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319
Advances in Environmental Biology, 6(1): 319-326, 2012
ISSN 1995-0756
This is a refereed journal and all articles are professionally screened and reviewed
ORIGINAL ARTICLE
Comparative study of heavy metal (Cd, Fe, Mn, and Ni) concentrations in soft tissue of
gastropod Thais mutabilis and sediments from intertidal zone of Bandar Abbas
1
M. Astani, 1A.R. Vosoughi, 1L. Salimi, 2M. Ebrahimi
1
2
Islamic Azad University, North-Tehran branch, Iran.
Persian Gulf and Oman Sea Ecological Research Institute, Bandar Abbas, Iran.
M. Astani, A.R. Vosoughi, L. Salimi, M. Ebrahimi; Comparative study of heavy metal (Cd, Fe, Mn,
and Ni) concentrations in soft tissue of gastropod Thais mutabilis and sediments from intertidal zone of
Bandar Abbas
ABSTRACT
This study was performed to determine the concentrations of heavy metals in sampled sediments and
individuals of Thais mutabilis. Sediments and T. mutabilis were collected from three stations of the Bandar
Abbas (NE Persian Gulf) in winter 2011, and the metal concentrations were determined for them. The sediments
maximum values (in microgram per gram dry weight [d.w.]) were 11764.69 for Fe; 444.19 for Mn; 66.23 for
Ni; and 1.88 for Cd. Specimens of T. mutabilis could be collected from all the sampling stations and the
concentrations of the heavy metals in their soft tissues were found respectively as follow: Fe (between 156.65
and 637.18 µgg-1 d.w.), Mn (between 8.68 and 57.37 µgg-1 d.w.), Ni (between 0.70 and 13.67 µgg-1 d.w.), and
Cd (between 1.90 and 35.54 µgg-1 d.w.). In three stations the Concentrations of Fe, Mn and Ni in sediment and
T. mutabilis did not differ significantly (p>0.05) but the value of Cd in sediment and T. mutabilis differed
significantly (p< 0.05). The main positive correlation was found between concentration of Ni in T.mutabilis and
sediments (p < 0.0001, r = 0 .941). The concentration of Cd in soft tissues of T.mutabilis was more than its
value in sediments, which demonstrate the potential of T. mutabilis as bioindicators of Cd and Ni pollution.
Key words: Bioaccumulation-Heavy metals-Gastropods-Persian Gulf-Polluted sediments.
Introduction
Metals transport to aquatic environment from
natural sources such as volcanic emissions, forest
fires, and anthropogenic sources such as urban,
industrial & agriculture wastes, fossil fuels, garbage
& solids wastes dump and etc [14,18].
Metal pollution can affect sediments and
organisms and have a risk to human health [19,10].
To determine the amount of metals in aquatic
environments can be analyzed water, sediments and
marine organisms. Biomonitoring can provide useful
information to determine the metals pollution in
aquatic ecosystem [32,19,34,10].
The use of soft tissue of marine snails is not a
new suggestion since numerous studies have already
been reported [27,13,16,12,18,10]. There are,
however, several factors (age, size, sex, sexual state
and physiological functions) that affect metal
accumulation in the soft tissue of molluscs. From
these factors body size play a major rule for
accumulation
of
metals
in
soft
tissue
[7,11,8,13,31,12,10].
Chan [11] suggested that levels of metals
accumulated in some marine organisms may be more
than its value in background which demonstrate the
potential of species as bioindicators of metal
pollution [19]. Moreover, studying the relationships
between the concentrations of pollutants in the
sediments and organism can be a valuable tool to
assess the contamination levels [10].
Muricids occur in all warm waters, especially
within the tropics and prey upon invertebrates,
including other molluscs such as barnacles and
bivalves [6]. Thais mutabilis (Link, 1807) is one of
the caenogastropod muricids and lives on muddy
littoral rocks (FAO web site).
Previous studies, however, have shown that the
Persian Gulf receives contaminant metals by various
industrial outputs (including: thermal power plant
and oil refinery in Bandar Abbas [22,25].
The aims of this study were: (a) to determine the
levels of metals in soft tissue of gastropod Thais
mutabilis and sediments from intertidal zone of
Bandar Abbas; (b) to assess the existence of length
dependent differences in metal contents of the Thais
mutabilis; and (c) to study if the species of Gastropod
analyzed could be acceptable biomonitors of metal
pollution in the Persian Gulf and other similar
systems.
Corresponding Author
M. Astani, Islamic Azad University, North-Tehran branch, Iran.
Ph: +989122061138 E-mail: [email protected]
320
Adv. Environ. Biol., 6(1): 319-326, 2012
Materials and Methods
2.1 Study area:
The Persian Gulf is large basin with an average
depth of 35–40 m, a total area of around 240,000
km2. The northern part of Persian Gulf, Due to the
low depth, restricted rotation; high salinity and
temperature are much more affected by pollutants
[28,1,22,4]. Three stations were selected for the
sampling from the tidal shores of Bandar Abbas (NE
Persian Gulf) during low tides in January 2011 (Fig.
1). Sampling location position was detected using
GPS (Table 1).
Fig. 1: Map of sampling sites.
Table 1: Geographical information of sampling area in Bandar Abbas coast, winter 2011.
Name of area
Station
X
Y
South Golshahr
1
E 56°19.294
 N 27°10769
Posht-e- shahr waterfront
2
E 56°15.647
N 27°10163
Soro
3
E 56°14.850
N 27°09.391
2.2 Thais mutabilis Sampling and Analysis:
Nine subsamples of a marine snail, Thais
mutabilis Link, 1807(Mollusca, Gastropoda) were
collected by hand at each station. Samples were
rinsed with seawater from their sampling locations
and were put in acid-washed polyethylene bags and
transported to the laboratory [24]. In the laboratory,
samples were sized and placed in acid-washed
polyethylene bags and frozen at -20oC until analysis.
At a later date, the whole soft tissues were removed
from their shells by using a stainless steel crusher
and rinsed quickly with distilled water. All soft
tissues of marine snails were dried at 105oC until
constant dry weight (dw) [3]. Then 0/5 g of each
dried tissues with three replicates were digested in
concentrated HNO3 & HCLO4 (Merck) in the ratio
of 3:1. Samples were put into a hot-block digester at
140oC for at least 1.5 h [3]. The digested samples
were filtrated by using filter paper (Whatman No. 42)
and diluted with double deionized water
appropriately in the range of standards which were
prepared from stock standard solution of the metals
(Merck). After dilution, the metals contents of
tissues, Cd, Fe, Mn and Ni were analyzed by using
flame atomic absorption spectrometer (Varian, model
AA-220) and metals concentration in soft tissues
were presented as microgram metal/gram dry weight.
2.3 Sediments Sampling and Analysis:
At each station, three subsamples of sediment
were taken (top 10 cm), put in acid-washed
polyethylene bags, and homogenized. In the
laboratory, sediment samples were dried at 105oC
until constant dry weight [2]. The dried sediment
samples were sieved through a 0/5 mm aperture
stainless steel sieve and were shaken vigorously to
produce homogeneity. For the analyses of total Cd,
Fe, Mn and Ni concentrations in the sediment
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Adv. Environ. Biol., 6(1): 319-326, 2012
samples 0/5 g of each dried sediment samples with
three replicates were digested in concentrated HNO3
& HCLO4 (Merck) in the ratio of 3:1.Samples were
put into a hot-block digester at 140oC for at least 1.5
h [2]. The digested samples were filtrated by using
filter paper (Whatman No. 42) and diluted with
double deionized water appropriately in the range of
standards which were prepared from stock standard
solution of the metals (Merck). Metals were
measured in the same equipment as in the case of the
molluscs.
2.4 Statistical Analysis:
Statistical analysis was performed with SPSS
18.0 software. One-way ANOVA of variance with
the 95% confidence interval followed by a Tukey
HSD test was accepted to check the differences
between concentrations of metals in the T. mutabilis
and sediment samples in different stations.
Pearson correlation & Regression analysis was
used, to test the relationships among the
characteristics of the sediments and metal
concentrations in the T. mutabilis, although to test
the relationships between body size and metal
concentrations in T.mutabilis.
3. Results:
3.1 Sediments:
Concentrations of metals in sediment samples
indices are in Fig. 2 and Table 3. The highest
concentrations in sediments for all metals (Cd:
1/8433±0/06351, Fe: 10717/1767± 1052/99211, Mn:
417/3067± 33/16178 & Ni: 53/7300± 10/89053)
were recorded at station 2.
The one way analysis of variance (ANOVA)
performed; no significant differences (P > 0.05) were
recorded between the concentrations of Fe, Mn, and
Ni in the sediment samples from the three stations.
Significant differences (P > 0.05) were recorded
between the concentrations of Cd in the sediment
samples from the station 1 & 2 with 3.
The pattern of the metal occurrence in the
sediments of all the stations could be arranged in the
following sequence:
Fe >Mn> Ni > Cd (Fig. 2).
3.2 Thais mutabilis:
Specimens of T.mutabilis could be collected at
all the sampling sites. Total length (size range) of
T.mutabilis at three stations are given in Table 2.
T.mutabilis specimens that collected from station 1
was significantly smaller than those collected from
the other stations (p<0.05).
Concentrations of metals in soft tissues of
T.mutbilis varied as follows (µgg-1 d.w.): Cd between
12/9822±10/64148 (station 1) and 4/4178±3/43636
(station 2); Fe between 403/6433±116/80310 (station
3) and 252/2744±104/21001 (station 2); Mn between
17/9578±8/41192 (station 1) and 15/9644±5/43223
(station 3); Ni between 3/8778±2/90094 (station 2)
and 2/6567±1/35648 (station 1)(Fig. 3).
The one way analysis of variance (ANOVA)
performed; no significant differences (P > 0.05) were
recorded between the concentrations of Fe, Mn, and
Ni in the T.mutabilis samples from the three stations.
Significant differences (P < 0.05) were recorded
between the concentrations of Cd in the T.mutabilis
samples from the station 2 with 1.
The pattern of the metal occurrence in the soft
tissues of T. mutabilis of all the stations could be
arranged in the following sequence:
Fe >Mn > Cd >Ni (Fig. 3).
Size dependent relationship with the metal
content measured in T.mutbilis is shown in Fig. 4.
These figures shows that for Cd, content increases
with the decrease of length, as expressed by the
strong negative relationships between metal content
and total length (p<0.0001, r = - 0.640).
Relationships among the metal concentrations in
the sediments and in T.mutbilis are shown in Fig. 5.
Only the significant positive correlation was found
between Ni Concentration in T. mutabilis and in the
sediments (p < 0.0001, r =0 .941).
Discussion:
The results of the present study show that the
highest concentrations in sediments for all metals
that were recorded at station 2.This founding may be
attributed to one or more of the following reasons:
(a)The motor-boats traffic in the Posht-e-shahr
waterfront entering the engine oil and the entry of oil
pollution.
(b) Discharge of untreated municipal sewage [18]
from the city of Bandar Abbas.
(c) A large amount of waste had been accumulated in
this station that, leaching of metals from solids
wastes dump [18].
The one way analysis of variance (ANOVA)
performed, significant differences (P > 0.05) were
recorded between the concentrations of Cd in the
sediment samples from the station 1 & 2 with 3 .This
finding can, at the first station for urban waste water
effluent and in the second station due to factors listed
above (a, b and c). So, Cadmium contamination in
the first and second station is more than the station 3,
the sewage effluent that is no more.
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Adv. Environ. Biol., 6(1): 319-326, 2012
Table 2: Total length of T.mutabilis at three stations in the Bandar Abbas coast, winter 2011 (mm).
n
Min
Max
Mean ± 1 SD
Station 1
9
37/51
46/30
41/05± 3/35
Station 2
9
44/19
52/38
48/01± 2/56
Station 3
9
44/30
50/33
47/47± 2/15
14000
2.5
12000
2
Cd µgg -1 (d.w.)
Fe µgg -1 (d.w.)
10000
8000
6000
4000
1.5
1
0.5
2000
0
0
1
2
3
1
2
Station
3
Station
70
500
450
60
400
50
Ni µgg -1 (d.w.)
Mn µgg -1 (d.w.)
350
300
250
200
150
40
30
20
100
10
50
0
0
1
2
3
Station
1
2
3
Station
Fig. 2: Fe, Cd, Mn, and Ni contents in sediment samples taken from three sampling stations in the Bandar
Abbas (in µgg-1 d.w.). Lines over the bars indicate 1 SD (n=3).
Maximum and minimum value of Fe
(10717/1767± 1052/99211 – 9420/0800 ±
340/08055) & Mn (417/3067± 33/16178 – 368/4467
± 9/47498) in sediments was recorded at same
station, 2 and 1 respectively. This is in confirmation
with the findings of Hamed and Emara [19], this can
be described by the reality that their hydroxides are
impulsive together in the bottom [26], and the
chemical science [5].
Results in Table 3 showed that Fe levels in
sediments from all stations were within the
recommended values (41000.00 µgg-1) of unpolluted
marine sediments [17,29]. Mn levels in sediments
from all stations were within the recommended
values (770.00 µgg-1) of unpolluted marine sediments
[29]. Cd levels in sediments from all stations were
higher than the recommended values (0.11 µgg-1) of
unpolluted marine sediments [17,29,20], may be due
to discharges of untreated municipal sewage [21],
from the city of Bandar Abbas. Ni levels in
sediments at stations 1 & 3 were high, but at station 3
exceeded than the high alert levels (HAL: 50 µgg-1)
[33], this may be due to oil pollution [25,19].
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Adv. Environ. Biol., 6(1): 319-326, 2012
500
25
400
20
Cd µgg -1 (d.w.)
Fe µgg-1 (d.w.)
600
300
200
15
10
5
100
0
0
1
2
1
3
2
3
Station
Station
6
5
30
4
Ni µgg -1 (d.w.)
Mn µgg-1 (d.w.)
25
20
15
3
2
10
1
5
0
0
1
2
3
Station
1
2
3
Station
Fig. 3: Fe, Cd, Mn, and Ni contents in soft tissues of T.mutabilis from three sampling stations in the Bandar
Abbas (in µgg-1 d.w.). Lines over the bars indicate 1 SD (n=9).
Table 3: Comparison of detected values (mean ± SD) of metals with recommended values of unpolluted sediments (µgg-1).
Metal
Station 1
Station 2
Station 3
Recommended value
Fe
9420/08 ± 340/08
10717/17± 1052/99
10493/51 ± 294/37
41000.00 *
Cd
1/77± 0/07
1/84± 0/06
1/57± 0/06
0.11 **
Mn
368/44 ± 9/47
417/30± 33/16
400/02± 13/75
770.00 ***
Ni
44/56± 2/30
53/73± 10/89
42/9767± 1/37493
50 ****
* (GESAMP, 1982; Salomons and Froster, 1984).
** (GESAMP, 1982; Salomons and Froster, 1984; IAEA, 1989).
*** (Salomons and Froster, 1984).
**** (USEPA, 1996).
Margalef [23] indicated that biological
communities existing in polluted sites had an upper
growth rate because the low number of species
accomplished of tolerating the most stressful
conditions reduces competition and facilitates
admission to the resources by the adapted organisms.
The larger size of T. mutabilis specimens collected in
the station 2; seem to be in agreement with this
finding.
The highest concentrations belonging to iron and
manganese in the soft tissues of T. mutabilis was
generally seen in marine gastropods, because these
are essential elements incorporated in proteins,
respiratory proteins and enzymes [19,12,9,30].
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Adv. Environ. Biol., 6(1): 319-326, 2012
Cervantes et al. [10] indicated that Hexaplex
trunculus belongs to the family of Muricidae satisfies
all the requirements to be a biomonitor of metal
contamination as they are abundant, sedentary, easy
to identify, and tolerate high concentrations of
metals. T.mutabilis too belongs to the same family
and has similar features of the intertidal zone also (1)
provide sufficient tissue for analysis, (2) the main
positive correlation was found between concentration
of Ni in T.mutabilis and sediments (p < 0.0001, r = 0
.941), and (3) the concentration of Cd in soft tissues
of T.mutabilis was more than its value in sediments,
so it could be used as bioindicator for heavy metals
Cd and Ni.
40
700
y = ‐10.18x + 815.3
R² = 0.085
600
500
r = ‐ 0.292
P = 0.140
400
300
200
Series1
100
Linear (Series1)
Cd in Thais mutabilis (µgg -1 d.w.)
Fe in Thais mutabilis (µgg -1 d.w.)
The highest concentration of Cd in soft tissues of
T.mutabilis specimens was observed at station 1 and
the lowest at station 2. This can be explained by size
of samples, because concentration of Cd in soft
tissues of T.mutabilis specimens was showed strong
negative relationships with total length (p<0.0001, r
= - 0.640).
T.mutabilis specimens at station 1 had lowest
size and at station 2 had upper. According to studies
on aquatic animals, concentration of cadmium
decreases with increasing size, because the
concentration of metals in the younger animals, that
have smaller size, is higher due to higher metabolic
activity [8,9].
0
y = ‐1.173x + 61.57
R² = 0.409
35
30
r = ‐ 0.640**
P = 0.000
25
20
15
Series1
10
Linear (Series1)
5
0
0
20
40
0
60
y = 0.307x + 3.123
R² = 0.015
60
50
r = 0.123
P = 0.541
40
30
Series1
20
Linear (Series1)
10
Ni in Thais mutabilis (µgg -1 d.w.)
70
Mn in Thais mutabilis (µgg -1 d.w.)
20
40
60
Length of Thais mutabilis (mm)
Length of Thais mutabilis (mm)
16
y = 0.069x + 0.233
R² = 0.01
14
12
r = 0.1
P = 0.619
10
8
6
Series1
4
Linear (Series1)
2
0
0
0
20
40
0
60
20
40
60
Length of Thais mutabilis (mm)
Length of Thais mutabilis (mm)
14000
y = ‐2.719x + 11129
R² = 0.206
12000
10000
r = ‐ 0.455
P = 0.219
8000
6000
Series1
4000
Linear (Series1)
2000
0
0
200
400
600
800
Fe in Thais mutabilis (µgg -1 d.w.)
Cd in Sediments ( µgg -1 d.w.)
Fe in Sediments ( µgg -1 d.w.)
Fig. 4: Linear regressions between Fe, Cd, Mn, and Ni contents in soft tissues of T.mutabilis and length.
2
1.8
1.6
1.4
1.2
1
0.8
0.6
0.4
0.2
0
y = 0.001x + 1.717
R² = 0.013
r = 0.116
P = 0.765
Series1
Linear (Series1)
0
10
20
30
Cd in Thais mutabilis ( µgg -1 d.w.)
40
325
70
500
450
400
350
300
250
200
150
100
50
0
y = ‐ 0.707x + 408.8
R² = 0.133
r = ‐ 0.366
P = 0.333
Series1
Linear (Series1)
0
20
40
60
Ni in Sediments ( µgg -1 d.w.)
Mn in Sediments ( µgg -1 d.w.)
Adv. Environ. Biol., 6(1): 319-326, 2012
y = 1.882x + 39.82
R² = 0.884
60
50
r= 0.941**
Sig=0.000
40
30
Series1
20
Linear (Series1)
10
0
80
0
Mn in Thais Mutabilis ( µgg -1 d.w.)
5
10
15
Ni in Thais mutabilis ( µgg-1 d.w.)
Fig. 5: Linear regressions between Fe, Cd, Mn, and Ni contents in soft tissues of T.mutabilis and the contents in
corresponding sediments.
Acknowledgment
8.
M. Astani would like to thank Dr. Musazadeh,
Eng. Moassesi and Eng. Farzin from environmental
Laboratory of the Atomic Energy Organization of
Iran, also all the members of the Persian Gulf and
Oman Sea Ecological Research Institute. Special
thanks to Eng. M.E. Noorian, Eng. Mariam Astani &
E. Roozbahan.
9.
10.
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