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Assessment trace elements concentrations in tissues in Caspian Pond
Turtle (Mauremys caspica) from Golestan province, Iran
Reza Yadollahvand
a,1
, Haji Gholi Kami
b,2
, Abdulreza Mashroofeh
c
,
Alireza Riyahi Bakhtiari
c,
n
a
Department of Marine Biology, Faculty of Marine Sciences, Tarbiat Modares University, PO Box 64414-356, Noor, Mazandaran, Iran
b
Department of Biology, Faculty of Sciences, Golestan University, PO Box 49138-15759, Gorgan, Golestan, Iran
c
Environmental Forensic Laboratory, Department of Environmental Sciences, Faculty of Natural Resource, Tarbiat Modares University, PO Box 64414-356,
Noor, Mazandaran, Iran
article info
Article history:
Received 9 July 2013
Received in revised form
24 December 2013
Accepted 28 December 2013
Keywords:
Caspian Pond Turtle
Mauremys caspica
Different Organs
Trace metals
Iran
abstract
Concentrations of cadmium, lead, zinc, and copper were measured in different organs and tissues of 15
Caspian Pond Turtle (Mauremys caspica) collected from Gharehsu River, Golestan province, Iran in June and
July 2012. Mean concentrations (dry weight) of zinc and copper were 66.9 and 6.7 mgg
1
in liver, 147 and
3.4 mgg
1
in heart, 93.2 and 4.9 mgg
1
in shell, and finally 150.7 and 4.5 mgg
1
in muscle, respectively.
Mean concentrations of cadmium and lead were 5.8 and 32.4 mgg
1
in liver, 2.9 and 20.9 mgg
1
in heart,
3.5 and 21.5 mgg
1
in shell, and finally 2.5 and 27.5 mgg
1
in muscle, respectively. On average, lead,
cadmium, copper and zinc concentrations in the analyzed tissues were much higher than those reported in
otherfreshwaterturtlespecies.Inparticular,themeanconcentrationsofleadinliverandmuscleofCaspian
Pond Turtle was extremely high. To our knowledge, this is the first report into metal accumulation in tissues
and organs of Caspian Pond Turtle from of the Gharehsu River in Golestan province, Iran.
&2014 Elsevier Inc. All rights reserved.
1. Introduction
Metals enter the aquatic environments by atmospheric deposi-
tion, by erosion of the geological matrix due to rain, or from
anthropogenic sources, such as agriculture drainage, municipal,
residential, industrial effluents, and mining wastes (Al-Yousuf et al.,
2000; Mashroofeh et al., 2012). They are a serious threat because of
their high toxicity, long persistence, bioaccumulation, and biomagni-
fication in the food chain (Papagiannis et al., 2004), as well as metals
are causing cytotoxic, mutagenic and carcinogenic effects in animals
(More et al., 2003). Metal toxicity occurs when toxic elements
displace nutrient elements from their metabolic site (Guirlet and
Das, 2012). In addition, they are not biodegradable through bacterial
metabolic pathways in a short period of time. Trace metals such as
cadmium (Cd) and lead (Pb) are non-essential elements to all living
organisms and exhibit toxic effects at low concentrations, whereas
zinc (Zn) and copper (Cu) are biologically essential elements in
organism nutrition and fulfill many biochemical functions in organ-
ism metabolism, and exhibit toxic effects at high concentrations
(Mashroofeh et al., 2012). Both essential and non-essential metals
can be taken up or ingested by aquatic organisms and then
accumulated in their tissues (Anan et al., 2001).
The Mauremys caspica (Gmelin, 1774), belongs to the order
Testudines, suborder Cryptodira, family Geoemydidae and sub-
family Geoemydinae (Rhodin et al., 2010). It is distributed from
central Anatolia east- and southeastwards across Syria and the
Caucasus region to Iraq and Iran; isolated relict populations are
known from Bahrain and adjacent Saudi Arabia (Vamberger et al.,
2013). In Iran the Caspian Pond Turtle, is widely distributed in
Golestan, Mazandaran, Guilan, Ardebil, East and West Azarbaijan,
Kordestan, Kermanshah, Lorestan, Ilam, Khouzestan and Fars
provinces (Kami et al., 2006). Major threats to the survival of
freshwater turtles predominately are anthropogenic, including loss
of nesting habitat, illegal harvest (over-harvest) of eggs and meat,
infectious disease such as Fibropapillomatosis, and serious chemi-
cal pollution (Lutcavage et al., 1997; Spotila et al., 2000; Barreiros
and Barcelos, 2001; Bugoni et al., 2001; Lam et al., 2006). Among
these, pollution and pollution-related diseases seems to be one of
the most significant factors influencing the freshwater turtle
population. Unfortunately, there is no published information on
pollution levels and their effects in freshwater turtle populations
in Iran, particularly the Caspian Pond Turtle.
Turtles are useful as biomonitors of environmental contami-
nants because they are widely distributed, occupy a variety of
habitat
0
s types, feed a wide range of trophic levels, are long-lived,
Contents lists available at ScienceDirect
journal homepage: www.elsevier.com/locate/ecoenv
Ecotoxicology and Environmental Safety
0147-6513/$- see front matter &2014 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.ecoenv.2013.12.028
n
Corresponding author. Fax: þ98 122 6253499.
E-mail addresses: rezayadollahvand.tmu@gmail.com (R. Yadollahvand),
hgkami2000@yahoo.com (H.G. Kami), a.r.mashrofe@gmail.com (A. Mashroofeh),
riahi@modares.ac.ir,ariyahi@gmail.com (A.R. Bakhtiari).
1
Fax: þ98 122 6253499.
2
Fax: þ98 171 2245964.
Ecotoxicology and Environmental Safety 101 (2014) 191–195
allowing for long-term exposure to contaminants and have suffi-
cient tissue mass for multiple endpoint measurements (Meyers‐
Schöne et al., 1993; Kami et al., 2006; Andreani et al., 2008).
In addition, carnivorous species may accumulate greater concen-
trations of hazardous chemicals through trophic transfer, and
some species are relatively sedentary, making them useful for
monitoring contaminants within a specific area (Yu et al., 2011).
The use of biomonitors serves an important function from the
ecotoxicological point of view. This is due to the fact that they
provide integrated measures of the bioavailable metals which are
of ecotoxicological significance in a habitat (Yap et al., 2006).
Despite this, there are only a few studies that focus on the
accumulation of metals and other environmental contaminants
in freshwater turtles.
Knowledge of trace element concentrations in freshwater
turtles is important both with respect to nature management
and human consumption of freshwater turtles. The objectives of
present study were to evaluate the accumulation of Zn, Cu, Pb and
Cd in different tissues and organs from Caspian Pond Turtle from
the Golestan province (Islamic republic of Iran). The study also
compares the distribution of the trace elements in different body
tissues and compares these data with those reported from other
locations.
2. Material and methods
2.1. Sample collection and pretreatment
15 Caspian Pond Turtles were collected from Gharasu River in Golestan province
(Fig. 1), during June and July 2012. The turtles were transported alive to the laboratory,
and kept in a vivarium before analysis. They were dissected with laboratory set, and
different tissues of liver, heart, muscle and shell were quickly removed, washed with
distilled water and stored on 20 1C until chemical analysis. The biological data of the
specimens are shown in Ta ble 1.
2.2. Analysis procedure
The procedure used for measuring trace elements concentrations in turtle
samples has been described previously (Mashroofeh et al., 2013) with minor
modifications. Approximately 1 g of the homogenized powder from each dried
sample was added to 8 ml of concentrated (65 percent) supra-pure HNO
3
(Merck,
Darmstadt, Germany) in a closed cell, polytetrafluoroethylene (Teflon™) lined
digestion vessel and incubated for 1 h at 40 1C in a hot block digester, followed by
heating at 140 1C for 3 h. Then samples were left to cool for half an hour, after
which 2 ml of H
2
SO
4
(Supra-pure (96 percent), Merck, Darmstadt, Germany) was
added, and the beaker was returned to the hot block for another hour for lipid
digestion. Upon cooling, extracts were diluted to 25 ml with ultrapure Milli-Q
quality water. Samples were filtered through Whatman No. 1 filter paper, and then
analyzed. Concentrations of Zn, Cu, Pb and Cd were measured using an atomic
absorption spectrometer (Shimadzu, AA-670, Kyoto, Japan) with an air/acetylene
flame. Quality assurance was assessed for each batch of 20 digested samples by
inclusion of two blanks and reference materials SRM1577b (Bovine liver; National
Institute of Standards and Technology, Gaithersburg, MD, USA) and DORM2
(Dogfish muscle; National Research Council Canada). Recoveries of all elements
ranged from 92.5 percent to 106 percent. In this study, trace elements concentra-
tions are expressed as mgg
1
of tissue on dry weight basis.
2.3. Data analyses
All data were tested for goodness of fit to a normal distribution with Shapiro–
Wilk
0
s test. Data were analyzed using parametric procedures after log
10
transfor-
mation of trace element concentrations. To test the statistical differences of trace
element concentrations among different tissues, Duncan
0
s method, along with one-
way analysis of variance (ANOVA), were carried out using the SPSS version 17 (SPSS
Inc., Chicago, IL, USA). A probability value of less than 0.05 was considered to
indicate statistical significance.
3. Results and discussion
Concentrations of trace elements in different tissues and organs
of Caspian Pond Turtle are shown in Table 2. The analysis has
shown that Zn, Pb, Cu and Cd were detected in all the samples
analyzed. Zinc concentrations were highest among the trace
elements examined, while concentrations of Cd were generally
the lowest in the analyzed tissues and organs of our specimens
(Table 2 and Fig. 2). The comparison of the extent of trace element
accumulation in analyzed tissues showed that the differences in
distribution among different tissues were statistically significant
for all assessed trace elements (po0.05). In general, different
tissues and organs showed different capacities for accumulating
trace elements. Trace element levels were generally low in muscle,
except for Zn which exhibited the highest mean level in this tissue.
Liver displayed the highest Pb, Cd and Cu levels, reaching 32.41,
5.80 and 6.74 mgg
1
dry weight, respectively. Similar distribution
pattern of trace elements has been reported for marine turtle
species as well (Sakai et al., 2000; Maffucci et al., 2005; Storelli
et al., 2005; García-Fernández et al., 2009; Jerez et al., 2010).
The difference in accumulation potential between the four ana-
lyzed tissues can be explained by the activity of metallothioneins,
proteins that are present in liver but not in the muscle and other
tissues and organs, which have the ability to bind certain trace
elements and thus allow the tissue to accumulate them at a high
degree (Barbieri, 2009; Mashroofeh et al., 2013). Metallothioneins
play an important role in trace element homeostasis and in protec-
tion against trace element toxicity (Papagiannis et al., 2004). More-
over, the differences in levels are at least one order of magnitude and
originate from differences in physiological functions of different
tissues and organs (Mashroofeh et al., 2013).
Fig. 1. Map of sampling location of Caspian Pond Turtle in the Gharasu River, Iran.
Table 1
Biometry data of Caspian Pond Turtle from Golestan Province, Iran.
Specimen Sex Size (mm) Weight (g)
1 Male 214.35 1157
2 Male 143.40 351
3 Female 211.66 1265
4 Male 103.09 120
5 Female 153.72 473
6 Male 197.66 878
7 Male 154.56 466
8 Male 166.61 490
9 Male 144.15 348
10 Female 198.12 985
11 Male 233.71 1351
12 Male 166.87 523
13 Female 224.80 1467
14 Male 111.51 174
15 Male 205.47 978
R. Yadollahvand et al. / Ecotoxicology and Environmental Safety 101 (2014) 191–195192
3.1. Comparison of trace elements concentrations in different organs
of Caspian Pond Turtle
Zinc is an essential element for human nutrition and good health
but very high intakes can cause acute adverse effects and health
problems (Mashroofeh et al., 2013). In the present study, mean Zn
concentrations of different tissues varied from 66.89 to 150.67 mgg
1
dry weight in Caspian Pond Turtle and the distribution patterns
concentrations of Zn follows the order: muscle 4heart4shell 4liver
(Table 2). No significant differences were found between muscle and
heart (p40.05). Zinc revealed the highest concentrations in Caspian
Pond Turtle muscle followed by the heart (Fig. 2). Zinc concentrations
in muscle were about two-fold higher than those in the liver. Zinc
had the highest concentration in the muscle, which is in line with
findings of Maffucci et al. (2005) and Gardner et al. (2006),butwhich
differs from findings of other studies, suggesting the liver as the
centre of their accumulation (Torrent et al., 2004; García-Fernández
et al., 2009). Zinc concentrations obtained in the liver were higher
than those reported in the literature (Albers et al., 1986). On the other
hand, the data would seem to indicate that Zn is regulated through
homeostatic processes, maintaining a balance between metabolic
requirements and prevention against toxic effects, which has been
suggested recently by Maffucci et al. (2005).Inthissense,onecould
consider the Zn levels detected to be physiological; and presuming
so, this element is actually not a problem on the health status of
these Caspian Pond Turtles.
Copper is an essential element but toxic for turtles above thresh-
old concentrations (Franzellitti et al., 2004). Copper mean concentra-
tions of different tissues varied from 3.37 to 6.74 mgg
1
dry weight
in Caspian Pond Turtle. The accumulation patterns of lead following
the sequence: liver4shell 4muscle4heart (Table 2). No significant
differences were found between muscle, shell and heart (p40.05).
The highest concentrations of Cu was found in the liver (po0.05),
whichisinlinewithpreviousfindings of Xu et al. (2006) and Storelli
et al. (2005). Nevertheless, it reached about 1.4 to 2-times higher
concentrations than it is in other tissues and organs. Copper
concentrations in liver tissue in our study is lower than the
concentrations found in liver tissue of Trachemy scripta elegans
(Yu et al., 2011), but the Cu concentrations in the muscle tissue is
higher than the levels reported (Yu et al. , 2011). Unfortunately, the Cu
concentrations in the heart and shell did not measure. High Cu levels
in freshwater turtles, including the Caspian Pond Turtle of the
present study, are likely to have arisen from species-specificbioac-
cumulation, and unlikely to reflect pollution or higher natural back-
grounds of Cu in their habitats. As an essential element, Cu is a
component of some enzymes and may play an important role in
immunefunction (Yu et al., 2011). However, little is known about the
effect of Cu on immunity in wildlife, and further studies are
recommended to determine the role of Cu in the immune function
of turtles and other reptiles (Yu et al., 2011).
Cadmium is a nonessential element to all living organisms, and
it has several toxic effects including suppression of the immune
system (Bishop et al., 2010; Okocha and Adedeji, 2011). The Cd
concentrations in Caspian Pond Turtle were found to be in ranged
of 2.51–5.80 mgg
1
dry weight, and the distribution patterns of Cd
concentrations follows the sequence: liver4shell 4heart4mus-
cle (Table 2). Cadmium concentrations in various tissues of the
Caspian Pond Turtle were significantly different (po0.05). Cad-
mium revealed the highest concentrations in Caspian Pond Turtle
liver (Fig. 2). Cadmium concentrations in liver were approximately
two-fold higher than those in the muscle and heart. However, the
average concentrations of Cd in liver of Caspian Pond Turtle from
Golestan province were high compared to previously reports for
freshwater turtle tissues (Albers et al., 1986). Elevated Cd concen-
trations in Caspian Pond Turtle are worrying, especially consider-
ing the fact that it could be one of the most toxic metals, even at
relatively low concentrations (Rie et al., 2001). Accumulation of Cd
in living organisms is a major ecological concern, especially
because of its ability of fast accumulation and slow process of
cadmium excretion from living organisms (Rie et al., 2001).
Lead is one of the most ubiquitous of toxic metals and has no
known biological necessity; at high levels it is lethal for most living
organisms (Goyer, 1993; Bishop et al., 2010). Lead mean concentra-
tions ranged from 20.86 to 32.14 mgg
1
dry weight in Caspian Pond
Turtle. The distribution patterns of lead were following the sequence:
liver4muscle4shell4heart (Table 2). The concentrations of Pb in
different tissues of the Caspian Pond Turtle were significantly
different (po0.05). Lead concentrations in liver were about 1.5-fold
higher than those in other tissues and organs (Fig. 2). In general, the
Pb concentrations obtained in the analyzed tissues were higher than
those reported previously (Albers et al., 1986; Overmann and
Krajicek. 1995; Bishop et al., 2010; Yu et al., 2011). The maximum
Pb concentrations was observed inliverandshellofCaspianPond
Turtle, reaching 46.59 and 34.75 mgg
1
dry weight, respectively.
Elevated Pb levels in the Caspian Pond Turtle are worrying, especially
considering the fact that it could be one of environmental contami-
nants which can promote serious damage to species health (Bishop
et al., 2010). The majority of the Pb burden existed in bones (Sakai
et al., 2000). In the body, 95 percent of Pb is sequestered in bone as in
soluble phosphates with an expected half-life of 20–30 years
(Baldwin and Marshall, 1999). Accumulation of Pb brings about a
multitude of effects in animal skeletal systems (Pounds et al., 1991).
These effects include disruption of bone development, formation and
resorption, as well as interference with the function of bone–cell
hormones. Lead also reduces levels of the hormonal form of vitamin
Table 2
Concentration (μgg
1
dry weight) of metals in different organs of Caspian Pond
Turtle.
Tissues Zinc Cadmium Lead Copper
Liver Mean7S.D. 66.89 722.59 5.8072.32 32.41 76.22 6.7473.89
Median 59.96 6.79 30.56 6.10
Min–max 40.75–120.83 2.48–8.96 26.49–46.59 1.82–13.15
Heart Mean7S.D. 147.02756.56 2.9870.30 20.86 74.16 3.3770.84
Median 159.63 2.96 22.29 3.26
Min–max 19.93–217.04 2.54–3.57 11.74–27.02 2.15–4.99
Muscle Mean7S.D. 150.67735.49 2.5170.24 27.4573.69 4.50 71.09
Median 156.98 2.53 25.99 4.33
Min–max 77.32–188.05 2.17–3.04 20.87–32.93 3.13–7.4 8
Shell Mean7S.D. 93.23 732.34 3.5471.06 21.5477.15 4.8671.82
Median 94.27 3.83 24.65 5.15
Min–max 3.23–126.86 0.82–4.65 8.11–34.75 1.05–7.87
Fig. 2. Comparison of trace element concentrations in different tissues and organs
of Caspian Pond Turtle. Concentrations with different letters are significantly
different (po0.05, Duncan
0
s method, along with one-way ANOVA). Each point
and bar indicates the mean and standard deviation (S.D.), respectively.
R. Yadollahvand et al. / Ecotoxicology and Environmental Safety 101 (2014) 191–195 193
D (1,25-dihydroxyvitamin-D), which is necessary in the regulation of
serum calcium and phosphorous levels, and controls bone growth
and mineralization (Fullmer, 1997; Goyer, 1993; Pounds et al., 1991).
It has been demonstrated that bioavailability and toxicity of Zn,
Cu, Cd and Pb in aquatic organisms depend on the total concen-
tration of each metal in the water (Papagiannis et al., 2004).
Concentrations of persistent toxic substances in different tissues
and organs reflect discharges of these substances into receiving
aquatic environments, bioaccumulation through the food web, and
chemical partitioning and kinetics in the turtles. Many researchers
indicated that different marine and freshwater turtle species from
the same area contained different trace elements levels in their
tissues (Storelli and Marcotrigiano, 2003; Maffucci et al., 2005;
Barbieri, 2009; García-Fernández et al., 2009; Jerez et al., 2010).
Trace element bioaccumulation of turtles is species-dependent
(Sakai et al., 2000). Further, concentrations of metals in tissues and
organs of turtles depend upon many different factors including
body size, biotransformation and excretion, organismal trophic
position and physiological adaptations (Rainbow, 2002; Luoma
and Rainbow, 2005). Therefore, exposure and accumulation can
vary greatly across geographical areas and among species, espe-
cially between taxa with different foraging behaviors and life
histories (Luoma and Rainbow, 2005).
4. Conclusions
This study determined the trace element concentrations in
different tissues and organs of the Caspian Pond Turtle for the first
time. Trace elements are taken up through different organs of the
turtle because of the affinity between them. In this process, many
of these metals are concentrating at different levels in different
tissues and organs at the turtle body. Among the metal contami-
nants, high concentrations of Cd, Cu and Pb were found in Caspian
Pond Turtle liver, Therefore, liver in this species does serve as an
indicator for this elements whereas the high accumulation of Zn in
Caspian Pond Turtle muscle was remarkable and muscle can be an
suitable indicator for Zn. Concentrations of Cd, Zn, Cu and Pb in
most tissues of the Turtle, measured in the current study, were
generally high and do appear to have adverse effects on turtles
inhabiting rivers. In addition, serious contamination of Caspian
Pond Turtle by organochlorine and metallothionein compounds
was recently reported (Alam and Brim, 2000; Gardner et al., 2003;
Andreani et al., 2008). Thus, further studies are needed to reveal
the possible adverse effects of harmful substances on turtles, as
part of restoration programs of the freshwater turtle populations.
Acknowledgments
We thank Mrs. Okhli and Mr. Boroughani from Golestan
University for their help in sample collection. We are grateful to
our laboratory staff at the Tarbiat Modares University including
Mrs. Afshar and Mrs. Haghdoost.
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