp peak at 1561 cm1
attributable to the presence of aromatic C C group appeared.
The CN stretching vibration band (1187 cm1 ) was observed at
1194 cm1 . The band at1606 cm1 , assigned to aromatic C C ring
stretching showed weak absorbance at 1603 cm1 as a shoulder. The band at 1260 cm1 representing aromatic ether groups
appeared at 1258 cm1 with strong absorbance [30]. In the FT-IR
spectrum of chitosan, the absorption band at 1589 cm1 , which
is corresponded to the NH2 groups stretching, disappeared after
the cross-linking with glutaraldehyde, and the band appearing at
1640 cm1 can be corresponded to the imine stretching [31]. The
absorption bands, observed at 1656, 1640, 1575 and 1549 cm1
in the spectrum of chitosan/sporopollenin microcapsules were
shifted after forming complexes with metal ions. Additionally, the
alterations in the intensity of CH2 scissoring bands at 1418 cm1
could be attributed to the contribution of CH2 OH side chains in
metal interaction (Fig. 3) [32]. Here, the characteristic broader band
at 3293 cm1 (assigned to stretching vibration of NH and axial
vibration of OH groups present in chitosan) did not shift after crosslinking. But, the band at 2873 cm1 (assigned to intermolecular
hydrogen bonds of chitosan and the axial CH stretching [33])
was shifted and two peaks, at 2919 and 2849 cm1 (symmetric

and asymmetric modes of CH2 group vibration) appeared in spectrum of cross-linked chitosan/sporopollenin microcapsules. These
two peaks were also observed in the presence of metal ions but
with some alterations. These observations demonstrated that the
interaction of metal ions with the microcapsules occurred mainly
via amino, hydroxyl and phenolic groups. Earlier workers studied
interactions of metal ions with raw and modied sporopollenin.
These workers reported that sporopollenin itself had an afnity for
the metal ions due to the functional hydroxyl, carbonyl/carboxyl
and ether moieties on it. Based on ndings reported [34,35] and
the analysis of FT-IR spectra of pristine and treated sporopollenin
(Fig. 2) in this study, it can be commented that functional groups
on sporopollenin particles could also contribute to the sorption of
the metal ions.
3.1.3. Thermogravimetric analysis
The thermal stability of the microcapsules and the beads was
evaluated by TGA (Fig. 4). In the thermogram of the microcapsules,
three decomposition steps were observed. The rst decomposition
step could be resulted from the evaporation of water molecules
[36]; the others can be ascribed to the degradation of the chitosan polymer and the sporopollenin grains within the matrice.
The microcapsules exhibited two maximum decomposition temperatures (DTGmax ) (272.4 and 278.8 C); whereas the chitosan
beads one at lower temperature 269.3 C. In a recent paper by
Fraser et al. (2014) [21], it has been reported that the sporopollenin grains are heat-resistant and the grains start to decompose
at around 300 C. Therefore, the higher DTGmax (278.8 C) could be
corresponded to the degradation of sporopollenin grains. It appears
that sporopollenin grains contributed to the thermal stability of the
microcapsules.
3.2. Effect of the adsorbent dosage on metal uptake
The effect of the amount of chitosan/sporopollenin microcapsules and the chitosan beads on metal sorption was investigated
for each metal ion (Fig. 5). As the sorbent dose was increased, so
did the amount of metal ions sorbed by the microcapsules to a certain extent. Sorption saturation point, where increase in sorbent
dosage did not contribute much to the metal sorption, was different for all the metal ions studied. As seen, such saturation point was
reached at about 0.1500 g of microcapsules or the beads.
3.3. Effect of contact time
Contact time determining studies were conducted for each
metal ion for 6 h (Fig. 6). Initial adsorption rate of Cu(II) ions onto
the microcapsules was relatively higher than the rest; demonstrating rapid uptake process in rst 120 min. Sorption equilibrium for
Cr(III), Zn(II), Cd(II) and Ni ions was attained nearly at 240 min.
3.4. Effect of solution pH on metal sorption
Changes in pH of the metal solution can affect both metal ion
speciation in the solution and the nature of the sorbent especially
through protonation/deprotonation of the functional moieties.
Lower sorption percentage observed in more acidic conditions
(Fig. 7) may be explained by the competition between hydrogen
ions and cationic species for the same binding sites. Presence of
excessive hydrogen ions could lead to protonation of the amino
and hydroxyl groups of chitosan, lowering electron-donating ability of N and O atoms. Additionally, metal binding ability of hydroxyl,
carbonyl and carboxyl groups on sporopollenin [35] could be weakened at lower pH values.
The enhancement observed in sorption capacity of chitosan/sporopollenin microcapsules at higher pHs may be attributed

I . Sargn, G. Arslan / International Journal of Biological Macromolecules 75 (2015) 230238

233

Fig. 1. SEM images of the sporopollenin grains (ad) (magnication: a: 1000, b: 3000, c: 5000 and d: 10000) and chitosan/sporopollenin microcapsules (eh):
(magnication: e: 80, f: 250, g: 1000 and h: 5000).

G = RT lnKC

(2)

G = H T S

(3)

changes (H ) conrming the endothermic nature of the sorption of metal ions onto the microcapsules, the negative values
of G indicated that the sorption process was spontaneous and
thermodynamically feasible at studied temperatures. Additionally,
regarding the high enthalpy changes, particularly in case of Cu(II)
and Cd(II) ions, it appeared that metal sorption primarily occurred
on the surface of the microcapsules rather than within the pores
[39]. Sorption of the metal ions onto the cross-linked chitosan beads
was endothermic. On the other hand, after the incorporation of
sporopollenin grains into the chitosan microcapsules, Cu(II) and
Cd(II) sorption occurred exothermically. The sorption of Cd(II) and
Zn(II) onto the beads were nonspontaneous, but onto the microcapsules the sorption was opposite in nature. Also, considering the
increase in negative values of G with increasing temperature for
the ions other than Ni(II) ions, it can be suggested that metal ion
sorption on the microcapsules was more efcient at higher temperatures. The standard entropy changes were found to be positive,
indicating the increase in the entropy during the adsorption of the
ions onto the chitosan/sporopollenin microcapsules. Similar trend
was observed for the Cu(II), Cd(II) and Cr(III) ions onto the chitosan beads with exception Ni(II) and Zn(II) ions. The entropy of the
equilibrium system decreased upon sorption of these ions onto the
cross-linked chitosan beads. This complex thermodynamic nature
of the different ions onto the same sorbent has been dealt with in
a recent paper by Liu and Lee [40]. The authors performed metaanalysis to critically assess these phenomena and concluded that
the thermodynamic assessment of any metal or dye-sorbent system
dees simple explanations and needs clarifying by more elaborate
experimental study.

(4)

3.7. Adsorption isotherms

to the characteristic of chelation mechanism [37] and the weakened

competition of hydrogen ions for the sorption sites.
3.5. Effect of initial metal ion concentration
The amount of metal ions adsorbed onto the microcapsules
increased in more concentrated metal ion solutions (from 2 to
12 mg L1 ) at initial pH the metal solutions (Cd(II): 5.69; Cu(II):
5.40; Cr(III): 4.02, Ni(II): 5.80; Zn(II): 5.62.); Cu(II):0.141.16,
Cd(II): 0.070.66, Cr(III): 0.380.90, Ni(II): 0.260.50, Zn(II):
0.160.65 mmol g1 . Similar behaviour was observed in the
removal of the ions with chitosan beads; Cu(II):0.040.89,
Cd(II): 0.040.13, Cr(III): 0.330.94, Ni(II): 0.080.30, Zn(II):
0.040.25 mmol g1 . This could be explained with the increasing
concentration gradient of metal ions, acting as a driving force for
the mass transfer of the metal ions to the solid phase [37].
3.6. Thermodynamic analysis
The linear form of the vant Hoff equation was used to derive
thermodynamics parameters governing sorption behaviour of the
metal ions studied onto the microcapsules and the chitosan beads.
Changes in standard free energy (G ), enthalpy (H ), and
entropy (S ), obtained from the linear vant Hoff plot of log KC
versus 1/T, were analysed and discussed.

logKC =

 S   H 
2.303R

2.303RT

where KC is the thermodynamic equilibrium constant i.e., the

ratio of the equilibrium concentration of metal ions on the adsorbent to that in the solution and R is universal gas constant,
8.314 J mol1 K1 and T is the temperature (K). The value of
standard entropy change, S and the standard enthalpy, H are
calculated from the slope (H /2.303R) and intercept (S /2.303R)
of vant Hoff plot, log KC versus 1/T. Operating the equation (3),
Gibbs free energy values were obtained for each temperature [38].
Thermodynamic parameters for the adsorption of Cu(II), Cd(II),
Cr(III), Ni(II) and Zn(II) on chitosan/sporopollenin microcapsules
are presented in Table 1. While the positive value of enthalpy

To make quantitative evaluation of the sorption behaviour of the

metal ions, adsorption isotherm model analysis was done. Although
binding of metal ions to biosorbents often ts the Langmuir [41] and
Freundlich models [42], two other models, DubininRadushkevich
(DR) [43] and Scatchard plot analysis [44], were used to describe
the sorption equilibrium as well.
i. The Freundlich model:
log qe = logKF +

1
n

log Ce

(5)

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234

Fig. 2. FT-IR spectra of sporopollenin (a), methanol-NaOH treated sporopollenin (b), chitosan (c) and chitosan/sporopollenin microcapsules (c).

Table 1
Thermodynamic parameters for the adsorption of Cu(II), Cd(II), Cr(III), Ni(II) and Zn(II) on sporopollenin/chitosan microcapsules and chitosan beads.
Metals

Sorbents

H (J mol1 )

S (J K1 mol1 )

G (J mol1 )
T = 298.15 (K)

T = 308.15 (K)

T = 318.15 (K)

Cu(II)

Microcapsules
Beads

3626.650
2364.790

14.112
15.835

7834.190
2356.560

7975.310
2514.910

8116.430
2673.270

Cd(II)

Microcapsules
Beads

1748.600
6933.527

3.676
7.927

2844.730
4569.999

2881.500
4490.725

2918.260
4411.452

Cr(III)

Microcapsules
Beads

2115.865
275.924

10.397
1.762

984.125
249.304

1088.100
266.921

1192.070
284.573

Ni(II)

Microcapsules
Beads

5323.172
385.834

16.027
8.578

544.734
2943.469

368.464
3029.252

224.195
3115.036

Zn(II)

Microcapsules
Beads

5736.771
2814.771

19.512
2.068

80.706
3431.343

275.826
3452.023

470.945
3472.703

I . Sargn, G. Arslan / International Journal of Biological Macromolecules 75 (2015) 230238

235

Fig. 3. FT-IR spectra of chitosan/sporopollenin microcapsules loaded with copper(II) (a), zinc(II) (b), cadmium(II) (c), chromium(III) (d), nickel(II) (e).

with qe , amount of solute adsorbed in mmol g1 , Ce , the equilibrium concentration of the adsorbate in mM L1 and KF
(mmol g1 ) and n Freundlich constants denoting adsorption
capacity and intensity of adsorption, respectively.
ii. The Langmuir model:
Ce
1
Ce
= 0 + 0
qe
Q
Q b

(6)

with qe , amount of solute adsorbed in mmol g1 , Ce , the equilibrium concentration of the adsorbate in mmol L1 , Q0 (in
mmol g1 ) and b (in L mmol1 ) Langmuir constants related to
adsorption capacity and energy of adsorption.
iii. The DR model:
ln qe = lnXm K2

(7)

where (Polanyi Potential) is [RT ln(1 + (1/Ce ))], qe is the amount

of solute adsorbed per unit weight of adsorbent (mmol g1 ) and
Xm is the adsorption capacity (mmol g1 ), K is a constant related
to the adsorption energy in mol2 kJ2 . The values of Xm and K
were calculated from the intercept and slope of the ln qe versus
2 plots. By using the K values in the equation below, the mean
free energy of adsorption (E) was obtained:
E = (2K)0.5

(8)

iv. The Scatchard plot analysis:

qe
= Ks (Qs qe )
Ce

(9)

where Ce , the equilibrium concentration of the adsorbate in

mmol L1 , qe , equilibrium adsorbate capacity in mmol L1 , Ks

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I . Sargn, G. Arslan / International Journal of Biological Macromolecules 75 (2015) 230238

Fig. 4. TG-DTG curves of chitosan/sporopollenin microcapsules (a) and chitosan beads (b).

Fig. 5. Effect of the adsorbent dosage on metal uptake; chitosan/sporopollenin microcapsules and chitosan beads (at initial pH; metal concentration 10 mg L1 ; volume of
solution 25 mL; temperature 25 C; contact time 4 h).

Fig. 6. Effect of contact time on metal uptake; chitosan/sporopollenin microcapsules and chitosan beads (at initial pH; metal concentration 10 mg L1 ; volume of solution
25 mL; temperature 25 C; adsorbent dosage 0.15 g).

Fig. 7. Effect of pH on metal uptake; chitosan/sporopollenin microcapsules and chitosan beads (metal concentration 10 mg L1 ; volume of solution 25 mL; temperature 25 C;
contact time 4 h; adsorbent dosage 0.15 g).

0.866
0.942
7.906
10.000
0.008
0.005
0.954
0.340
0.571
0.811
0.853
0.296
60.000
460.900
0.940
0.954
0.707
0.246

1.028
1.153

2.113
0.552

Microcapsules
Beads

Microcapsules
Beads

Ni(II)

Zn(II)

2.421
3.205

0.823
0.890

50.480
10.690

0.831
0.861
10.000
5.000
0.005
0.020
0.728
0.444
0.816
0.234
0.649
0.874
108.500
3.449
0.991
0.949
0.583
0.813

1.667
2.723
microcapsules
Beads
Cr(III)

4.274
1.362

0.739
0.910

72.886
2.398

0.965
0.979
7.906
6.455
0.008
0.012
1.084
1.359
0.904
0.948
0.983
1.222
51.190
25.090
0.991
0.988
0.993
1.164

12.050
0.321
Microcapsules
Beads
Cd(II)

3.300
2.198

0.937
0.941

47.288
38.805

0.931
0.954
6.455
6.455
0.012
0.012
1.902
0.187
0.379
0.848
1.367
0.170
40.710
25.880
0.944
0.959
0.773
0.152

14.388
5.888
Microcapsules
Beads
Cu(II)

1.406
2.119

0.878
0.917

85.930
0.827

0.973
0.972
11.180
7.906
0.004
0.008
1.935
1.191
0.799
0.717
1.157
1.621
1156.000
23.340
0.955
0.916
1344.086
60.650
1.344
1.456
0.833
0.990

R
Qs (mmol/g)
Ks (L/mmol)
R
b (L/mmol)
Q0 (mmol/g)
R
n
KF (mmol/g)
Sorbents
Metal ions

2.105
1.706

Xm (mmol/g)

DR

Scatchard

Langmuir

Freundlich
Isotherms

Table 2
The parameters of Freundlich, Langmuir, Scatchard and DR isotherms for sorption of Cu(II), Cd(II), Cr(III), Ni(II) and Zn(II) on chitosan beads and sporopollenin/chitosan microcapsules.

K (mol2 /kJ2 )

E (kJ/mol)

R2

I . Sargn, G. Arslan / International Journal of Biological Macromolecules 75 (2015) 230238

237

(in L mmol1 ) and Qs (in mmol g1 ) are the Scatchard isotherm

constants.
The parameters and correlation coefcients obtained from the
plots of Freundlich (log qe vs. log Ce ), Langmuir (Ce /qe vs. Ce )
and DR (ln qe vs. 2 ) and the Scatchard plot analysis (qe /Ce
vs. qe ) are listed in Table 2. The adsorption isotherm data
analysis showed that the adsorption behaviour of the metal
ions onto chitosan/sporopollenin microcapsules could be better
explained by the Langmuir model. The adsorption degrees of chitosan/sporopollenin microcapsules for the Cd(II), Cr(III), Cu(II),
Ni(II) and Zn(II) ions at room temperature were in the following order; Cu(II): 1.34, Cr(III): 0.99, Cd(II): 0.77, Zn(II): 0.71
and Ni(II): 0.58 mmol g1 . The model analysis also showed that
plain chitosan beads had higher afnity for Cu(II): 1.46, Cr(III):
1.16 and Ni(II): 0.81 mmol g1 but lower for Zn(II): 0.25 and
Cd(II): 0.15 mmol g1 . The Langmuir adsorption capacity of chitosan/sporopollenin microcapsules for Cd(II) and Zn(II) was higher
than the other metal ions studied. The ionic radius order of
these ions is Ni(II) < Cu(II) < Zn(II) < Cd(II) < Cr(III). The microcapsules exhibited lower afnity for the Ni(II) ions, which has the
lowest radius but the highest charge density. On the other hand,
the microcapsules had much higher afnity for Cd(II) and Zn(II) but
slightly less for Cu(II) and Cr(III) ions. Sporopollenin entrapped in
the chitosan matrix enhanced Cd(II) and Zn(II) ions sorption capacity of the chitosan microcapsules. In DR isotherm model analysis,
the value of mean free energy of adsorption, E, can give information about the nature of the interaction between the surface and
the adsorbate. Values higher than 16 kJ mol1 may indicate chemical adsorption while values in a range of 816 kJ mol1 show an
ion-exchange mechanism [28]. Considering the values of mean
free energy of adsorption (E) calculated in the analysis of DR
isotherm model, it appears that the adsorption of metal ions onto
the microcapsules could proceed through chemisorption rather
than physisorption. As seen from Table 2, the deviation from linearity in the Scatchard plot analysis indicated the presence of more
than one type of the sorption sites on the chitosan/sporopollenin
microcapsules [45]. This may be explained by the chemical nature
of the sporopollenin grains already entrapped within the network
of the chitosan polymer. As mentioned, in spite of the efforts to elucidate the chemical composition of sporopollenin grains, there have
been still some uncertainties regarding its exact chemical structure
[18].
4. Conclusions
This present study reports an easy way of preparing chitosan/sporopollenin microcapsules for heavy metal removal.
Chitosan/sporopollenin microcapsules take the advantages of being
natural and its preparation does not require much chemical
treatment. The microcapsules composed of two natural biomacromolecules; chitosan, the derivative of the second most abundant
biopolymer and sporopollenin, a chemically and physically resistant macromolecule of direct biological origin. Sporopollenin grains
entrapped within the polymeric matrice signicantly contributed
to the sorption of Cd(II) and Zn(II) ions onto the microcapsules. Sporopollenin grains enhanced the thermal stability of the
microcapsules. Physical features and surface morphology of the
microcapsules were investigated by SEM studies. The interaction of microcapsules with the metal ions was evaluated in FT-IR
analysis studies. Adsorption isotherm analysis showed that sorption equilibrium could be well dened by Langmuir adsorption
model, indicating homogeneity of the sorption sites on the surface of the microcapsules. Thermodynamic analysis demonstrated
that Cd(II) and Zn(II) ions sorption by chitosan/sporopollenin

I . Sargn, G. Arslan / International Journal of Biological Macromolecules 75 (2015) 230238

238

microcapsules thermodynamically feasible and spontaneous. The

study also revealed the partial decomposition of sporopollenin
in methanol-NaOH solution; which requires further investigating.
In further studies on chitosan/sporopollenin composite microcapsules, molecular weight of chitosan, chitosan/sporopollenin ratio
and incubation time in gelation solution can be manipulated and
this novel bio-based sorbent can be tested in removal of other heavy
metal ions and dyes in aqueous solutions.

[14]
[15]
[16]
[17]
[18]

Conict of interest

[22]
[23]
[24]
[25]

The authors declare no conict of interest.

Acknowledgements
The authors are greatly indebted to the Selcuk University
Research Foundation for providing a nancial support (project
number: BAP-14201082).

[19]
[20]
[21]

[26]
[27]
[28]
[29]
[30]
[31]

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