Australian Journal of Basic and Applied Sciences, 5(6): 897-905, 2011 ISSN 1991-8178
Heavy Metals Accumulation in the Mantle of the Common Cuttlefish Sepia pharaonis from the Arabian Gulf
1Saleh Al Farraj, 2Amel H. El-Gendy, 1Hamad Alyahya and 1Magdy El-Hedeny
1Department of Sciences, College of Teachers, King Saud University, Riyadh, Kingdom of Saudi Arabia. 2Department of Zoology, Faculty of Science, Alexandria University, Alexandria, Egypt.
Abstract: The cuttlefish Sepia pharaonis Ehrenberg 1831, is a preferred marine edible species for the population of the Saudi Arabia captured from the Arabian Gulf water with a history of anthropogenic and industrial pollution, and receiving urban effluents. As the mantle is the edible part, this study was conducted on this organ to ascertain the levels of heavy metals, both essential (Cr, Cu, Zn and Ni) and non essential (Cd and Pb). The level of elements was determined by atomic absorption spectrophotometry (AAS). The concentration ranges found for these heavy metals, expressed on a wet weight basis, were as follows: Pb, Zn, Cu, Cr, Cd and Ni concentrations in cuttlefish samples were 0.25 - 0.54, 5.74 - 9.44, 2.12 - 3.98, 0.19 - 0.47, 0.03 - 0.09 and 0.15 - 0.40 mg kg -1, respectively. The level of contamination in Sepia pharaonis by these heavy metals is compared to those studied in other parts of the world and the legal standards set by international legalizations. We provide evidence for the following: (1) levels of heavy metal in the studied species were found to be within the safe limits for human consumption, (2) there was a negative correlation between Cu and Zn (r = - 0.2578), (3) the mantle length influenced metal concentration in different ways.
Key words: Heavy metals; accumulation; cuttlefish; Sepia pharaonis; Saudi Arabia; Arabian Gulf.
INTRODUCTION
The development of urban infrastructure, along the east coast of Saudi Arabia during the past 30 years and the several industrial complexes has been established along its coast line has been detected during the past decades (e.g. Khan and Al-Homaid 2000; Alyahya, et al. 2011). Fisheries, maritime cultivation, transport and tourism, deficient wastewater treatment has caused major disturbance to the coastal environment of the Arabian Gulf (Sadiq and Alam 1989; Al-Saleh and Shinwari 2002; Khan and Al-Homaid 2003; Alyahya, et al. 2011). Moreover, the first and the second Gulf wars resulted in two of the largest oil spills to the marine water (Abu- Hilal and Khordagui 1993; Price et al. 1993; Massoud et al. 1998; Banat et al. 1998; El Hakeem et al. 2007). All these different sources of pollutants resulted in serious pollution of heavy metals in the Arabian Gulf water and its creatures (Sadiq and Zaidi 1985; Sadiq and McCain 1993; Al-Madfa, et al. 1998; Al-Saleh and Shinwari 2002; Al-Bader 2008; Alyahya et al. 2011). Stock of marine fish and shellfish within the Saudi Arabia are increasingly threatened by aquatic pollution, but no data are available on the extent pollution impacts (Al-Kahtani 2009). Exposure and ingestion of polluted marine organisms as sea foods can cause health problems in people and animals including neurological and reproductive problems (Han et al. 1998; Osfor et al. 1998; Allen and Moore 2004). Cephalopod represents an increasing component of the world’s fisheries (Boyle and Rodhouse 2006; FAO 2007). They are consumed throughout the world, both as food and as feed supplement and have a great commercial value (Navarro and Villanueva 2001; Koueta and Boucaud-Camou 2001). Indeed, they are actually much appreciated as a protein source and because of their gustative quality. Cephalopods are consumed not only fresh, but also manufactured into processed food in huge quantities such as dry frozen and chilled products (Paredi and Crupkin 1997; Ueng and Chow 1998; Hurtado et al. 2001). Many studies have been achieved on the contamination of different cephalopods species with heavy metals in different parts of the world (e. g. Bryan 1968; Miramand and Bentley 1992; Bustamante et al. 2002a,b; Suhaimi et al. 2005). Till now, there are no studies on heavy metal contamination in cephalopods of the eastern coast of Saudi Arabia waters. The pharaoh cuttle Sepia pharaonis Ehrenberg, 1831 (Cephalopoda:
Corresponding Author: Magdy El-Hedeny, Department of Sciences, College of Teachers, King Saud University, Riyadh, Kingdom of Saudi Arabia
897 Aust. J. Basic & Appl. Sci., 5(6): 897-905, 2011
Sepiida) is a broadly distributed species of substantial fisheries importance found in the wet market of the Saudi Kingdom. So far, most Saudi people obtain their fish and shellfish from fish markets and supermarkets. Hence, it is important to know the contaminant levels in these kinds of seafood. Because most of these foodstuffs have a local origin, the exposure to different marine pollutants could pose a risk for the health of the population. However, consumers cannot make informed decisions about what they have to eat if they do not know how contaminants vary among those animals. The aims of our study are two-fold: first, to assess the health risks from exposure to metals through the consumption of the local cuttlefish Sepia pharaonis for the population living in the Eastern Province of the Saudi Kingdom. Secondly, we attempt to find potential relationships for heavy metal concentrations with specimen's mantle length.
MATERIAL AND METHODS
2.1. Collection of Samples: Al- Khobar is a large city located in the Eastern Province of the Kingdom of Saudi Arabia on the Arabian Gulf. It was a small port, inhabited mainly by fishermen. Since the discovery of oil in this area, the city was transformed into an industrial port. In time, it has become the commercial hub of the Eastern Province. Besides, it is developing into an important industrial city. The studied samples of the cuttlefish Sepia pharaonis were collected from different fish markets at Al- Khober City, east coast of the Saudi Arabia. They were selected for analysis based on their popularity among local consumers. The collected animals should be of consumable or “market” size. The animals were packed in ice and transported in an insulated container bags to the laboratory.
2.2. Preparation of Samples: Upon arrival at the laboratory, the specimens were identified to select the studies species. The cuttlefish specimens were identified, then, divided into 14 groups (each group contain 5 animals) according to the mantle length increase. Immediately frozen in individual plastic bags, in order to minimize mobilization of metals between organs (Martin and Flegal 1975) and kept at !25 °C until later processing for analysis.
2.3. Chemical Analysis:
Reagents: De-ionized water was used to prepare all aqueous solutions. All mineral acids and oxidants used were of the highest quality (Merck, Germany). All the plastic and glassware were cleaned by soaking overnight in a 10% (w/v) nitric acid solution and then rinsed with deionized water.
Digestion: Approximately one-two grams of the mantle tissues were weighted and transferred into an air-tight quick
flask with glass stopper. A mixture of 4 ml of conc. HNO3 and 1 ml of 60% perchloric acid were added to each sample and digested in a temperature controlled hot plate at 85°C. After removal from hot plate, the samples were cooled at room temperature. Then, the samples were separately filtered using an ashless filter paper and diluted to 100 ml with deionized water and stored for analyses of heavy metals. Sample blanks were prepared in the laboratory in a similar manner to the field samples. Metal contents were expressed as mg kg-1 wet weight. The accuracy of the method was determined by measuring the recovery, recoveries were > 92% for the known amount of each element.
2.4. Metal Analysis: In this study, Zn, Cu, Ni, Cd, Cr and Pb in the mantle of the cuttlefish Sepia pharaonis were determined using Perkin-Elmer Analyst 300 Atomic Absorption Spectrophotometer (AAS). The analyses were performed at least in triplicate.
2.5. Statistical Analysis: An independent t test analysis was applied to the observed data to check the level of significance site-wise. Pearson’s Correlation Coefficient Statistical functions on Microsoft Excel were used to test the relation between the metal concentrations and the mantle length of the specimens.
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RESULTS AND DISCUSSION
Levels of contaminants in marine animals are of particular interest because of the potential risk to humans who consume them. In particular, the tendency of heavy metals to accumulate in various organs of cephalopods, which in turn may enter the human metabolism through consumption causing serious health hazards. Accumulation of metals in marine animals is the function of their respective membrane permeability and enzyme system, which is highly species specifics and because this fact different metals accumulated in different orders in the studied cuttlefish samples. Therefore, the present study was undertaken to evaluate the heavy metals accumulation of Zn, Cu, Pb, Cr, Ni and Cd in the mantle tissues of the edible cuttlefish, Sepia pharaonis. The studied metal concentrations revealed an order of Zn > Cu > Pb > Cr > Ni > Cd (Fig. 1). Furthermore, we attempted to find a correlation between the mantle length and the heavy metal accumulation abilities in Sepia pharaonis (Fig. 2).
Fig. 1: Average concentration of heavy metals in the cuttlefish Sepia pharaonis.
3.1. Lead: Lead constitutes a serious health hazard to both children and adults. The adverse toxic effect caused by Pb on human was documented by Subramanian (1988). The high blood lead level can cause kidney dysfunction, brain damage, anemia and can inhibits the normal functioning of many enzymes (Forstner and Wittmann 1983; USFDA 1993). In the present study, Pb concentrations in the mantle tissue of Sepia pharaonis varied from 0.25 to 0.54 mg kg-1; all these values are lower than the Maximum Permissible Level (MPL) established by the European Council Commission (CE 2006) (1.0 mg kg-1 of Pb for bivalves and cephalopods) and also recommended by the Food Standards of Australia (FSA 2002) in mollusks. The low value (average content 0.28 mg kg-1) of Pb concentration in the present study may indicates that the mantle of the Sepia pharaonis is not the target organ for Pb accumulation. This may agree to the study of Craig and Overnell (2003). They concluded that Pb concentration in the digestive gland of the squid Loligo forbesi was 64.3 mg kg-1 wet weight, while in mantle of the same species was 0.6 mg kg-1 (Table 1). Later, Lourenço et al. (2009) stated that the concentration range of lead in arms and the mantle of Sepia officinalis was between 0.03 and 0.05 mg kg-1 wet wt. The accumulated Pb in the mantle of the present species may due to the fact that the Arabian Gulf water is highly stressed with respect to lead (Sadiq et al. 1992; Hassan et al. 1996; Banat et al. 1998; Alyahya et al. 2011).
3.2. Zinc: Zinc is an essential trace element required by all living organisms because of its critical role both as a structural component of proteins and as a cofactor in enzyme catalysis (Lall 1989; Sandstrom 1997; Leigh Ackland and Michalczyk 2006). Zinc is always present in seafood, but concentrations found in mollusks are
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generally higher (Lall 1995; Celik and Oehlenschläger 2004). Zn is involved in numerous protein functions such as the carbonic anhydrase and is efficiently absorbed and strongly retained in Sepia officinalis both from the food and seawater pathways (Villanueva and Bustamante 2006). This study showed that Zn concentrations ranged between 5.74 and 9.44 mg kg-1. Although the average Zn concentration (5.17 mg kg-1) represents the highest metal value (Fig. 1), it seems rather low when compared to the values detected in the mantle of other cephalopod species (Table 1). Moreover, it is lower than the values determined by Lourenço et al. (2009) in arms and mantles of some common Portuguese cuttlefish (14.0- 22.5 mg kg-1 wet weight).
Table 1: Average of the heavy metal concentrations (mg/kg) in the mantle of some species of Coleoidea in comparison to the present study. Species Zn Cu Cd Ni Pb Reference The squid Illex argentinus 12.8 5.14 0.74 - - Gerpe et al. 2000 The cuttlefish Sepia officinalis 14.1 2.05 0.0 - - Mirmand and Bentley 1992 The octopus Eledone cirrhosa 20.6 3.33 0.0 - - Mirmand and Bentley 1992 The squid (adult) Loligo forbesi 17.0 4.1 0.1 1.1 0.6 Craig and Overnell 2003 The cuttlefish Sepia pharaonis 5.17 2.19 0.04 0.21 0.28 Present study
Craig and Overnell (2003) found that Zn present in the cytosol, as a percentage of total tissue metal, in squid Loligo forbesi tissues, in mantle was 11.5, while in the digestive gland was 43.0. This agrees with the results of previous studies which reported an increase of zinc concentration stored in metal-containing enzymes and metalloproteins in the digestive gland of the cephalopods (e.g. Miramand and Bentley 1992; Gerpe et al. 2000; Villanueva and Bustamante 2006; Lacoue-Labarthe et al. 2008). Accordingly, although Zn is an essential element for most cephalopods, mantle tissues still accumulate the lower values.
3.3. Cadmium: Concerning Cadmium, the capability of cephalopods to concentrate high quantities of cadmium is well known (Miramand and Guary 1980; Miramand and Bentley 1992; Bustamante et al. 1998).The mantle of cuttlefish does not mentioned before as a specific organ for Cd accumulation ,whereas, the digestive gland plays a primary role in the accumulation of Cd in cuttlefish. Such a role can be related both to the very efficient detoxification processes of the metal occurring in this organ and to the very high Cd assimilation efficiency (Bustamante et al. 2002a; Bustamante et al. 2006). Dorneles et al. (2007) reported very high Cd concentrations; reach up 1000 µg g-1 wet wt, in the digestive gland of the short-lived species Illex argentinus. They stated that this value represents the highest cadmium level ever reported for a cephalopod. However, in this study, the average concentration of Cd in the mantle of Sepia pharaonis was (0.04 mg kg-1). This result is compared with values recorded by other authors (Table 1). Lourenço, et al. (2009) found that Cd concentrations in the arms and the mantle of Sepia officinalis ranged between 0.03 and 1.0 mg kg-1 basis on wet wt. The present results exceeded the maximum levels permitted (2 µg g-1) in molluscs that are recommended by FSA (2002) and disagree with Prafulla, et al. (2001) who stated that in the squid, mantle tissues accumulated relatively low values for Cd and was far below the tolerance limit. Generally, many studies have suggested that squid mantle could be consumed safely in most countries, considering the Cd concentration is two orders of magnitude lower than those in the digestive gland (Kim et al. 2008).
3.4. Copper: Mollusks, particularly cephalopods use the soluble copper containing protein haemocyanin as a respiratory pigment, therefore copper is required in large concentrations (Decleir et al. 1978; Viant et al. 2002). In addition, Martoja and Marcaillou (1993) stated that Cu accumulates in membrane-limited vesicles (spherules) within the basal cells of the liver the Sepia officinalis. They postulated that copper was bound to a ‘metallothionein-like’ protein which has been detected in heat-treated liver cytosols from cephalopods (Bustamante et al. 2002a).
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Fig. 2: Variations of metal concentrations (mg/kg wet weight) in the cuttlefish Sepia pharaonis in relation to the mantle length.
The present study recorded that Cu forms the second most abundant element after zinc in the mantle tissues of the Sepia pharaonis (average concentration 0.04 mg kg-1) (Fig. 1). A comparison to the average Cu concentrations in the mantle of the different cephalopod species is tabulated in table 1. The involvement of this element in several metabolic functions, such as in metal-dependent enzymes (Bustamante et al. 2000; Craig and Overnell 2003) may explain its high concentration in the present species. Lourenço et al (2009) showed that Cu in the edible part (arms and mantle) of some cuttlefish species was ranged between 1.7-10.3 mg kg-1. Among the various body organs of the squids Loligo duvauceli and Doryteuthis sibogae, the muscles had the lowest Cu content (Prafulla et al. 2001). Craig and Overnell (2003) concluded that Cu present in cytosol of the squid Loligo forbesi as follows (as a percentage of total tissue metal) 20% in the mantle and 35% in the digestive gland. Hence, the mantle tissue looks as if it is not the target organ for Cu accumulation.
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3.5. Nickel: A few years ago, the physiological functions of nickel (Ni) were unclear. Nowadays, it is thought that Ni plays an important role in hormone, lipid and cell membrane metabolism. Several studies on nickel indicated to the role of nickel in various enzymatic system as well as activating enzymes associated with the glucose breakdown and use (Nielsen 1971; Waters et al. 1975, Nielsen et al. 1984; Lall 1995; Acu-Cell 2007). In the present study, Ni concentration in the mantle of Sepia pharaonis ranged between 0.21 ± 0.05 and 0.40 ±0.08 mg kg-1 wet wt. Bustamante et al. (2008) have noticed that very little data are available on the variation of Ni concentrations in cephalopod tissue. However, our obtained values are higher than those detected by Lourenço, et al. (2009) in the edible parts (arms and mantle) of the cuttlefish Sepia officinalis (0.02-0.09 mg kg-1 wet wt.). On the other hand, Villanueva and Bustamante (2006) observed low concentrations of Ni in the European cuttlefish Sepia officinalis as compared to the European squid Loligo vulgaris and the common octopus Octopus vulgaris. Concerning the relationship between Ni concentration and specimen sizes of squid, Ichihashi et al. (2001) have noticed that the concentration of Ni was greater in adults of the squid Sthenoteuthis oualaniensis than in the juveniles. On the other hand, Craig and Overnell, (2003) observed that adults of the species Loligo forbesi have an average Ni concentration of 1.1 mg kg-1 wet wt (Table 1).
3.6. Chromium: Chromium is an essential trace element for human body for glucose tolerance (Dung 2001). Despite its high toxicity at high doses (Burger and Gochfeld 1995), mammalian bodies can tolerate 100 to 200 times their total natural body content of Cr without harmful effects (Moore and Ramamoorthy 1984). In the present specimens, the mean average concentration of Cr in their mantles was 0.22 mg kg-1 (Fig. 1). Schumacher et al. (1992) found that the mean concentrations of chromium in the flesh of cephalopods were ranged from 0.090 to 0.220 µg/g of fresh weight. On the other hand, Prafulla et al. (2001) found that the mean muscle value for Cr in the two squids species Loligo duvauceli and Doryteuthis sibogae was < 1.0 ppm. After their study on some species of the cuttlefish Sepia, Ahdy et al. (2007) concluded that the average concentration of Cr was 2.2 µg/g. From other point of view, Cr concentrations were higher in juveniles than in adults, in the squid Sthenoteuthis oualaniensis (Ichihashi et al. 2001).
Conclusions: The edible cuttlefish, Sepia pharaonis Ehrenberg 1831 is a preferred marine animal for the population of the Saudi Arabia. Heavy metal concentrations in the mantle of different size samples of this species follow the order Zn > Cu > Pb > Ni > Cr > Cd. The levels of contamination in the mantle of the cuttlefish, Sepia pharaonis are generally low and /or well within the maximum permitted concentrations imposed by various organizations and authorities. So, the concentration levels of heavy metal in S. pharaonis, available in the wet markets of the Eastern Province of the Saudi Kingdom, were found to be within the safe limits for human consumption and do not pose any risk to the consumers. Statistically significant positive correlations were detected between the concentrations of Ni, Pb, Cd and Cr and the mantle lengths of Sepia pharaonis, while Zn displayed a significant negative correlation. However, no significant correlation was observed between Cu concentration and the mantle length of the studied specimens. The average concentration of Zn was significantly decreased by increasing the mantle length that may suggests that small specimens are highly dependent on this metal to fulfill their metabolic demands.
ACKNOWLEDGMENT
The authors would like to thank the Research Center, College of Teachers, King Saud University and the Center of Excellence for Biodiversity Research, College of Science, King Saud University, Riyadh, Kingdom of Saudi Arabia for supporting this project (BIO/200152).
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