Mercury, lead, and cadmium in tissues of the Caspian Pond Turtle (Mauremys caspica) from the southern basin of Caspian Sea

Abstract

Concentrations of cadmium, lead, and mercury were measured in different tissues (liver, muscle, and shell) of 60 Caspian Pond Turtles collected from Tajan and Shiroud Rivers, southern basin of the Caspian Sea. Based on the results, different tissues showed different capacities for accumulating trace elements. The general trend of metals accumulation was: liver > shell > muscle. Results also showed that accumulation of these elements was not significantly different between sex and river in turtles (p > 0.05). Based on the results, Hg and Pb concentrations recorded in the present study were higher than some of the maximum concentration permissible. To our knowledge, this is the first report into heavy metal accumulation in tissues and organs of Caspian Pond Turtle from the southern basin of Caspian Sea. Further studies are needed to measure different heavy metals and trace metals in this valuable species.

Full text

FATE AND EFFECT OF POLLUTANTS IN RIVERS: FROM ANALYSIS TO MODELLING
Mercury, lead, and cadmium in tissues of the Caspian Pond Turtle
(Mauremys caspica) from the southern basin of Caspian Sea
Milad Adel
1
&Hasan Nasrollahzadeh Saravi
2
&Maryam Dadar
3
&Leila Niyazi
4
&
Cesar P. Ley-Quinonez
5
Received: 7 June 2015 /Accepted: 30 November 2015
#Springer-Verlag Berlin Heidelberg 2015
Abstract Concentrations of cadmium, lead, and mercury
were measured in different tissues (liver, muscle, and shell)
of 60 Caspian Pond Turtles collected from Tajan and Shiroud
Rivers, southern basin of the Caspian Sea. Based on the re-
sults, different tissues showed different capacities for accumu-
lating trace elements. The general trend of metals accumula-
tion was: liver> shell>muscle. Results also showed that accu-
mulation of these elements was not significantly different be-
tween sex and river in turtles (p> 0.05). Based on the results,
Hg and Pb concentrations recorded in the present study were
higher than some of the maximum concentration permissible.
To our knowledge, this is the first report into heavy metal
accumulation in tissues and organs of Caspian Pond Turtle
from the southern basin of Caspian Sea. Further studies are
needed to measure different heavy metals and trace metals in
this valuable species.
Keyword Caspian Pond Turtle .Mauremys caspica .Heavy
metal .Tissues .Sex .Caspian Sea
Introduction
Heavy metals are accumulated in environment by different
ways, e.g., extraction, diffusion, combustion, and industrial
activities, and then enter in the aquatic environment by dis-
charge of domestic, industrial, agricultural waste water, acci-
dental leakage, Ballast water discharges by ships and soil ero-
sion (Bahnasawy et al. 2009;Javed2005). These metals can
be strongly accumulated along water and aquatic food chains,
thus resulting in sub lethal effects or death in local fish popu-
lations and finally in human (Perez-Lopez et al. 2008). Study
of some heavy metals, such as cadmium, mercury, and lead
are so important due to their toxicity and bio accumulative
behavior in aquatic organisms and even in human food chains
(Kalantzi et al. 2013). Aquatic species diversity and equilibri-
um of ecological consumers can be modified by the effects of
heavy metals. Aquatic organisms such as fish and turtles cause
biomagnification by accumulate metals as Hg to high concen-
trations than those in water and prey organisms. Selection of
biological components such as sea turtles or birds for wide
distribution and high position in the food chain can be useful
as bioindicator in health monitoring and predict future chang-
es in the environment (Kim et al. 2007).
The Caspian turtle (Mauremys caspica) is a species of tur-
tles in the family Geoemydidae, living in the eastern
Mediterranean region from northwestern of Saudi Arabia,
Iraq, Bahrain, Turkey, Caucasus, Tbilisi to northern, central,
and south western part of Iran (Vamberger et al. 2013). This
species is widely dispersed in different provinces of Iran, e.g.,
Mazandaran, Golestan, Guilan, Ardabil, Azerbaijan,
Kurdistan, Fars, and Khuzestan (Iverson 1994). There have
been many reports of this species in Tajan and Shiroud Rivers.
The effects of heavy metals and other contaminants in Caspian
Sea fishes have been previously documented (Nasrollahzadeh
Saravi et al. 2013), but with the given available data, only one
Responsible editor: Philippe Garrigues
*Milad Adel
miladadel85@yahoo.com
1
Department of Aquatic Animal Health and Diseases, Iranian
Fisheries Research Center, Tehran, Iran
2
Department of Environmental Science and Policy, Caspian Sea
Ecology Research Center, Sari, Iran
3
Center of Biotechnology and Biology Research, Shahid Chamran
University, Ahvaz, Iran
4
Department of Marine Chemistry, Mazandaran University,
Babolsar, Mazandaran, Iran
5
Servicios de Salud de Sinaloa, Culiacán, Mexico
Environ Sci Pollut Res
DOI 10.1007/s11356-015-5905-5

study was done by Yadollahvand et al. (2014) on different
tissues of Caspian turtle in Golestan province. On the other
hand, Tajan and Shiroud were selected as locations which had
agriculture and industrial activity and pesticides such as or-
ganophosphates (cinosulfuron, triadimenol, phosphamidon,
and tricyclazole). However, despite the importance of biodi-
versity and high frequency of this valuable species, few stud-
ieshavebeendoneonitinMazandaranprovince.Therefore,
this study is not only to measure and compare lead (Pb), mer-
cury (Hg), and cadmium (Cd) in different tissues of both sexes
Caspian turtle in Tajan and Shiroud Rivers but also is a com-
plementary study on this species in other rivers of the Caspian
Sea basin.
Material and methods
Sixty adult Caspian Pond Turtles were collected from Tajan
and Shiroud River in Mazandaran province (Fig. 1), during
September and October 2014 in the rainy season. Their feed-
ing habit includes water plants, mollusks, crustaceans, small
amphibians, and small fish. Permission to collect of Caspian
Pond Turtle was authorized by the Iran Department of
Environment (Permission Number: 1184-N/14/2; 2014; 22th
September). The Tajan River is one of the most important
river, has a watershed of 1.80 million km
2
(36° 43′36″N
and 53° 7′36″E). Shiroud River is located in the distance of
8 km from Tonekabon and 15 km from west part of Ramsar at
Mazandaran province (44° 50′36″Nand45°2′36″E).
The turtles were transported alive to the central laboratory
of Caspian Sea Ecology Research Center, and their size in
curved carapace length (CCL in cm) and weight (g) were
measured. They were euthanasia by 200 mg/kg of ketamine
hydrochloride (5 %) and 3 mg/kg of diazepam (5 %) before
analysis and were dissected with laboratory set, and different
tissues of liver, muscle, and shell were quickly removed,
washed with distilled water, and refrigerated at −20 °C until
chemical analysis (Yadollahvand et al. 2014). All the labora-
tory materials used were completely acid-washed to prevent
contamination of samples (Paez-Osuna et al. 2010).
The procedure used for measuring trace elements concen-
trations in turtle samples has been described previously
(Yadollahvand et al. 2014) with minor modifications. All sam-
ples were dried by oven and homogenized using blender.
Approximately 0.3 g of the homogenized powder of dried
sample was added to 4 ml of concentrated (%65) ultra pure
HNO
3
(Merck, Darmstadt, Germany) in a closed cell,
polytetrafluoroethylene (Teflon™) lined digestion vessel and
incubated for 1 h at 40 °C, followed by heating at 140 °C for
3 h. For mercury digestion, the sample was added to 45 mg
V
2
O
5
. Then, they were diluted to 50 ml with 20 ml distilled
water and K
2
Cr
2
O
7
(%2). Samples were filtered through
Whatman No. 1 filter paper and then analyzed.
Concentrations of Cd and Pb by graphite furnace and Hg
using vapor generation were measured using an atomic ab-
sorption spectrometer (Thermo M5, Japan). Quality assurance
was assessed for each batch of 20 digested samples by inclu-
sion of two blanks and reference materials (RM) TORT-2.
Calibration curves were made for the spectrophotometer using
SIGMA 3000 (Perkin Elmer). The limit of detection (LOD)
for Pb, Cd, and Hg were 0.70, 0.33, and 0.39 ppb, respective-
ly. To rule out possible contamination, weight samples were
used with deionized water. To determine the percentage of
recovery and evaporation during the digestion process, repli-
cates were used of the reference material (RM) TORT-2.
Recovery of RM (TORT-2) and standard repetition added with
Fig. 1 Sampling sites of Tajan
(a)andShiroud(b) Rivers (north
of Iran), Mazandaran Province
(Caspian Sea basin)
Environ Sci Pollut Res

SIGMA 3000, and the percentage of recovery was between 87
and 95 %. The coefficient of variation on replicate, spiked
samples ranged up to 10 %. Concentrations of trace elements
are expressed as mg kg
−1
of tissue on dry weight basis.
Reported statistics are arithmetic means and standard devi-
ation (SD). All data obtained from the two sampling sites were
used for statistical analyses using SPSS 18.0 Software. One-
way analysis of variance (ANOVA) along with Duncan’s
method was carried out to examine mean differences among
the tissues. In this study, pvalues of ≤0.05 were used to de-
termine significant differences. The correlations among the
different heavy metals in tissues were determined using a sim-
ple regression model R
2
<50 % used as a statistical indicator.
Arithmetic means is given to facilitate comparisons with other
studies.
Results
The turtles biometric characteristics captured are shown in
Table 1. No statistical differences were observed in size or
weight by sex or among rivers specimens. The specimens
captured can be considered sub-adult by the size.
The heavy metals concentration in various tissues of
Caspian Pond Turtle from the Tajan and Shiroud Rivers are
presented in Table 2. The results showed that metals concen-
trations were statistically different among tissues of Caspian
Pond Turtles (Pb: F
(2, 57)
=68.1, p=0.001; Cd: F
(2, 57)
=87.3,
p=0.001; Hg: F
(2, 57)
=116.4, p= 0.001). Pb concentrations
were highest among the trace elements examined, while con-
centrations of Hg were generally lowest in analyzed tissues
(Table 2). The trend of metals accumulation was liver>shell>
muscle (Table 2). Metal concentrations were generally low in
muscle, except for Hg which exhibited the highest mean level
than shell. The Duncan’s results showed three different groups
for all tissues (Table 2). In the present study, mean Pb concen-
trations in different tissues varied from 21.88±1.27 to 35.46±
1.90 mg kg
−1
dry weight in Caspian Pond Turtle, and the
distribution patterns of Pb concentration follows the order:
Pb
liver
>Pb
shell
>Pb
muscle
(pvalue=0.008). Statistical differ-
ences were observed in Pb concentration between the three
tissues. Mean concentration of Cd and Hg varied from 4.82±
2.82 to 2.10±0.10 and 2.79± 0.19 to 0.95±0.04 mg kg
−1
dry
weight, respectively. The accumulation patterns of Cd and Hg
following these sequences: Cd
liver
>Cd
shell
>Cd
muscle
(pval-
ue=0.003) and Hg
liver
>Hg
muscle
>Hg
shell
(pvalue=0.024)
(Table 2). Results showed that accumulation of these elements
was not statistically different among sex or river population in
turtles (p>0.05). Pearson correlation shows that Pb, Cd, and
Table 1 Biometry data of Caspian pond Turtle from the Tajan and
Shiroud Rivers in Mazandaran province Iran
River Sex CCL (cm) Weight (g) Age (year)
Shiroud Male 11.3±3.8 277.3±14.2 3± 1
Female 10.84±2.6 271.8±10.6 3± 1
Statistical test p=0.126 p=0.108 p=0.324
Tajan Male 11.5±4.1 285.3±13.9 3± 1
Female 10.9±3.5 276.8± 10.4 3± 1
Statistical test p=0.365 p=0.282 p=0.337
The statistical test used is the analysis of variance (ANOVA); statistical
test data as mean±SD followed by Duncan’s test in parentheses, if sig-
nificant differences were found. Data are presented as mean±SD. Values
in each row with different superscripts show significant difference
(p<0.05)
Table 2 Mean concentration
(±SD) of heavy metals (mg/kg
dry weight) in liver, shell, and
muscle of Caspian Pond Turtle
from the southern basin of
Caspian Sea
River Sex Tissues Pb Cd Hg
Shiroud Male Liver 35.46±1.90 (a) 4.29±0.19 (a) 2.70± 0.13 (a)
Shell 29.32±0.66 (b) 3.3±0.11 (b) 1.04±0.06 (b)
Muscle 23.82±1.12 (c) 2.10± 0.10 (c) 1.63± .0.11 (c)
Statistical test p=0.006 p=0.009 p=0.032
Female Liver 35.34± 2.05 (a) 4.82± 2.82 (a) 2.78± 0.18 (a)
Shell 29.7±1.35 (b) 3.4±0.16 (b) 1.05±0.08 (b)
Muscle 22.12±1.57 (c) 2.29± 0.19 (c) 1.66± 0.14 (c)
Statistical test p=0.005 p=0.003 p=0.021
Tajan Male Liver 32.96±1.42 (a) 4.00±0.29 (a) 2.68± 0.17 (a)
Shell 28.8±1.32 (b) 3.43± 0.12 (b) 0.95± 0.04 (b)
Muscle 24.28±1.17 (c) 2.13± 0.11 (c) 1.57± 0.07 (c)
Statistical test p=0.008 p=0.024 p=0.018
Female Liver 35.34± 1.34 (a) 3.87± 0.13 (a) 2.79± 0.19 (a)
Shell 28.1±1.02 (b) 3.36± 0.13 (b) 1.08± 0.09 (b)
Muscle 21.88±1.27 (c) 2.19± 0.15 (c) 1.61± 0.08 (c)
Statistical test p=0.003 p=0.043 p=0.006
Environ Sci Pollut Res

Hg were not significantly correlated with by sex and rivers in
length and weight (Table 3)(R
2
<0.50; p>0.05). No correla-
tions were found in metals concentrations with size or weight
(R
2
<0.50; p>0.05).
Discussion
Pb concentrations reported in Caspian Pond Turtle tissues in
this study present high concentrations that other metals, par-
ticularly in liver and previously reports for fresh water turtles
(Overmann and Krajicek 1995;Bishopetal.2010;Yuetal.
2011; Yadollahvand et al. 2014). Yadollahvand et al. (2014)
mention that elevated Pb levels in the Caspian Pond Turtle are
worrying, especially considering the fact that this toxic metal
could produce serious damage to species health, including
infertile eggs, and changes in behavior, growth, and survival
of turtles (Zavala-Norzagaray et al. 2014).
The Hg concentrations in liver were 1.4–3.6 times higher
than those reported in the Kemp’s ridley turtles, Lepidochelys
kempii (Innis et al. 2008), Chelonia mydas (Bezerra et al.
2014) Leatherback sea turtles, Dermochelys coriacea
(Davenport and Wrench 1990;Perraultetal.2013)and
Loggerhead turtle, Caretta caretta (Caurant et al. 1999).
High contamination levels of Hg may be related to the high
frequency of fish-based diets (Zavala-Norzagaray et al. 2014).
Hopkins et al. (2013) observed a negative correlation among
Hg levels with reproduction season in the common snapping
turtle (Chelydra serpentina) and increased the egg infertility
and embryonic mortality. Also, Matson et al. (2005) mention
that high level of Hg causes chromosomal damage in Emys
orbicularis and M. caspica inhabiting contaminated sites in
Azerbaijan (west of Caspian Sea). The Hg concentration
found in the muscle tissue of Caspian Pond Turtle (1.65±
0.12) was 1.8–4.2 time higher than those measured in the
other sea turtles such as: Dermochelys coriacea (Perrault
et al. 2013), Caretta caretta (Storelli et al. 1998)and
Stenella coeruleoalba (Storelli et al. 1998). High Hg concen-
tration in muscle found in this study could be accumulated in
human brain, liver, and kidney and cause nose irritation, skin
burns, irritation of respiratory system, rashes, muscle coordi-
nation, and severe diseases such as acrodynia, Hunter-Russell
syndrome, and Minamata disease (Tan et al. 2009; Rajeswari
and Sailaja 2014).
Highest Cd levels were observed in of Caspian Pond Turtle
liver; these results are similar than previously observed by
Yadollahvand et al. (2014) and higher than those previously
reported in liver of green and olive ridley turtles (Gardner et al.
2006) and Lepidochelys olivacea (Paez-Osuna et al. 2010)
(Table 4). Kitana and Callard (2008) mentioned that high level
of Cd reduced proliferation and delay migration of germ cells
to genital ridge, finally affect on gonadal developmental pro-
cesses, and threat the reproductive success of freshwater tur-
tles (Trachemys s cripta,Chrysemys picta).
Certain factors such as body requirements of marine organ-
isms for copper and zinc, excretion of cadmium, lead and
mercury, and the other changes could play an important role
in heavy metals accumulation in the living organisms (Filazi
et al. 2003). Yadollahvand et al. (2014) published that accu-
mulation of these elements was not statistically different
among sex, which was confirmed in this study. This shows
that the metal accumulation is similar in the whole Caspian
Pond Turtle populations in our study area; however, more
studies about the relation among heavy metal concentrations
and the turtles’age are necessary and have all essential infor-
mation about whether factors such as age, weight, and size
influence on processes of turtle pollution.
Our results indicated that the highest concentration of all
metals is found in liver, which is a major tissue of short-term
storage in turtles (Thomas et al. 1994; Rie et al. 2001). This is
in accordance with previous publications on heavy metals
accumulation in Caspian Pond Turtle (Yadollahvand et al.
2014), Chelonia mydas (Lam et al. 2004)andCaretta caretta
(Sakai et al. 2000). Storelli et al. (2008) studied some heavy
metals in Chelonia mydas; the results showed that Cd concen-
trations in muscle were about two fold higher than those in the
liver. In this study, Cd had the higher concentration in the liver
than muscle, suggesting the liver as the center of their accu-
mulation (Torrent et al. 2004; García-Fernández et al. 2009).
The difference in accumulation potential between tissues can
be justified by the activity of metallothioneins, proteins that
are created in liver and present in the muscle and other tissues,
Table 3 Pearson correlation of heavy metals at different sex and rivers
in Caspian Pond Turtle from the southern basin of Caspian Sea
Heavy metals Rivers/sex Pb Cd Hg
Pb Male 1 r=0.755
a
r=0.418
b
Cd 1
Hg 1
Pb Female 1 r=0.783
a
r=0.385
b
Cd 1 r=0.442
b
Hg 1
Pb Tajan 1 r=0.792
a
Cd 1 r=0.526
a
Hg 1
Pb Shiroud 1 r=0.721
a
r=0.431
b
Cd 1
Hg 1
Pb Total 1 r=0.764
a
r=0.388
a
Cd 1 r=0.386
a
Hg 1
a
Correlation is significant at the 0.01 level (2-tailed)
b
Correlation is significant at the 0.05 level (2-tailed)
Environ Sci Pollut Res

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). Moreover, the differences in
levels are the results of polluted water, sediments and foods,
age, weight, body width and length, sex, and differences in
physiological functions of different tissues and organs and
physicochemical characteristics of water (temperature, hard-
ness, and salinity) (Mashroofeh et al. 2013). This result of this
study showed that there were no statistical differences in metal
levels as a function of gender, rivers, size, and weight (R
2
<
0.50; p>0.05). Therefore, gender, rivers, size, and weight do
not play an important role to accumulation of these three toxic
heavy metals in Caspian Pond Turtle. On the other hand, other
aforementioned factors are most important to accumulate of
Pb, Cd, and Hg.
In our study, Hg had the lowest concentration among other
heavy metals which is in line with findings of Ley-Quinoez
et al. (2011) on loggerhead turtles (Caretta caretta)and
Bezerra et al. (2012) on green turtle (Chelonia mydas). Low
accumulation of Hg in the tissues is directly related to nour-
ishment and bioaccumulation capacity of this precious speci-
men (Malik et al. 2013). The Cd emission in rivers are mainly
due to the production and use of artificialphosphate fertilizers,
mineral phosphate, zinc production processes, and manure
manufacturing industries are the most significant emission of
cadmium sources (Bonomelli et al. 2003). In the current study,
the accumulation of Cd in different tissues followed this pat-
tern: liver>shell >muscle, which was in accordance with find-
ings of Yadollahvand et al. (2014). but which differs from
findings of Malik et al. (2013) on soft-shell turtle
(Aspideretes gangeticus).Some of these activities are carried
out in the river of our study area, and these factors could
increase the Cd accumulation in Caspian Pond Turtles.
Hg and Pb concentrations recorded in the present study
were higher than the acceptable values for designated by stan-
dards which is the consequence of Mazandaran wood and
paper industry, Antibiotic Company, Municipal and village
sewage, Cattle and Poultry Industries, Pasteurized milk facto-
ry, MDF Factories, Fisheries Farms, and agricultural activities
(Hosseini et al. 2011).
The heavy metal concentrations present in Caspian Pond
Turtle could be considered a risk, not only for this species but
also for others organisms that develop in the region, including
humans. Aguirre and Tabor (2004)establishedtheuse“senti-
nels”species, are species that serve as indicators of their en-
vironment. In this case, like the sea turtle, maybe our turtle
species can serve as sentinels for the quality of health of
aquatics ecosystems, and make contributions to the environ-
mental authorities, who should also monitor the health of hu-
man society and make good solutions to reduce the disposal of
industrial and toxic waste water to watershed of Caspian Sea
and prevent the accumulation of heavy metals in coastal areas.
To our knowledge, this is the first report about heavy metal
accumulation in tissues and organs of Caspian Pond Turtle
from two rivers of southern basin of Caspian Sea. Further
studies are needed to measure different heavy metal concen-
trations and blood parameter to establish the health risk in the
populations of this species.
Table 4 Concentrations (μgg
_1
dry weight) of heavy metals in
liver, shell, and muscle of sea
turtles
River Author Tissues Pb Cd Hg
Mauremys caspica Current study Liver 35.46±1.90 4.55±1.32 2.74±0.15
Shell 29.5±1.82 3.35±0.12 1.04 ±0.08
Muscle 23.06±1.06 2.2±0.14 1.65±.0.12
M. caspica Yadollahvand et al. (2014) Liver 32.41±6.22 4.29± 0.19 NA
Shell 21.54±7.15 3.54±1.06 NA
Muscle 27.45±3.69 2.51± 0.24 NA
Dermochelys
coriacea
Perrault et al. (2013) Liver NA NA 2.11 ±0.38
Shell NA NA 0.45±0.06
Muscle NA NA 0.83±.0.18
Aspideretes
gangeticus
Malik et al. (2013) Liver 1.93± 0.32 1.93±0.32 NA
Shell 0.98±0.19 0.85±0.03 NA
Muscle 1.23±1.40 0.23±0.03 NA
Caretta caretta García-Fernández et al.
(2009)
Liver 0.69±0.08 5.85±0.14 NA
Shell NA NA NA
Muscle 0.06±0.02 0.04±0.01 NA
Lepidochelys olivacea Gardner et al. (2006) Liver 3.32± 0.30 3.28±0.22 NA
Shell NA NA NA
Muscle 0.01±0.001 3.1± 2.4 NA
Environ Sci Pollut Res

Acknowledgments This study was supported by Caspian Sea Ecology
Research Center and Chamran University. The authors wish to thank Mr.
Ahmad Nosrati Movafagh for his kind assistance.
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