Environmental Science and Pollution Research (2019) 26:6336–6347

https://doi.org/10.1007/s11356-018-04108-8

RESEARCH ARTICLE

Characteristics and performance of Cd, Ni, and Pb bio-adsorption using

Callinectes sapidus biomass: real wastewater treatment
Rauf Foroutan 1 & Reza Mohammadi 2 & Sima Farjadfard 3 & Hossein Esmaeili 4 & Maryam Saberi 1 & Soleyman Sahebi 5,6 &
Sina Dobaradaran 7,8,9 & Bahman Ramavandi 7,8

Received: 29 September 2018 / Accepted: 27 December 2018 / Published online: 7 January 2019
# Springer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract
In the current study, the bio-adsorption potential of Callinectes sapidus biomass for control of cadmium, nickel, and lead from the
aqueous stream was assessed. Spectrum analysis of FTIR, AFM, EDAX, mapping, SEM, TEM, and XRF was used to study the
properties of the C. sapidus biomass. The XRF analysis revealed that C. sapidus bio-adsorbent has various effective metal oxides
that can be useful to adsorb pollutants. The best model to describe the equilibrium data was Freundlich isotherm. The Langmuir
bio-adsorption capacity was reported at 31.44 mg g−1, 29.23 mg g−1, and 29.15 mg g−1 for lead, cadmium, and nickel ions,
respectively. Pseudo-first-order and pseudo-second-order kinetic models were studied to test the kinetic behavior of the process.
An intra-particle diffusion model was used to determine the effective mechanisms involved in the bio-adsorption. Based on t1/2, it
can be concluded that the equilibrium speed of the bio-adsorption process is high. The thermodynamic study showed that the
metal bio-adsorption process using C. sapidus biomass is exothermic and spontaneous. The field applicability of the crab bio-
adsorbent for eliminating concurrently several contaminants (metal ions, antibiotics, sulfate, nitrate, and ammonium) from an
actual wastewater was successfully examined.

Keywords Callinectes sapidus . Heavy metals . Kinetic study . Aqueous stream . Antibiotic . Hospital wastewater

Responsible editor: Tito Roberto Cadaval Jr

Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s11356-018-04108-8) contains supplementary
material, which is available to authorized users.

* Soleyman Sahebi 5
Department for Management of Science and Technology
soleyman.sahebi@tdt.edu.vn Development, Ton Duc Thang University, Ho Chi Minh
City, Vietnam
* Bahman Ramavandi
ramavandi_b@yahoo.com; b.ramavandi@bpums.ac.ir 6
Faculty of Environment and Labor Safety, Ton Duc Thang
1
University, Ho Chi Minh City, Vietnam
Young Researchers and Elite Club, Bushehr Branch, Islamic Azad
University, Bushehr, Iran 7
Systems Environmental Health and Energy Research Center, The
2 Persian Gulf Biomedical Sciences Research Institute, Bushehr
Polymer Research Laboratory, Department of Organic and
Biochemistry, Faculty of Chemistry, University of Tabriz, University of Medical Sciences, Bushehr, Iran
Tabriz, Iran
8
3 Department of Environmental Health Engineering, Faculty of Health,
Department of Environmental Engineering, Graduate School of the
Bushehr University of Medical Sciences, Bushehr, Iran
Environment and Energy, Science and Research Branch, Islamic
Azad University, Tehran, Iran 9
The Persian Gulf Marine Biotechnology Research Center, The
4
Department of Chemical Engineering, Bushehr Branch, Islamic Persian Gulf Biomedical Sciences Research Institute, Bushehr
Azad University, Bushehr, Iran University of Medical Sciences, Bushehr, Iran
Environ Sci Pollut Res (2019) 26:6336–6347
Introduction
The presence of heavy metals inside environment and superficial
waters causes serious problems for the environment and public
health (Long et al. 2018). Today, heavy metals have been used in
various industries including mining, electroplating, battery, textile
factories, metalworking processes, oil, paint, electronics, and tim-
ber production (Naeimi et al. 2018). Nickel, lead, and cadmium
metal ions are significantly found inside industrial wastewaters
such as metal coatings, color manufacturing plants, pigments,
tanning, photography, and printing industries (Arim et al.
2018). Heavy metals are considered as one of the hazardous
pollutants because they are toxic with high durability in the en-
vironment and food chains (Li and Zhou 2018; Franus and
Bandura 2014). In addition, these metals are not decomposed
and have a capacity to accumulate in the environment and change
the physical, chemical, and biological quality of the waters
(Barros et al. 2007). The human body can exhibit different reac-
tions to the toxicity of heavy metals. Lead ions can damage the
liver, the kidneys, the nervous system, the reproductive system,
and the brain (Naeimi et al. 2018). According to the World Health
Organization (WHO), the maximum allowable amount of lead
ion in drinking water is 0.07 mg L−1. Nickel is another popular
toxic metal and its toxicity causes headache, vomiting, dizziness,
chest pain, nausea, shortness of breath, dry cough, swelling of the
skin, rapid breathing, cyanosis, and finally body weaknesses
(Long et al. 2018). Based on the WHO and the US
Environmental Protection Agency (US EPA), the permitted nick-
el in drinking water was determined as 0.5 mg L−1 (Petrella et al.
2018). One of the most toxic and harmful heavy metals to human
health is cadmium which, more than its permitted levels
(0.003 mg L−1), can bring renal failure, hypertension, hepatic
injury, damage to the lungs, bone damage, and cancer (Fawzy
et al. 2016). Therefore, control of heavy metals from wastewaters
and waters is an important issue for the environment and public
health. The techniques for heavy metal control from aqueous
streams include chemical (precipitation or oxidation), physical
(adsorption, ion change, solvent extraction, reverse osmosis,
and evaporation), and biological (Foroutan et al. 2017a).
Among these techniques, the physical technique is more likely
to be exploited due to the possibility of pollutant recyclability and
ease of operation. And among physical techniques, the adsorption
process has been used a lot in recent years by researchers because
this process has advantages like high performance and low oper-
ational cost (Teimouri et al. 2017; Gruszecka-Kosowska et al.
2017). Also, this technique is known as an eco-friendly method
because renewable biomass is used to make bio-adsorbents
(Ahmad et al. 2012; Castillo-Araiza et al. 2015). Many bio-
adsorbents have been used to control the heavy metal ions in-
cluding all types of algae (Birungi and Chirwa 2015; Karthikeyan
et al. 2007), barley straw (Pehlivan et al. 2012), chitin and chito-
san (Kamble et al. 2007), agricultural wastes such as dew melon
peel (Ahmadi et al. 2016), activated carbon derived from bagasse
6337
(Mohan and Singh 2002), tea wastes (Amarasinghe and Williams
2007), and olive oil milling operations (Petrella et al. 2018).
In this research, Callinectes sapidus wastes have been used
for bio-adsorption of heavy metals (lead, cadmium, and nick-
el) from aqueous media which is a low-cost and abundant bio-
adsorbent and has not been studied yet. This crab is annually
produced or collected from the sea on a large scale worldwide,
and about 50% of it remains waste (claws, chest, and legs)
when used (Baron et al. 2017). Therefore, any use of this
waste is ecologically and economically admirable.
The main objective of the current work is using C. sapidus
wastes as a low-cost bio-adsorbent to recycle and control toxic
heavy metals of lead, cadmium, and nickel from aqueous
streams and also study the important and effective parameters
on bio-adsorption of metals such as solution initial pH, tem-
perature, contact time, and adsorbent dose. The characteristics
of the fresh and used bio-adsorbent are presented. The field
applicability of the C. sapidus bio-adsorbent was also ex-
plored for pollution control of a hospital wastewater which
simultaneously contained heavy metals and antibiotics.
Experimental
Metals solution
A stock solution for each metal was separately made by dis-
solving 0.1550 g Pb(NO3)2, 0.2744 g Cd(NO3)2·4H2O, and
0.4340 g Ni(NO3)2·4H2O in 100 mL of double distilled water
(electrical conductivity < 10 μS cm−1). Metal stock solutions
were diluted to prepare the working solution with a
concentration of 10 mg L−1.
Preparation of bio-adsorbent
The C. sapidus crab was obtained from the northern coast of
the Persian Gulf, Bushehr, Iran. Dead crabs that were trapped
in the fishing creel of the fishery were discarded and its waste
(claws, chest, legs, and shell) was used for the production of
the bio-adsorbent material. The wastes after being separated
were washed with enough running water to remove the sand
and attached layers. Then, it was put in an oven (110 °C) for
48 h and fully dried. The dried biomass was powdered by a
Molineux mill (made in Germany), granulated by sieve no. 25
(ASTM E11), and finally stored inside the plastic-cap bottles
at 4 °C as bio-adsorbent.
Measurement techniques
A digital pH meter (Metrohm 744) device was used to measure
the samples’ pH before and after the bio-adsorption process. The
concentration of heavy metal ions of lead, cadmium, and nickel
inside aqueous solutions and the crab wastes was analyzed using
6338
inductively coupled plasma atomic emission spectroscopy (ICP-
AES 4100; Agilent). Details regarding metal analysis using this
instrument were provided elsewhere (Safari et al. 2018). The
analysis of required parameters like biochemical oxygen de-
mand (BOD5) and chemical oxygen demand (COD) was per-
formed according to Standard Methods for Examination of
Water and Wastewater (Clesceri et al. 1998). The concentration
of the antibiotics in the hospital wastewater was detected by a
high-performance liquid chromatography instrument equipped
with an electrospray ionization tandem mass spectrometry
(HPLC–ESI-MS-MS). All details including preparation of the
samples, quality analysis and quality control, the recovery per-
centages, and limits of quantification (LOQ) are presented in our
previous study (Kafaei et al. 2018).
An infrared spectrometer (FTIR) (Bruker Vector 22) was
used to detect the functional groups inside the bio-adsorbent
prepared from blue crab wastes, and the prepared infrared
spectrum before and after the bio-adsorption process of lead,
nickel, and cadmium was recorded at 400–4000 cm−1. To
examine superficial changes of the bio-adsorbent before and
after adsorption of the mentioned heavy metals, the energy-
dispersive X-ray (EDX) and mapping analyses were done
using a scanning electron microscope (SEM; Hitachi S4160,
Japan) at an acceleration voltage of 15 kV after the bio-
adsorbent samples were coated with a thin layer of gold. The
main compositions of the C. sapidus bio-adsorbent were de-
termined using an X-ray fluorescence spectrometer (XRF;
Oxford ED 2000 model). TEM images of the bio-adsorbent
were prepared using transmission electron microscope model
LEO 906 at voltage = 80 kV and scale = 200 nm and 250 nm.
An atomic force microscope tool (AFM; NanoScope III,
Digital Instruments Co., USA) was applied to observe mor-
phological structures of the bio-adsorbent particles.
Bio-adsorption procedure
The bio-adsorption process for control of lead, cadmium, and
nickel from the aqueous stream was discontinuously done
using the C. sapidus bio-adsorbent. All tests were conducted
at 500 rpm inside 250-mL Erlenmeyer flasks containing
100 mL solution with initial metal concentration of
10 mg L−1. A heater with a magnetic stirrer (yellow MAG
HS 7) was applied to supply heat and simultaneously agitate
the working solutions. The impacts of parameters such as
temperature, contact time, pH, and bio-adsorbent quantity
were considered on the bio-adsorption efficiency of heavy
metal ions. The initial pH of the working solution was set
and studied in the range of 2–9 to examine the effect of pH
on the bio-adsorption efficiency of cadmium, nickel, and lead
ions. Dilute solution of 1 M sodium hydroxide or sodium
chloride was used to regulate the initial pHs of solutions.
Tests were accompanied in conditions of 3 g L −1 bio-
adsorbent dose, 500 rpm stirrer rate, 10 mg L−1 metal ion
Environ Sci Pollut Res (2019) 26:6336–6347
concentration, 25 °C temperature, and 60 min contact time
to determine the optimum pH value. In order to examine the
effect of temperature and contact time on the bio-adsorption
efficiency of metal ions, the bio-adsorption process was man-
aged at the conditions of 25–55 °C temperature, 5–130 min
contact time, the determined optimum pH, 500 rpm stirrer
rate, 3 g L−1 bio-adsorbent quantity, and 10 mg L−1 initial
concentration of metal ions. Similarly, the bio-adsorbent dose
was studied (1–10 g L−1) to examine the impact of bio-
adsorbent dose on the bio-adsorption efficiency of nickel,
lead, and cadmium. In all tests, the bio-adsorption percentage
of metals from the aqueous stream was calculated by Eq. 1:
 
HM i −HM t
Bio−adsorption ð%Þ ¼  100 ð1Þ
HM i
Moreover, the bio-adsorption capacity of metal ions per
gram used bio-adsorbent (qt) was determined using Eq. 2:
 
HMi−HM t
qt ¼ V ð2Þ
W
where HMi (mg L−1) and HMt (mg L−1) are the concentration
of heavy metal ions inside the solution at t = 0 and t = t, re-
spectively, V (L) is the aqueous stream volume containing
heavy metal ions, and W (g) is the used bio-adsorbent mass
inside the solution.
All tests were conducted three times and an average of
measurements was reported herein.
Hospital wastewater sampling
Hospital wastewater samples were taken from the influent of a
wastewater treatment plant (WWTP) in the Bushehr city
(28°55′N, 50°55′E), Iran. The sampling was done during
February 2016. A conventional activated sludge treatment
system was used in WWTP (flow rate = 14.5 m3 day−1). The
composite samples were gathered for three continuous days.
For each day, 200-mL sample taken every 8 h during a day
(i.e., 7:00, 15:00, and 23:00) was independently analyzed and
treated by the blue crab bio-adsorbent. Hospital wastewater
samples were transferred to the laboratory for half an hour and
kept at 4 °C before being treated.
Results and discussion
C. sapidus bio-adsorbent characteristics
The bio-adsorbent efficiency of heavy metal ion removal de-
pends on the adsorbent porosity and functional groups on the
adsorbent surface. The FTIR analyzer was used to identify the
present functional groups on the C. sapidus bio-adsorbent
surface (Fig. 1a). The used C. sapidus bio-adsorbent shows
Environ Sci Pollut Res (2019) 26:6336–6347
Fig. 1 Analysis of C. sapidus bio-adsorbent: (a) FTIR, (b, c) two-dimensional and three-dimensional AFM, (d) TEM
peaks at 3439–3845 cm−1 area which can be resulted by vi-
brations of the hydroxyl (OH) functional group on the
C. sapidus structure (Masoumi et al. 2016). The observed
peaks at 2929 cm−1 and 871 cm−1 show C–H functional group
in the bio-adsorbent structure (Venkateswarlu et al. 2015). The
peaks revealed at 1695 cm−1, 1646 cm−1, and 871 cm−1 area
correspond to C=O vibration in the carboxyl group. Some
peaks were observed at 1008 cm−1 to 669 cm−1 showing
PO43− group in C. sapidus bio-adsorbent structure (Salem
and Velayi 2012). It is to be noticed that the present peaks at
669 cm−1 can be resulted by vibration of the hydroxyl func-
tional group (Gogoi et al. 2013). After bio-adsorption of lead,
cadmium, and nickel ions, the position of the hydroxyl group
(3439–3845 cm−1) has changed compared to the pre-adsorp-
tion. Changes in the peak range of hydroxyl groups indicate
that the OH group changes from the multimer to the
monopolymer and the degree of polymerization of the hydrox-
yl group in the bio-adsorbent structure is reduced by the sorp-
tion of lead, cadmium, and nickel. This state makes more
change to connect and link the mentioned metals to the hy-
droxyl group (Anayurt et al. 2009). Peaks at 2929 cm−1 and
871 cm−1 area related to C–H functional group changed after
bio-adsorption of lead, cadmium, and nickel using C. sapidus
waste bio-adsorbent. These changes show that the C–H func-
tional group of C. sapidus bio-adsorbent is effective in bio-
6339
adsorption of the metals. The related peaks to C=O functional
group inside C. sapidus structure transferred to 1697 cm−1,
1643 cm−1, and 875 cm−1 position after lead ion sorption, to
1693 cm−1, 1642 cm−1, and 868 cm−1 for cadmium ion, and to
1648 cm−1 and 875 cm−1 range after nickel ion. The present
peaks in 1008 cm−1 and 669 cm−1 range show the vibration of
PO43− group transferred to 1029 cm−1 and 674 cm−1 range
after adsorption of lead ion, to 1022 cm−1 and 673 cm−1 range
after cadmium ion, and to 1015 cm−1 and 671 cm−1 range after
nickel adsorption. The results show that there are chemical
interactions and ion changes between OH, C–H, C=O, PO43
−
, and heavy metal ions in the bio-adsorption process of lead,
cadmium, and nickel using the crab sorbent.
AFM analysis was used to explore and study the thickness
and surface of the produced bio-adsorbent. In Fig. 1b and c, two-
dimensional and three-dimensional AFM images of the blue
crab bio-adsorbent are shown, respectively. Based on the two-
dimensional AFM image, the bio-adsorbent particles have the
same color, which can be deduced that they have almost the
same thickness (Peng et al. 2016). Considering the AFM 3D
image (Fig. 1c), peaks, ruggedness, and couriers are observed, it
can be concluded that the crab bio-adsorbent has a porous and
rugged surface (Masoumi et al. 2016). Pores and porosity of the
bio-adsorbent prepared from C. sapidus are also visible in the
SEM images, which can confirm the AFM analysis.
6340
Another effective examination in the metal adsorption
using adsorbents is the constitutional elements and com-
pounds in adsorbent structure. The constitutional elements of
the C. sapidus waste are shown in Table S1 in the supplemen-
tary material. According to the results, most of the constituents
of the bio-adsorbent included CaO, P2O5, and MgO. In addi-
tion, the oxide of other compounds was found in the bio-ad-
sorbent, as expressed in Table S1. The major components of
the C. sapidus adsorbent are effective in adsorbing or combin-
ing with lead, cadmium, and nickel ion, and thus increase the
sorption efficiency.
TEM, SEM, and mapping analyses were used to determine
the size, element distribution, and morphology of the prepared
adsorbent from C. sapidus wastes. The results of TEM were
shown in 250 nm scale (see Fig. 1d). Based on TEM analysis,
it could be concluded that the prepared adsorbent from
C. sapidus shell is made from particles with different shapes,
and the size of some particles is very fine. Therefore, it can be
estimated that the size of the used particles is not in nano-scale
(100–200 nm). The SEM analysis of the prepared bio-
adsorbent before and after the adsorption of lead, cadmium,
and nickel ions are shown in Fig. 2a–j. The obtained SEM
images showed that the bio-adsorbent has ragged, irregular,
and porous surface with various pores which can be effective
in the adsorption process of heavy metal ions from aqueous
media. The SEM image of the reacted bio-adsorbent showed
that the porosity of the sorbent surface is filled with metal
contaminants and there have been significant changes in the
morphology of the bio-adsorbent that arise from the removal
of metal ions by active sites present on the adsorbent surface.
The results of mapping analysis of the fresh and used bio-
adsorbent are shown in Fig. 2. This analysis shows the density
and distribution of the elements that make up the C. sapidus
adsorbent structure before and after the removal of metal ions.
It should be noted that in map analysis, the elements with high
percentages were shown.
Elemental analysis was used to study the elements in the
bio-adsorbent structure prepared from the C. sapidus before
and after the adsorption of lead, cadmium, and nickel.
According to Fig. 2c, f, i, and l, the amount of lead, cadmium,
and nickel ions in the bio-adsorbent prior to the reaction is
zero, while these ions are detectable in the structure of reacted
adsorbent. In the EDAX analysis, the presence of metal ions in
the reacted bio-adsorbent confirms that the sorption of the
pollutants has been successful.
Effect of pH
The pH effect on the bio-adsorption of lead, cadmium, and
nickel ions was studied in the range of 2–9 and results are shown
in Fig. 3. The removal efficiency of metal ions increased from
37.42% to 97.1% for lead, from 31.18% to 96.6% for cadmium,
and from 33.18% to 95.1% for nickel by increasing pH from 2
Environ Sci Pollut Res (2019) 26:6336–6347
to 6, and maximum bio-adsorption of lead, nickel, and cadmium
was recorded at pH = 6. Many factors support the effect of initial
solution pH on adsorption process including the composition
and complexity of the C. sapidus bio-adsorbent and the charac-
teristics, ionic radii of the target adsorbate and co-existing ions,
and adsorption behavior of heavy metals (Rafatullah et al. 2009;
Ahmadi et al. 2017). In low solution pHs (< 3), the bio-
adsorption process efficiency of the pollutant ions is low be-
cause heavy metal ions inside the solution compete with hydro-
gen ions (H+) to occupy the active sites on the C. sapidus ma-
terial, thus preventing binding of heavy metals to the bio-
adsorbent surface (Rafatullah et al. 2009). With increasing pH,
the amount of positive loads decreases on the bio-adsorbent
surface, and therefore the electrostatic gravity force between
the metal ions and the active sites on the surface of the crab
waste material increases. As a result, the efficiency of the metal
ion bio-adsorption procesb–ks increased. Attaining the maxi-
mum efficacy of heavy metals adsorption in pH = 6 could be
justified by the interactions between M+, M(OH)+, and M(OH2)
with the present functional groups on the bio-adsorbent surface.
Published studies suggest (Zheng et al. 2016; Mohan and Singh
2002) that the ionic radii may affect the adsorption of the metal.
The smaller the ion radii, the greater the electronegativity, and
thus, the greater adsorption occurs (Mahmoud et al. 2018;
Zheng et al. 2016). The hydrated ion radii of nickel, lead, and
cadmium ions are 0.600 nm, 0.590 nm, and 0.500 nm, respec-
tively (Zheng et al. 2016). At pH solution of 6, the removal
efficiency of all three metals is approximately equal (taking into
account the error bars). Therefore, more factors are likely to
affect the removal of metals by the C. sapidus biomass. At high
pHs (> 6), the bio-adsorption efficiency decreased, which could
be due to the formation of a metal ion complex with the hydrox-
ide ion (OH−) in the aqueous stream. This is due to the mecha-
nism of ion modification of the active agent groups at the surface
of the bio-adsorbent or the hydrogen ion bond shown below
(Rafatullah et al. 2009):

2ð−ROHÞ þ ½HM2þ →2Hþ þ 2ðROÞ½HM
Ion exchange −ROH þ ½HMðOHÞþ →Hþ þ ð−ROÞ½HMðOHÞ
2ð−ROHÞ þ ½HMðOHÞ2 →ð−ROHÞ2 þ ½HMðOHÞ2 H−bonding
where [HM] and R indicate heavy metal and C. sapidus
biomass.
Effect of temperature and contact time
Optimization of equilibrium time is one of the important pa-
rameters to develop an adsorption system. The effect of con-
tact time on the removal efficiency of lead, cadmium, and
nickel using C. sapidus bio-adsorbent is depicted in Fig. 4.
The bio-adsorption efficiency of the toxic heavy metals in-
creased by increasing the contact time to 60 min, then it was
relatively constant. The bio-adsorption of metal ions happened
at a higher rate in the initial contact times because of the empty
Environ Sci Pollut Res (2019) 26:6336–6347
Fig. 2 Analysis of SEM, mapping, and EDX of fresh C. sapidus bio-adsorbent (a, b, c), after bio-adsorption of Pb (d, e, f), after bio-adsorption of Cd (g,
h, i), and after bio-adsorption of Ni (j, k, l)
available active sites on the C. sapidus bio-adsorbent surface.
It should also be noted that at the initial times of contact, the
gradient of initial metal concentration in the solution is high
and over time, the gradient decreases (Nagy et al. 2014).
Therefore, the efficiency of the bio-adsorption process re-
mains nearly constant. The highest adsorption efficiency of
lead, cadmium, and nickel at 25 °C and 60 min was deter-
mined to be 97.1%, 96.6%, and 95.1%, respectively, and the
contact time of 60 min is the optimal time for the bio-
adsorption of all studied metals.
6341
Adsorption test was also conducted at the solution temper-
ature of 25–55 °C to examine the effect of temperature on the
bio-adsorption efficiency of toxic heavy metal ions, and re-
sults are shown in Fig. 4. Results show that the bio-adsorption
of lead, cadmium, and nickel is a temperature-dependent re-
action. The bio-adsorption percent of lead, cadmium, and
nickel at 60 min equilibrium time and 25–55 °C temperature
range was reduced from 97.1% to 89.37% for Pb, from 96.6%
to 88.42% for Cd, and from 95.1% to 88.37% for Ni. These
results record that the adsorption of lead, cadmium, and nickel
6342 Environ Sci Pollut Res (2019) 26:6336–6347

100
Pb (II) leave the adsorbent surface (solid phase) and is delivered to
90 the solution (Sarı and Tuzen 2009) or damage the active sites
Cd (II)
on the bio-adsorbent surface (Sari et al. 2008). Therefore, the
Adsorption (%)

80

70
Ni (II) solution temperature of 25 °C was chosen as an excellent
temperature for bio-adsorption of lead, cadmium, and nickel
60
metals from aqueous solutions by the C. sapidus bio-
50 adsorbent.
40

30
Effect of bio-adsorbent dose
2 3 4 5 6 7 8 9
pH value
The influence of bio-adsorbent quantity on the toxic metal ad-
Fig. 3 Impact of pH (metal concentration = 10 mg L−1, agitation speed = sorption is represented in Fig. 5. By increasing the bio-adsorbent
500 rpm, temperature = 25 °C, time of contact = 60 min, and bio-
dose from 1 to 3 g L−1, the sorption efficiency was increased
adsorbent quantity = 3 g L−1)
from 75.45% to 97.1% for Pb, from 70.343% to 96.6% for Cd,
and from 68.43% to 95.1% for Ni. This increase in the removal
is an exothermic process. Generally, the reduction of removal
efficiency could be due to the accessibility of a greater surface
efficiency for lead, cadmium, and nickel ions by extending the
area of the bio-adsorbent for the placement of toxic metals in the
temperature can be resulted from the intention of metal ions to
aqueous environment (Saber et al. 2018). Consequently, by in-
100 creasing the bio-adsorbent quantity, the surface and number of
(Pb) active sites are sufficiently provided to easily penetrate and
Bio-adsorption (%)

90
placement of heavy metal ions. By increasing the C. sapidus
80
25°C dose (> 3 g L−1), the metal bio-adsorption efficiency was almost
70 constant, which could be due to the collision of bio-adsorbent
35°C
60 45°C particles with each other and, consequently, their condensation
50 55°C (Sarı and Tuzen 2009). Congestion of bio-adsorbent particles
can interrupt the active sites and reduce the effective surface to
40
0 20 40 60 80 100 120 140 put metal ions. Thus, the bio-adsorbent efficiency reduces by
Contact time (min) increasing its dosage. The bio-adsorbent quantity of 3 g L−1
was determined as the optimum value to recycle and remove
100 lead, cadmium, and nickel ions.
(Cd)
90
Bio-adsorption (%)

80 Isotherm study
25°C
70 35°C Equilibrium data for bio-adsorption of lead, cadmium, and
60 45°C nickel using C. sapidus biomass was analyzed by Langmuir
50 55°C and Freundlich isotherm models. The linear relationship of Ce/
40
qe versus Ce for nickel, lead, and cadmium ion bio-adsorption
0 20 40 60 80 100 120 140 is shown in Fig. S1 and the resulted graph was used to deter-
Contact time (min) mine the value of the Langmuir model parameters (KL and qm)
100 100
(Ni) Pb
90 95
Bio-adsorption (%)

Cd
Bio-adsorption (%)

80 90
25°C Ni
85
70
35°C
80
60 45°C
75
50 55°C
70
40
65
0 20 40 60 80 100 120 140 1 2 3 4 6 8 10
Contact time (min) Bio-adsorbent dose (g/L)
Fig. 4 Impact of time of contact and temperature on the bio-adsorption of Fig. 5 Effect of bio-adsorbent dosage on the adsorption of Pb(II), Cd(II),
toxic heavy metals onto C. sapidus bio-adsorbent (metal concentration = and Ni(II) onto Callinectes sapidus biomass (initial metal
10 mg L−1, bio-adsorbent quantity = 3 g L−1, pH = 6) concentration = 10 mg L−1, temperature = 25 °C, contact time = 60 min)
Environ Sci Pollut Res (2019) 26:6336–6347 6343

(see Table 1). The q m parameter was determined as
31.44 mg g−1, 29.23 mg g−1, and 29.15 mg g−1 for lead,
cadmium, and nickel, respectively. Table S2 lists the compar-
ison of the C. sapidus bio-adsorbent capacity with the other
adsorbents, which recognizes the admirable bio-adsorbent ca-
pacity to control toxic metals from aqueous media. The high
correlation coefficient (R2) of the Langmuir equation showing
this model has a proper ability in the description of the iso-
thermal behavior of lead, cadmium, and nickel bio-adsorption
using C. sapidus biomass. The RL (RL= 1/1 + KL. HMo) value
was determined to be 0.0409–0.299, 0.0584–0.383, and
0.0462–0.326 for lead, nickel, and cadmium, respectively,
showing the properness of the prepared bio-adsorbent to con-
trol and remove heavy metal ions from aqueous streams.
The linear relationship of ln qe versus ln Ce to adsorb nick-
el, lead, and cadmium is shown in Fig. S1. The linear relation-
ship of ln qe versus ln Ce was used to calculate Freundlich
model parameters (n, Kf). The n parameter was determined as
1.93, 1.95, and 2.03 to adsorb nickel, lead, and cadmium,
respectively. The n values confirm that the toxic metal ions
adsorption using C. sapidus bio-adsorbent is physically and
desirable as n < 1 (Foroutan et al. 2017b; Kyzioł-Komosińska
et al. 2015). The correlation coefficient value (R2) of the
Freundlich model was determined 0.9941, 0.9924, and
0.9901 for lead, cadmium, and nickel, respectively. Results
show that the Freundlich model is more able to describe the
equilibrium behavior of the adsorption process than the
Langmuir model and thus, the surface of bio-adsorbent was
energetically heterogeneous (Teimouri et al. 2017).
Thermodynamic study
To determine the adsorption behavior of lead, cadmium, and
nickel heavy metal using C. sapidus biomass, thermodynamic
parameter (enthalpy (ΔH°), entropy (ΔS°), and Gibbs free
energy (ΔG°)) values were determined under the conditions
of temperature = 25–55 °C, pH = 6, HMi = 10 mg L−1, bio-
adsorbent quantity = 3 g L−1, and contact time = 60 min.
Thermodynamic parameters are determined using the follow-
ing equations (Milonjić 2007):
ΔG° ¼ −RT lnð55:5  K D Þ ð3Þ
where ΔG° represents Gibbs free energy, R represents the
universal gas constant (8.314 J (mol K)−1), T represents abso-
lute temperature (K), KD represents equilibrium constant, and
the number 55.5 represents the amount of moles of H2O per
liter of solution. Equilibrium constant value of the bio-
adsorption is determined by Eq. (4):
qe
KD ¼ ð4Þ
Ce
The following equation was also used to calculate ΔH° and
ΔS°.
−ΔG° −ΔH ° ΔS °
lnð55:5  K D Þ ¼ ¼ þ ð5Þ
RT RT R
The parameters of ΔH° and ΔS° were determined by slope
and intercept of ln KD against 1/T diagram, respectively (Fig.
S2). The amount of thermodynamic parameters for the bio-
adsorption process of lead, nickel, and cadmium from aqueous
solution using crab biomass has been reported in Table 2. The
parameter of Gibbs free energy was determined to be negative
for three metals which shows that bio-adsorption is desirable
and spontaneous. With increasing temperature, the ΔG° values
decreased for adsorption of lead, nickel, and cadmium, which
shows that with increasing temperature, the spontaneity of the
process has decreased. ΔH° parameter was also determined
negative for the mentioned metal ion adsorption. Accordingly,
it can be concluded that interaction between C. sapidus biomass
and lead, nickel, and cadmium metals is exothermic. Moreover,
this parameter shows that metal ion adsorption is physical be-
cause of ΔH° < 40 kJ mol−1. The ΔS° value for lead, cadmium,
and nickel was measured as − 14.67 J (mol K) −1 , −
8.92 J (mol K)−1, and − 17.79 J (mol K)−1, respectively. This
parameter indicates that accidental collisions are reduced at the

Table 1 Bio-adsorption isotherm

parameters Isotherm model Parameter Pb Cd Ni

Langmuir qm (mg g−1) 31.44 29.23 29.15

Ce/qe = Ce/qm + 1/KLqm KL (L mg−1) 0.234 0.206 0.161
R2 0.9671 0.9613 0.9677
RL 0.0409–0.299 0.0462–0.326 0.0584–0.383
Freundlich n 1.959 2.035 1.937
ln qe = ln Kf + 1/n ln Ce Kf (mg g−1(L mg−1)1/n) 6.542 5.875 5.003
R2 0.9941 0.9924 0.9901

KL (L mg−1 ) is Langmuir constant; Ce, qe, and qm are equilibrium concentration (mg L−1 ), equilibrium capacity
(mg g−1 ), and maximum bio-adsorption capacity (mg g−1 ); Kf (mg g−1 (L mg−1 )1/n ) and n are Freundlich
constants
6344 Environ Sci Pollut Res (2019) 26:6336–6347

Table 2 Thermodynamic parameters list solid (bio-adsorbent) surface and solution during the sorption
−1 −1
Pollutant T (K) ΔG° (kJ mol ) ΔH° (kJ mol ) ΔS° (J (mol K) ) −1 process (Kalhori et al. 2013).

Pb(II) 25 − 33.05 − 37.22 − 14.67

35 − 32.44 Kinetic study
45 − 32.39
55 − 32.61 Pseudo-first and second-order kinetic, as two famous models,
Cd(II) 25 − 32.65 − 34.95 − 8.92 were used to study the kinetic behavior of lead, cadmium, and
35 − 31.72
nickel bio-adsorption using C. sapidus biomass. The kinetic
45 − 31.89
models are exhibited in Figs. S3 and S4. The kinetic parameters
55 − 32.35 and constant for the lead, cadmium, and nickel bio-adsorption
Ni(II) 25 − 31.70 − 26.26 − 17.79 are shown in Table 3. Pseudo-second-order model in comparison
35 − 31.66
to the pseudo-first-order kinetic model has a higher correlation
45 − 31.63
coefficient (R2) showing the metal adsorption using C. sapidus
55 − 32.33
bio-adsorbent follows the pseudo-second-order model. The de-
termined bio-adsorption capacity (qe.cal) using the pseudo-first-
order model is not constantly and definitely changed by

Table 3 Results of bio-adsorption kinetic study

Kinetic model Parameters Temperature (°C)

25 35 45 55

Pseudo-first-order (Pb) qe.cal (mg g−1) 2.145 2.334 2.208 2.714

k1 (min−1) 0.0558 0.0548 0.0513 0.0598
qe.exp (mg g−1) 3.277 3.195 3.117 3.042
R2 0.9579 0.948 0.9533 0.9706
Pseudo-first-order (Cd) qe.cal (mg g−1) 2.976 2.134 2.751 2.687
k1 (min−1) 0.071 0.0515 0.0626 0.058
qe.exp (mg g−1) 3.241 3.156 3.0746 3.028
R2 0.9469 0.9687 0.9857 0.9796
Pseudo-first-order (Ni) qe.cal (mg g−1) 2.346 3.085 2.8 3.012
k1 (min−1) 0.0519 0.0674 0.0608 0.0607
qe.exp (mg g−1) 3.227 3.127 3.057 3.017
R2 0.9447 0.9701 0.9822 0.9768
Pseudo-second-order (Pb) qe.cal (mg g−1) 3.449 3.392 3.321 3.26
k2 (g (mg min)−1) 0.0486 0.041 0.0397 0.0376
qe.exp (mg g−1) 3.277 3.195 3.117 3.042
R2 0.9986 0.9979 0.9981 0.9971
Pseudo-second-order (Cd) qe.cal (mg g−1) 3.436 3.359 3.293 3.254
k2 (g (mg min)−1) 0.044 0.0404 0.0391 0.0364
qe.exp (mg g−1) 3.241 3.156 3.0746 3.028
R2 0.9977 0.9979 0.9979 0.9978
Pseudo-second-order (Ni) qe.cal (mg g−1) 3.404 3.359 3.294 3.287
k2 (g (mg min)−1) 0.0432 0.0369 0.0355 0.0307
qe.exp (mg g−1) 3.227 3.127 3.057 3.017
R2 0.9934 0.9967 0.997 0.9953

(Pseudo-first-order) ln(qe − qt) = ln qe − k1t

 
(Pseudo-second-order) qt ¼ k 21q2 þ qt
t e e

qe = weight of adsorbed ions per weight of bio-adsorbent at equilibrium state (mg g−1 ), k1 = pseudo-first-order model constant (min−1 ), k2 = pseudo-
second-order constant (g (mg min)−1 )
Environ Sci Pollut Res (2019) 26:6336–6347 6345

changing the temperature in comparison to the pseudo-second-
order kinetic model. It is worth noting that the values of bio-
adsorption capacity determined using pseudo-first-order kinetic
model are lower than that determined using the pseudo-second-
order model. Therefore, it can be argued that the pseudo-first-
order model is not well suited to describe the kinetic behavior of
the lead, cadmium, and nickel sorption process by using crab
biomass (Yadav et al. 2014), and the kinetic behavior of the
process follows a pseudo-second-order model.
The bio-adsorption function of heavy metal ion removal
from aqueous solutions using the blue crab biomass can be
evaluated by the following equations:
1
Rw ¼
1 þ k 2 qe t w
Ri ¼ k 2 qe
1 anisms which are useful for modeling and designing of com-
t 1=2 ¼
k 2 qe
w
tx ¼
k 2 qe
The value of Rw kinetic parameter for lead, cadmium, and
nickel bio-adsorption process was determined as 0.043, 0.048,
and 0.049, respectively, showing that the process is highly
near equilibrium state. The value of Ri kinetic parameter for
lead, cadmium, and nickel adsorption onto C. sapidus biomass
was calculated to be 0.16 min−1, 0.15 min−1, and 0.14 min−1,
and the parameter of t1/2 (half-life of the heavy metals in the
solution) was also determined as 5.96 min, 6.61 min, and
6.80 min. The half-life value of the bio-adsorption process
shows that metal ion removal using C. sapidus biomass hap-
pens fast. Further, the Ri parameter is an important and essen-
tial factor to determine a bio-adsorption fraction. The calcu-
lated tx data (for removing lead, cadmium, and nickel by the
ð6Þ blue crab sorbent) at different values of x are reported in
Table S3. Data of kinetic performance is important and effec-
ð7Þ tive to understand rate-limiting step and bio-adsorption mech-
ð8Þ mercial applications of the adsorbent.
ð9Þ Hospital wastewater treatment

where Rw is the nearest equilibrium factor, tw (min) is the
maximum conduction time of the process, Ri (min−1) is the
bio-adsorption rate of second-order kinetic, t1/2 (min) is the
essential time for bio-adsorption of half of the metals, tx is the
needed operational time for a part of desirable bio-adsorption
(x = qt/qe), and w = x (1 − x)−1. Rw kinetic parameter can show
various states of the process. If 0.1 < Rw < 1, the process is
near equilibrium state; if 0.01 < Rw < 0.1, it is well near equi-
librium state; and if Rw < 0.01, the process is highly near
equilibrium state (Foroutan et al. 2018).
In the final part of the work and in optimal conditions (i.e., the
bio-adsorbent dose of 3 g L−1, temperature 25 °C, but without
altering the pH parameter), the wastewater sample was treated
with the crab waste bio-adsorbent. The results of this section are
presented in Table 4. As shown in Table 4, the hospital wastewa-
ter contained antibiotic compounds. Six antibiotics of significant
amounts were found in the wastewater. The highest and lowest
antibiotic levels were detected for norfloxacin (149.63 ng L−1)
and cephalexin (7.89 ng L−1), respectively. The amount of anti-
biotics in the wastewater is within the range of values reported by

Table 4 The compositions of the

hospital wastewater after and Property (unit) Untreated value Treated value Efficiency (%)
before treated by C. sapidus bio-
adsorbent (n = 3) Tetracycline (ng L−1) 67.78 ± 6.5 27.58 ± 4.56 59.30
Norfloxacin (ng L−1) 149.63 ± 10.08 112.39 ± 11.51 24.88
Azithromycin (ng L−1) 18.35 ± 3.25 7.25 ± 1.10 60.49
Anhydroerythromycin (ng L−1) 10.28 ± 1.29 4.15 ± 0.39 59.63
Cephalexin (ng L−1) 7.89 ± 1.10 Non-detectable ≈ 100
Amoxicillin (ng L−1) 17.68 ± 5.64 9.54 ± 1.47 46.04
BOD5 (mg L−1) 280 ± 15.9 252 ± 12.6 10
COD (mg L−1) 625 ± 24.6 551 ± 29.7 11.84
Nitrate (mg L−1) 159.2 ± 14.3 143.5 ± 10.9 9.86
Ammonium (mg L−1) 59.6 ± 7.51 41.2 ± 4.87 30.87
Pb(II) (mg L−1) 0.32 ± 0.05 Non-detectable ≈ 100
Cd(II) (mg L−1) 0.09 ± 0.04 Non-detectable ≈ 100
Ni(II) (mg L−1) 0.10 ± 0.05 Non-detectable ≈ 100
pH (unit of pH) 6.8 ± 0.15 7.1 ± 0.1 –
PO43− (mg L−1) 10.16 ± 2.73 8.98 ± 1.1 11.61
Cl− (mg L−1) 335.75 ± 19.8 277.80 ± 15.64 17.25
SO42− (mg L−1) 105 ± 11.77 76 ± 12.90 27.61
6346
other researchers (Tran et al. 2016; Watkinson et al. 2007; Kafaei
et al. 2018). The removal efficiency of antibiotics by the crab bio-
adsorbent was achieved in the range of 24–100%, depending on
the type and initial concentration of antibiotics. Similar to our
work, three types of antibiotics (ofloxacin, azithromycin, and
sulfamethoxazole) were treated with zeolite powder and their
removal efficiency was in the range of 43–75% (de Sousa et al.
2018). The three heavy metals of this study (cadmium, lead, and
nickel) were detectable to a small extent in hospital sewage and
were completely eliminated using bio-adsorbent. Other anions
and cations mentioned in Table 4 were also partially affected by
the blue crab bio-adsorbent. The amount of pH in the treated
wastewaters slightly changed, which probably indicates that the
C. sapidus biomass is an amphoteric substance.
Conclusions
This research was conducted to examine the bio-adsorption
ability of lead, cadmium, and nickel ions using C. sapidus bio-
mass as a low-cost bio-adsorbent. Adsorption process of heavy
metals was done in discontinuous mode and the effects of pa-
rameters such as initial pH, temperature, contact time, and bio-
adsorbent quantity were examined. The obtained result from
FTIR showed that the C. sapidus bio-adsorbent has P–H, C–
H, C=O, and PO43− functional groups which can be effective in
chemical interactions and ion exchange with heavy metals.
Kinetic data were suitably described by the pseudo-second-
order model. Considering the half-life of the metal ions (t1/2)
and the value of the Rw parameter, it could be concluded that the
bio-adsorption process quickly approaches the desirable remov-
al and achieves a good equilibrium. Both Freundlich (R2 >
0.96) and Langmuir (R2 > 0.99) models were able to describe
the data. The Langmuir bio-adsorption capacity for lead, cad-
mium, and nickel was determined as 31.44 mg g −1 ,
29.23 mg g−1, and 29.15 mg g−1, respectively. Enthalpy value
for lead, cadmium, and nickel adsorption process was deter-
mined as − 37.225 kJ mol −1, − 34.95 kJ mol −1, and −
26.261 kJ mol−1 pointing that the heavy metal bio-adsorption
using the C. sapidus biomass is exothermic. The enthalpy value
of the adsorption process is negative confirming that the metal
ion bio-adsorption is spontaneous. The hospital wastewater
containing antibiotics and heavy metals was successfully atten-
uated using bio-adsorbent of C. sapidus blue crab, which illus-
trates the benefits of adsorbent material in this study.
Acknowledgements The authors acknowledge the University of Tabriz
for financial support (grant no. Tab-132-96) and Bushehr University of
Medical Sciences for technical support to conduct this work.
Compliance with ethical standards
Declarations of interest None.
Environ Sci Pollut Res (2019) 26:6336–6347
Publisher’s Note Springer Nature remains neutral with regard to jurisdic-
tional claims in published maps and institutional affiliations.
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