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��ࡱ�>��	������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������bjbj���������AW,�������f	f	�����4�������hHL�d�lN�����������L�L�L�L�L�L�L$P��Rd�LY�������L�����&N�)�)�)�&�����L�)��L�)�)6�>�GA�������3p�����'"�?�L<N0lN�?�T�'�T8GAT�GAL�vT�)[D�����L�L�(���lN������������������������������������������������������������������������T���������f	r:Title: Effects of Gender and Season on Potentially Toxic Metal Levels in Muscles of Adult Blue Swimmer Crabs (Portunus pelagicus) from the Northeastern Mediterranean Sea


Running title: Metal levels in Blue Swimmer Crab


Author: Deniz AYAS*
aDepartment of Seafood Processing Technology, Faculty of Fisheries, Mersin University, Mersin, Turkey

*Correspondence should be addressed to:
Dr. Deniz AYAS
Department of Seafood Processing Technology, 
Faculty of Fisheries, University of Mersin,
33160, Mersin, Turkey. 
Tel: (90) 324 3412813 Ext:1324
Fax: (90) 324 3413025
E-mail: ayasdeniz@mersin.edu.tr




ABSTRACT 
The effects of gender and season on potentially toxic metal levels in 2 muscle types (lump crabmeat, LCM, and chela crabmeat, CCM) of adult blue swimmer crabs, Portunus pelagicus, caught in Mersin Bay, northeastern Mediterranean Sea, were investigated. The annual ranges of metal levels in the LCM of blue swimmer crabs were: 0.50-1.01 mg Cd kg-1, 0.37-0.45 mg Cr kg-1, 0.10-0.40 mg Pb kg-1, 9.64-33.85 mg Cu kg-1, 37.80-78.16 mg Zn kg-1, and 9.35-25.51 mg Fe kg-1. The annual ranges of metal levels in the CCM of blue swimmer crabs were: 0.63-1.47 mg Cd kg-1, 0.31-0.53 mg Cr kg-1, 0.12-0.52 mg Pb kg-1, 25.13-72.50 mg Cu kg-1, 89.85-178.61 mg Zn kg-1, and 7.31-20.08 mg Fe kg-1. Cu and Zn levels in CCM of blue swimmer crabs were higher than in LCM (p <0.05). Cu and Zn specifically accumulated in CCM. In addition, metals such as Cu, Zn, and Fe showed seasonal variations. 

Keywords: Blue Swimmer Crab, Portunus pelagicus, Season, Gender, Metal Contamination












INTRODUCTION 
Blue swimmer crab, Portunus pelagicus, is an exotic species of Indio-Pacific origin. This species passed to the Mediterranean Sea with the opening of the Suez Canal. Today, they are particularly distributed along the Northeastern Mediterranean coast. 
Blue swimmer crab is one of the economically important big sea crabs, and they are caught for consumption around the world and in Turkey, where 55 and 95 metric tons of blue swimmer crabs were caught in 2003 and 2007, respectively, (Anonymous, 2010).
Mersin Bay is densely populated with over one million people living around the bay area and considerable agricultural and industrial activities are carried out there.  Mersin Port is one of the largest ports in Turkey. Many petrochemical facilities are located in the bay as well. Fertilizers and pesticides are heavily used in the agricultural fields in the bay area. Domestic, industrial, and agricultural pollutants are carried into the bay through the rivers in the region. 
Mersin Bay is an area where the fishing is intensive and it is important to determine the pollution in all species caught in Mersin Bay, particularly, given that invertebrate species have weak detoxification mechanisms. A small number of studies have been carried out on the heavy metal accumulation of invertebrate species in Mersin Bay (Ayas et al. 2009, Ayas and Ozogul 2011a,b). Metal accumulation in the crabs may vary with season, gender, size, sexual maturation, and muscle type. Thus, the objective of this study was to compare and determine the seasonal and gender effects on the metal levels of different muscle tissues of mature blue swimmer crabs harvested from Mersin Bay.




MATERIALS AND METHODS 
Materials
Blue swimmer crabs, Portunus pelagicus, were caught by dip net from Mersin Bay on the coast of the northeastern Mediterranean Sea. The samplings were done in April (spring), July (summer), October (autumn), and December (winter). In the fishing procedure, a dip net with mesh size of 32 mm was used. In each season, 40 male and 40 female crabs were caught and kept in polystyrene boxes with ice. When they were brought to the laboratory, they were no longer alive. Molting of crabs was observed in October-November, and the crabs caught in these months were semisoft shell crabs.
Sample preparation
Some morphometric measurements, carapace length (CL), carapace width (CW), and weight of all samples were done (Table 1). The morphometric measurements of crab carapace were done using calipers. After that, the muscle tissues from 40 individuals of each sex were taken out by hand. All assays were conducted on triplicate samples of the homogenates. 
Metal analysis
The metal analyses were made according to Canl1 and Atl1 (2003) with some modifications. The LCM and CCM samples (0.5 g dry weight each) used for metal analysis were dried at 105 �C to reach constant weight and then concentrated nitric acid (4 mL, Merck, Darmstadt, Germany) and perchloric acid (2 mL, Merck) were added to the samples, and they were put on a hot plate set to 150 �C until all tissues were dissolved. Inductively coupled plasma atomic emission (ICP-AES, Varian Model, Liberty series II, Sydney, Australia) was used to determine metal concentrations. The metal concentrations (Cr, Cd, Pb, Cu, Fe, and Zn) in samples are reported as mg metal kg-1 dry weight. A high purity multi-element standard (Charleston, SC, USA) was used for determination of the metals. 
 
Statistical analysis
Statistical analysis of data was carried out with SPSS 16.0. Duncan�s test was used to evaluate the season and gender effects on metal levels in LCM and CCM of blue swimmer crabs.

RESULTS AND DISCUSSION
The carapace width (CW) of the blue swimmer crabs was in the range 112.0-175.0 mm (Table 1). In a study carried out on the coast of Egypt by Razek (1988), male and female blue swimmer crabs (P. pelagicus) with CW over 90-100 mm were considered to be adults. In a similar study carried out in the Kakinada region of India, Devi (1985) accepted male and female blue swimmer crabs (P. pelagicus) with CW over 95 mm as adults.  In the study conducted by Shields and Wood (1993) at Moreton Bay in Australia, it was found out that a minimum CW of 96-109 mm was needed for sexual maturation. In a similar study, Chang and Hsu (2004) reported that the minimum CW for females should be 82.36 mm and 92.86 mm for males for the sexual maturation of P. sanguinolentus living near the coast of Taiwan. Thus, according to the results of these studies, the male and female blue swimmer crabs used in our study were adults.
The annual differences in the Cd, Cr, Pb, Cu, Zn, and Fe levels of muscle tissue in blue swimmer crabs were determined as 0.50-1.47 mg/kg, 0.31-0.53 mg/kg, 0.10-0.52 mg/kg, 9.64-72.50 mg/kg, 37.80-178.61 mg/kg, and 7.31-25.51 mg/kg, respectively. The quantity relationships generally found in the metal levels of blue swimmer crabs in all the seasons were: Zn > Cu > Fe > Cd > Cr e" Pb (Table 2). Ayas and Ozogul (2011a) had reported Cd, Cr, Pb, Cu, Zn, and Fe levels in muscle tissues of Atlantic blue crab (C. sapidus) as 0.4-1.1 mg Cd kg-1, 0.2-0.6 mg Cr kg-1, 0.2-0.6 mg Pb kg-1, 9.7-68.1 mg Cu kg-1, 39.5-175.2 mg Zn kg-1, and 8.8-32.5 mg Fe kg-1, respectively, also caught in Mersin Bay, northeastern Mediterranean Sea. All our metal levels were similar to those found in that study. This may be related to the fact that the 2 different species were caught in the same region in both of the studies. In a similar study, Al-Mohanna and Subrahmanyam (2001) reported that Cr, Pb, Cu, and Zn levels of blue swimmer crab (P. pelagicus) were 0.2-0.7 mg/kg, 1.7-2.1 mg/kg, 110.2-142.8 mg/kg, and 188.7-221.7 mg/kg, respectively, in Kuwait Bay. Cr, Pb, Cu, and Zn levels presented by those researchers were higher than the data obtained in our study, possible because of busier fuel transfers in Kuwait Bay than in Mersin Bay. In a similar study, G�kolu and Yerlikaya (2003) reported Zn, Fe, and Cu levels in muscle tissue of blue swimmer crab (P. pelagicus) as 37.2-46.8 mg/kg, 4.5-6.8 mg/kg, and 14.9-20.8 mg/kg, respectively, in Antalya Bay, northeastern Mediterranean Sea. It can be seen that the results presented by them were lower than those in our study, which may be due to the fact that the crabs had been caught in different areas with different contamination levels. 
The findings indicated that the annual ranges of metal levels in the muscle tissues of female blue swimmer crabs were: 0.71-1.23 mg Cd kg-1, 0.32-0.53 mg Cr kg-1, 0.10-0.52 mg Pb kg-1, 11.74-70.62 mg Cu kg-1, 37.80-178.61 mg Zn kg-1, and 7.76-25.32 mg Fe kg-1. The annual ranges of metal levels in the muscle tissues of male blue swimmer crabs were: 0.50-1.47 mg Cd kg-1, 0.31-0.44 mg Cr kg-1, 0.29-0.46 mg Pb kg-1, 9.64-72.50 mg Cu kg-1, 37.98-150.13 mg Zn kg-1, and 7.31-25.51 mg Fe kg-1 (Table 2). Muscle tissue metal levels of female and male blue swimmer crabs were similar to each other independent from season and muscle types. In the present study, it was found out that there was no relationship between gender and metal accumulation. Ayas and Ozogul (2011a) had reported that in a study done in Mersin Bay, muscle tissue metal levels of female and male Atlantic blue crabs (C. sapidus) were similar to each other independent of season and muscle types. Olusegun and others (2009) had stated that metal accumulation differences between the sexes of C. amnicola species of portunid crabs were not important. In a similar study, Beltrame and others (2010) also indicated that there was no relationship between gender and bio-accumulated metals in burrowing crab (Neohelice granulata) caught in a coastal lagoon in Argentina. Furthermore, Chen and others (2005) reported that there was no relationship between gender and metal accumulation in muscle tissues of the rock crab (Thalamita crenata) caught in Dapeng Bay, Taiwan. All of those studies present findings similar to ours. 
The annual ranges of metal levels in the LCM of blue swimmer crab were: 0.50-1.01 mg Cd kg-1, 0.37-0.45 mg Cr kg-1, 0.10-0.40 mg Pb kg-1, 9.64-33.85 mg Cu kg-1, 37.80-78.16 mg Zn kg-1, and 9.35-25.51 mg Fe kg-1. The annual ranges of metal levels in the CCM of blue swimmer crabs were: 0.63-1.47 mg Cd kg-1, 0.31-0.53 mg Cr kg-1, 0.12-0.52 mg Pb kg-1, 25.13-72.50 mg Cu kg-1, 89.85-178.61 mg Zn kg-1, and 7.31-20.08 mg Fe kg-1 (Table 2). It can be seen that Cu, and Zn levels in CCM were higher than those in LCM (p <0.05). Cu and Zn metals specifically accumulated in CCM. Ayas and Ozogul (2011a) also found out that Cu (22.17-68.09 mg/kg) and Zn (93.92-175.21 mg/kg) in CCM of Atlantic blue crabs (C. sapidus) were higher than Cu (9.72-43.70 mg/kg) and Zn (39.52-97.26 mg/kg) in LCM caught in Mersin Bay. In a similar study, G�kolu and Yerlikaya (2003) also reported that Cu (2.08 mg/kg) and Zn (4.68 mg/kg) in CCM of blue swimmer crab (P. pelagicus) were higher than Cu (1.49 mg/kg) and Zn (3.72 mg/kg) in LCM caught in Antalya Bay, northeasthern Mediterranean. Both of those studies showed findings similar to those obtained in our study. The accumulation of Cu and Zn in CCM of portunid crabs may be a general characteristic.
According to our findings, the levels of Cd, Pb, Cu, Zn, and Fe in P. pelagicus showed seasonal variations. Seasonally, Cd and Pb showed very small variations. On the other hand, metals such as Cu, Zn, and Fe exhibited large seasonal variations (Table 2). It was found that Cu, Zn, and Fe levels in muscle tissues of blue swimmer crabs in spring and summer seasons were higher than those in autumn and winter. Ayas and Ozogul (2011a) also reported that Cd, Cr, Pb, Cu, Zn, and Fe levels in muscle tissues of C. sapidus showed seasonal changes. It was stated that, particularly, Cu, Zn, and Fe levels were higher in spring and summer than in autumn and winter, indicating large seasonal changes. Beltrame and others (2010) also reported that concentrations of some metals (Cd, Cu) in N. granulata displayed some seasonal changes. Both of the studies presented findings similar to those obtained in our study. Overall, the studies show conclusively that the levels of Cu, Zn, and Fe in P. pelagicus showed seasonal variations (Table 2). 
Molting of blue swimmer crabs in Mersin Bay was observed in October-November, and the crabs caught in these months were semi-soft shell crabs. Cu, Zn, and Fe levels in muscle tissues of blue swimmer crabs were found to be higher in spring and summer than in autumn and winter (Table 2). Reductions in feeding in autumn and winter compared with the other seasons and carapace molting in autumn may have played a role in these results. In the present study, molting was associated with differences in metal levels depending on the type of metal and muscle tissue. Molting caused a decrease in the levels of Cu, Zn, and Fe of blue swimmer crabs by 40-60% in autumn and winter, with the decreases in the CCM being lower than those in LCM. Ayas and Ozogul (2011a) also reported metal elimination and a reduction in Cu, Zn, and Fe levels by nearly 70% during the molting of carapace in Atlantic blue crabs in Mersin Bay. In a similar study, Bergey and Weis (2007) also found metal elimination and a reduction in Cu and Zn levels by 3-12% and 8-22%, respectively, during the molting of carapace in crabs. In a related study carried out by Benjakul and Sutthipan (2009), decreases of 100% in Cu, Fe, and Zn in soft shell crabs were reported compared with hard shell crabs. The researchers reported that the decreases in LCM were higher than those in CCM. The findings of our study are therefore supported by those of Benjakul and Sutthipan (2009). 
		Cd, Cr, and Pb levels in muscle tissue of blue swimmer crabs were determined annually as 0.50-1.47 mg/kg, 0.31-0.53 mg/kg, and 0.10-0.52 mg/kg, respectively (Table 2). The Cd limit levels reported by Anonymous (2001) and Anonymous (2005a) for crabs were 0.5 mg Cd kg-1. It was determined that blue swimmer crabs living in Mersin Bay were contaminated with Cd. The Cr limit level reported by Anonymous (2005b) was 12 mg Cr kg-1 for crabs. Anonymous (2001) and Anonymous (2005a) set a Pb limit level for crabs at 0.5 mg Pb kg-1. Thus, it can be stated that blue swimmer crabs living in Mersin Bay were not contaminated with Cr and Pb. 
		Cu and Zn levels in muscle tissues of blue swimmer crabs were determined to be 9.64-72.50 mg/kg and 37.80-178.61 mg/kg, respectively (Table 2). The Cu and Zn limit levels reported by Anonymous (2005a) for crabs was 20 �gCug-1 and 50 mg Zn kg, respectively. In the present study, generally, Cu levels in LCM of blue swimmer crabs were only lower than those limit level in autumn and winter. Cu levels in all muscle tissues of blue swimmer crabs were higher than the reported limit level by Anonymous (2005a), except for Cu levels in LCM of blue swimmer crabs in autumn and winter. Zn levels showed similarities with Cu levels and Zn levels in all muscle tissues of blue swimmer crabs were higher than the reported limit level by Anonymous (2005a) except for Zn in LCM of blue swimmer crabs in autumn and winter. Similar results were obtained for Cu and Zn levels in the study conducted on Atlantic blue swimmer crab in Mersin Bay by Ayas and Ozogul (2011a).

CONCLUSION
	It was found that the Cd, Cu, and Zn levels in blue swimmer crabs caught in Mersin Bay, Turkey, were higher than those that are internationally accepted. All blue swimmer crabs were contaminated with these metals. Molting was found to be a good detoxification mechanism for this crab species. It was recommended that these big sea crabs caught in Mersin Bay should be consumed only when caught in autumn and winter and in the other seasons their harvesting and consumption should be avoided or prohibited. 

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TABLES
























Table 1. Morphological measurements of blue swimmer crabs in Mersin Bay
SeasonNSCL
 EMBED Equation.3 Min-max
(mm)CW
 EMBED Equation.3 Min-max
(mm)Weight
 EMBED Equation.3 Min-max
(g)Sex
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Different letters (a, b) in the same columns for each season indicate significant differences (p<0.05).











Table 2. The effects of season and sex on metal levels of different muscle tissues of 
the blue swimmer crab (mg kg-1) 
MetalSexSpring
 EMBED Equation.3 Summer
 EMBED Equation.3 Autumn
 EMBED Equation.3 Winter 
 EMBED Equation.3 Muscle

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Cr@&0.40�0.03a,xy0.37�0.02b,x0.43�0.03a,xy0.45�0.02b,yLCM0.32�0.06a,x0.53�0.05d,y0.34�0.02a,x0.53�0.02c,yCCMB&0.38�0.05a,x0.44�0.01c,x0.38�0.05a,x0.44�0.01b,xLCM0.38�0.02a,x0.31�0.04a,x0.38�0.02a,x0.35�0.04a,xCCM
Pb@&0.29�0.04a,y0.30�0.02a,y0.29�0.01a,y0.10�0.02a,xLC>�@�N�#	$IfgdZ6�kd�$$If�l4�
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