Environ Monit Assess (2011) 177:505514 DOI 10.

1007/s10661-010-1651-9

Heavy metal concentrations in some macrobenthic fauna of the Sundarbans mangrove forest, south west coast of Bangladesh
Kawser Ahmed Yousuf Mehedi Rezaul Haque Pulakesh Mondol

Received: 16 December 2009 / Accepted: 29 July 2010 / Published online: 17 August 2010 Springer Science+Business Media B.V. 2010

Abstract Heavy metal concentrations in some macrobenthic fauna have been reported for the first time from the Sundarbans mangrove forest, south west coast of Bangladesh, in the northern part of Bay of Bengal. The concentration of Fe, Cu, Zn, Cd and Pb in macrobenthos ranged from 235 10.11 to 1,051 38.42, 3.66 0.89 to 7.55 1.29, 76.8 8.55 to 98.5 6.49, 0.46 0.11 to 0.859 0.2 and 4.66 1.17 to 6.77 2.1 g/g, respectively. Significant variations ( p 0.05) in heavy metal concentrations have been observed among the mud crab, mudskipper and gastropod. However, heavy metal burdens did not vary significantly among the hermit and horseshoe crabs. In mud crab, horseshoe crab and gastropod, heavy metal concentrations were recorded in the sequence: Fe > Zn > Pb > Cu > Cd. Hermit crab and mudskipper contained heavy metals in the order of Fe > Zn > Cu > Pb > Cd. Fe and Zn

concentrations were found significantly ( p 0.05) higher in macrobenthos. The lead (Pb) concentration found in the edible portion of macrobenthos exceeded the international permissible limits certified by the WHO. Bioconcentration factors >1.00 obtained for Fe (17.05 in mudskipper) and Cd (1.87 in gastropod) indicated that these metals were highly bioaccumulated and biomagnified in benthic fauna of Sundarbans. The findings of this study refer to the potential impact of heavy metals in the mangrove ecosystem of Bangladesh. Keywords Heavy metals Macrobenthos Bioaccumulation Sundarbans mangrove forest

Introduction The Sundarbans mangrove forest, covering about 10,000 km2 of land and water, is a part of the worlds largest delta (80,000 km2 ) formed from sediments deposited by three great rivers the Ganges, Brahmaputra and Meghna (GMB, Seidensticker and Hai 1983). Mangrove is one of the biologically productive natural ecosystems (Blower 1985). The coastal area of Bangladesh is suitable for molluscan habitats (Ahmed 1990) and it is documented that the intertidal belt of the Sundarbans Reserve Forest (SRF) supports

K. Ahmed (B) Department of Fisheries, University of Dhaka, Dhaka 1000, Bangladesh e-mail: kawser@univdhaka.edu Y. Mehedi R. Haque P. Mondol Fisheries and Marine Resource Technology Discipline, Khulna University, Khulna 9208, Bangladesh

506

Environ Monit Assess (2011) 177:505514

diverse macrobenthic fauna (Mishra et al. 1983; Subba Rao et al. 1983; Chaudhury et al. 1984; Chakraborty et al. 1986). Sediments of the GMB river system in the Bengal Basin have the potential to trap contaminants because of their grain size and mineralogy (Haque et al. 2006). Among the contaminants, the accumulation of toxic metals to hazardous levels in aquatic biota has become a problem of increasing concern (Mukherjee et al. 2004; Tsangaris et al. 2007). Heavy metals, being non-biodegradable, can accumulate in the food chain, producing their toxic effects at points after being removed far away from the source of pollution (Tilzer and Khondker 1993). Even at very low sub-lethal concentrations, certain heavy metals can seriously hamper the basic metabolic functions of life. Several researchers (Sarkar et al. 1999, 2002; Bhattacharya et al. 2003) have reported the bioaccumulation of heavy metals in some biota of Hugli estuary, India. Studies on aquatic pollution, particularly in marine ecosystems, have received relatively less attention (Duarte 2000; Naeem 2006). To date, in Bangladesh, a few attempts have been made to study the heavy metal pollution in the coastal and mangrove areas. However, in Bangladesh, tests to measure the levels of the presence of few heavy metals in some marine fishes of the Bay of Bengal have been carried out (Sharif et al. 1991, 1993a, b). The texture, mineralogy of sediments and distribution of heavy metals in the surface sediments from the GMB river system have been reported by Datta and Subramanian (1998). Ahmed (2000), Holmgren (1994), Biswas et al. (1998), Ahmed et al. (2002, 2003, 2009, 2010) and Haque et al. (2003, 2004, 2005) have done some pioneering work to investigate the concentrations of heavy metals in the water and sediments of Sundarbans mangrove forest. However, to date, except Haque et al. (2006), no research work has been carried out on the heavy metal concentrations in benthic fauna in the rivers and estuaries of Sundarbans mangrove forest, Bangladesh. In view of this, the present study has been carried out to investigate the concentrations and bioconcentration factors (BCF) of heavy metals in some macrobenthic fauna of the Sundarbans mangrove forest, Bangladesh.

Materials and methods Study area The Sundarbans mangrove forest (89 00 and 89 55 E and 21 30 and 22 30 N) is located in the estuary of the river Ganges in southwest Bangladesh and the south-western region of the State of West Bengal in India. The forest meets the Bay of Bengal in the south. The forest covers an area of 577,000 ha (70%) of which 401,600 ha is land and the remaining 175,600 ha are under water in the form of rivers, canals and creeks with width varying from a few meters to several kilometers. Some of these are purely tidal in nature and not connected with any source of freshwater. Most creeks and canals flow into the large rivers which are interconnected (Chaffey et al. 1985). Recently, the Sundarbans mangrove forest has been declared as a UNESCO world heritage site and a management plan has been made to conserve the natural wetland ecosystem (FAO/UNDP 1998a, b).

Sampling Samples were collected from Dublarchar (21 43 41.72 N, 89 36 16.85 E) of Sundarbans mangrove forest (Fig. 1). It is the estuary circumscribed by the Sundarbans and formed by the rivers Passur and Shibsa and is located 87 km away from the Mongla Port. It is a very important point for ecological studies because the inland and on-shore water flows are crisscrossed, ultimately inundating the Sundarbans mangrove forest. Samples were collected from the intertidal zone during low tides and only shallow water macrobenthos of the continental shelf were considered. Samples were collected by cast net and also from the fishermen while they were catching crabs by using bait. Different macrobenthos samples and their average lengths are given in Table 1. Samples were preserved according to UNEP/FAO/IAEA/IOC (1984). After collection of the samples, mud and other organisms were removed by washing them with sea water at the

Environ Monit Assess (2011) 177:505514

507

Fig. 1 Location map of the Sundarbans mangrove forest and sampling site, Dublarchar

sampling site. Samples were kept overnight in a sea water tank for defaecation. Analytical procedure The softer parts of the body of the samples were separated and dried at room temperature and weighted. After washing, the samples were dried in an oven at 55 C to an anhydrous state until a constant weight was obtained. The dried samples were then ground with the help of a glass mortar and sieved thoroughly to produce a homogeneous powder. The powdered samples were finally stored in bottles and preserved in desiccators for further analysis. One gram of each powdered sample was kept in 50-ml Pyrex beaker and placed in the muffle furnace at 50 C, 450 C and 550 C for 10 min, 1 h and 8 h, respectively, by raising the temperature for complete ashing. Ashed samples were then digested with 2 ml of concentrated HNO3 on a water bath (above 100 C) for 30 min to about

an hour and were evaporated to about dryness. After evaporation, 1 ml of HNO3 was added in each beaker and heated for sometime. Then, 3 ml of deionized water were added and warmed on a water bath for a few minutes. Blank digestion was also made to quantify possible contamination. After cooling, the digested samples, along with the blanks, were filtered by using filter paper (Whatman 541) and made the filtrate up to 10 ml with deionized water. Prior to analysis, several dilutions of the digested samples were made.

Table 1 Average length (in centimeters) of macrobenthos studied Macrobenthos Gastropod (Assiminea brevicula) Hermit crab (Eupagurus sp.) Mud skipper (Gobius boddarti) Mud crabs (Scylla serrata) Horseshoe crabs (Carcinoscorpius rotundicauda) Average length (cm) 0.045 2.50 16 15 30

508
1200 1000 800 600 400 200 0 Hermit Horseshoe Mud Crab Gastropod Mud Crab Crab Skipper

Environ Monit Assess (2011) 177:505514

where BCF is the bioconcentration factor, Corg is the concentration of metal in the organism and Csed is the concentration of the same metal in the ambient environment (i.e. sediment). Statistical analysis Statistical comparison among means was performed by univariate analysis by SPSS software version 12.0 (SPSS Inc., Chicago, IL, USA). Differences were significant at p 0.05.

Fig. 2 Iron (Fe) concentration (mean SD) in the studied macrobenthos

The quantitative measurement of Fe, Cu, Zn, Pb and Cd were carried out using airacetylene flame with a combination of single-element hollow cathode lamps and Perkin Elmer 560 Atomic Absorption Spectrophotometer at the Chemistry Division, Atomic Energy Center, Dhaka. The standard solution of the elements Fe, Cu, Zn, Pb and Cd was procured from Fisher Scientific Company, USA. The standard solution was prepared before each analysis. The analytical quality of the work was checked by analysis of standard reference materials NBS-SRM-1573, tomato leaves, and NBS-SRM-1566, oyster tissue, prepared by the National Bureau of Standards, Washington, DC, USA. The analytical procedures were also calibrated against the above standard reference materials. The average recovery ranged between 94% and 107%. The BCF of the heavy metals in the macrobenthos samples were obtained as worked out by Vassiliki and Konstantina (1984) and Falusi and Olanipekun (2007) by using the following formula: BCF = Corg Csed

Fe (g g-1)

Results Iron (Fe) content in mudskipper was highest (1,051 38.42 g/g) and lowest in gastropod (235 10.11 g/g) among the five macrobenthos studied (Fig. 2). The concentration of Fe observed in mud crab was 595.29 25.72 g/g, in horseshoe crab was 480.66 22.54 g/g and in hermit crab was 375 17.23 g/g. Among the five benthos, hermit crab contained the highest Cu (7.55 1.29 g/g) and gastropod contained the lowest (3.66 0.89 g/g). Cu content in mud crab and in horseshoe crab was 6.28 2.13 and 5.66 1.36 g/g, respectively, and in mudskipper, it was recorded to be higher (7.23 1.1 g/g) than in crabs (Fig. 3). Another essential trace element Zn content was observed highest in gastropod (110 8.82 g/g) and lowest (76.8 8.55 g/g) in horseshoe crab. Among the rest, the mudskipper contained the highest (98.5 6.49 g/g) followed by the hermit crab (95.5 5.25 g/g) and mud crab (85.5 9.27 g/g; Fig. 4). The highest concentration of cadmium (Cd) was recorded in gastropod (0.859 0.2 g/g)

10 Cu (g g-1) Zn (g g-1) 8 6 4 2 0 Hermit Crab Horseshoe Mud Crab Gastropod Crab Mud Skipper

150 100 50 0 Hermit Crab Horseshoe Mud Crab Gastropod Crab Mud Skipper

Fig. 3 Cupper (Cu) concentration (mean SD) in the studied macrobenthos

Fig. 4 Zinc (Zn) concentration (mean SD) in the studied macrobenthos

Environ Monit Assess (2011) 177:505514

1.2 1 0.8 0.6 0.4 0.2 0 Hermit Crab Horseshoe Mud Crab Gastropod Mud Crab Skipper

509

Discussion The coastal region of the Bay of Bengal is a potential area of heavy metal pollution as it is the point of discharge for majority of the rivers of the subcontinent that carry industrial effluents and wastes to the sea. Sediments may act as indicators of heavy metal burden in a coastal environment, as they are the principal reservoir for heavy metals (Fitchko and Hutchison 1975). Mangroves act as sediment trap and hence mangrove macrobenthos are susceptible to potential heavy metal pollution. Fe content in molluscs (gastropods) from the Sundarbans mangrove forest varied from 224.0 37 to 485.3 339 g/g (Haque et al. 2006). Fe content in molluscs from New Caledonia was found to be 258 79 g/g (Bustamante et al. 2000). The average concentration of Fe in molluscs was 1,338 g/g (Pez-Osuna et al. 1993). Fe content in gastropods of Sundarbans mud flat of India was highest among the heavy metals and it varied seasonally from 442 to 1,216 g/g dry weight (Sarkar et al. 2002). The findings of the present study conform to the above studies. The highest concentration of Fe found in the present study might be due to ship breaking and repairing activities of Khulna Shipyard and boat and barge building and repairing activities of Khalishpur, Bangladesh. In Kuwaits marine environment, the highest concentration of Cu (12.5 g/g) was observed in clams as sediment of that region is enriched with this pollutant (Zorba et al. 1992). The concentration of Cu fluctuates seasonally within the range of 3.0 to 6.6 g/g in Patella sp. and 0.8 to 2.0 g/g in Fucus sp. (Miramand and Bentley 1992). Cu concentration in molluscs (bivalves) from the Dhaleswari and Shitalakhya rivers, Bangladesh were reported to vary seasonally from 7.55 to 11.5 and 5.47 to 8.19 g/g, respectively (Ahmed et al. 2009, 2010). Seasonal variations of Cu in molluscs of Sundarbans were moderate and the concentrations were high during the winter season with the maximum mean concentration (38.51 15 g/g) found downstream (Haque et al. 2006). Higher concentration of Cu (185 g/g dry weight) was reported in gastropods of Sagar Island, India (Sarkar et al. 2002), whereas much lower concentration of Cu in different tissues in bivalve (Marcia pinguis) was reported from the same

Fig. 5 Cadmium (Cd) concentration (mean SD) in the studied macrobenthos

and the lowest was in horseshoe crabs (0.46 0.11 g/g), whereas, in mudskipper, mud crab and hermit crab, it was 0.725 0.21, 0.551 0.13 and 0.462 0.12 g/g, respectively (Fig. 5). Besides, in mud crabs, lead (Pb) content was the highest (6.77 2.1 g/g) and the lowest was recorded in hermit crab (4.66 1.17 g/g). However, the horseshoe crab (5.8 1.99 g/g) and gastropods (6.5 0.74 g/g) contained higher Pb than that of the mudskipper (4.99 0.82 g/g; Fig. 6). The metal concentrations varied within the same species. Fe content was highest among all the five metals irrespective of species, whereas Cd content was lowest in the horseshoe crab (0.46 0.11 g/g). In mud crab, horseshoe crab and gastropod, metal concentrations were found in the order of Fe > Zn > Pb > Cu > Cd, and in the hermit crab and mudskipper, the order was Fe > Zn > Cu > Pb > Cd. The BCF of the heavy metals in macrobenthos is shown in Table 2. Among the heavy metals, Fe was found to score higher BCF in all macrobenthos and the highest value was observed in mudskipper (17.05).

Cd (g g-1) Pb (g g-1)

10 8 6 4 2 0 Hermit Crab Horseshoe Mud Crab Gastropod Crab Mud Skipper

Fig. 6 Lead (Pb) concentration (mean SD) in the studied macrobenthos

510 Table 2 Bioconcentration factor (BCF) of heavy metals in macrobenthos Sediment Fe Cu Zn Cd Pb 61.66a 129.8a 730b 0.46b 300b Hermit crab BC 375 7.55 95.5 0.462 4.66 BCF 6.08 0.06 0.13 1.00 0.02 Horseshoe crab BC 480.66 5.66 76.8 0.46 5.8 BCF 7.80 0.04 0.11 1.00 0.02 Mud crab BC 595.29 6.28 85.5 0.551 6.77 BCF 9.65 0.05 0.12 1.20 0.02

Environ Monit Assess (2011) 177:505514

Gastropod BC 235 3.66 110 0.859 6.5 BCF 3.81 0.03 0.15 1.87 0.02

Mud skipper BC 1,051 7.23 98.5 0.725 4.99 BCF 17.05 0.06 0.13 1.58 0.02

BC heavy metal concentration in the body (in microgram per gram), BCF bioconcentration factor a Ahmed et al. (2002) b Ahmed et al. (2003)

location (Saha et al. 2006). In mud crab (Scylla serrata), highest Cu (341.04 g/g) content was reported from Malanch region of Indian Sundarbans (Banerjee et al. 2006). Cu concentrations found in the macrobenthos of Bangladesh Sundarbans were lower than those of the Indian Sundarbans. The enrichment of Cu in macrobenthic fauna might be due to the offshore input of Cu in water and sediments. Cu is intimately related to the aerobic degradation of organic matter (Das and Nolting 1993). High litter falls in mangroves and their degradation might cause the high level of Cu accumulation in the macrobenthos. The average concentration of Zn in mangrove molluscs (Nerita lineata) in Cleveland Bay was 50 g/g (Jones et al. 2000). The concentration of Zn in sediment and water was found to be 80.6 to 730 g/g and 0.002 to 0.154 g/L, respectively, in upstream river of Sundarbans mangrove forest (Ahmed et al. 2003). The concentration of Zn in molluscs from the Basundia and Hironpoint, Bangladesh were 29.32 7.0 and 28.79 6.7 g/g, respectively (Haque et al. 2006). In S. serrata from Sundarbans mangrove forest, India, the highest concentration of Zn was found to be 648.29 g/g (Banerjee et al. 2006). In gastropods, Zn concentration is reported to vary seasonally from 55 to185 g/g in the Indian Sundarbans (Sarkar et al. 2002). In the present study, the concentrations of Zn conform to the above findings. Cd concentration in molluscs (bivalves) seasonally varied from 0.52 to 0.8 g/g from the Dhaleswari River and from 1.09 to 1.21 g/g from the Shitalakhya River, Bangladesh (Ahmed et al. 2009, 2010). The mean concentration of Cd in molluscs from New Caledonia was 16 6.5 g/g (Bustamante et al. 2000). Seasonal and inter-

species variations in Cd concentrations (below detectable level to 80 g/g) of gastropods were reported from Indian Sundarbans (Sarkar et al. 2002). Accumulation of Cd in clam (0.18 to 0.32 g/g) was reported to depend on the bioavailability of Cd in sea water and sediment (Zorba et al. 1992). Cd uptake rate increases with temperature and low salinity in Crassotrea viginica (Zaroogian 1980) and Saccostrea echinata (Burden-Jones and Denton 1984). Molluscs may accumulate Cd from littoral algae (Davies et al. 1991). The concentration of Cd in the present study is similar to the findings of Ahmed et al. (2009, 2010), Sarkar et al. (2002) and Bustamante et al. (2000). In molluscs (bivalves), the variations in Pb concentration ranged from 7.03 to 12.18 g/g in Dhaleswari River, Bangladesh (Ahmed et al. 2009), whereas, this range was 2.0219.69 g/g in molluscs from Bangladesh Sundarbans (Haque et al. 2006). These variations in Pb were evidently due to the seasonal changes and also to the influence of temperature and salinity (Zorba et al. 1992). The high Pb concentrations in the present investigation might be due to the discharge of various amounts of disposable solids, metal rust and lubricants from the scrapping of ships and industrial activities from Khulna and Mongla regions. Heavy metals such as copper (Cu), iron (Fe) and zinc (Zn) are essential for metabolism, whereas others, such as cadmium (Cd) and lead (Pb), do not play any role in biological systems (Diaz et al. 2006; Patra et al. 2006; Sprocati et al. 2006). Lead (Pb) is known to be readily absorbed in calcium carbonate skeletons. This accumulation is principally viewed as a detoxification mechanism. The WHO certified limits of Cd, Pb and Zn

Environ Monit Assess (2011) 177:505514

511

for marine fauna in wet weight basis is 0.5, 2.0 and 1,000.0 g/g, respectively (Kakulu et al. 1987). The higher bioaccumulation of Cd and Pb observed in the present investigation might be due to the ship breaking operations and industrial activities and discharges of various amounts of enriched toxic substances to the Sundarbans area. The certified values of Fe, Cu, Cd and Pb for the unpolluted marine sediments are 4,100, 33.0, 0.11 and 19.0 g/g, respectively (GESAMP 1982). In Sundarbans, Cd and Fe levels in sediment were beyond the limits but concentrations of other trace elements had exceeded the certified value given by GESAMP (1982) and Ahmed et al. (2003). The soil pH varies from 7.0 to 8.0 throughout the Sundarbans (Hussain and Acharya 1994). Some salts of heavy metals, such as copper, zinc and trivalent chromium, precipitate in weakly alkaline medium and thereby enlarge the silt deposits of the water body. The presence of these compounds, even relatively in low concentration, is harmful for aquatic biota. It is generally accepted that metals are taken up by aquatic biota in a passive process, down a concentration gradient into tissues (Simkiss and Taylor 1989). This can occur despite the presence of much higher concentrations of the elements in the tissues than in the external medium, as the metals in the tissues are bound to a wide range of biochemical sites (Manson et al. 1988). In few instances, uptake may also occur through ion pumps, and in these cases, energy dependence exists (Rainbow 1995). Many large and small rivers occupy about 30% of the Sundarbans, Bangladesh. The two rivers (Bhairab and Rupsha) carry water to Poshur and Shibsha which flows along the SRF and eventually flows to the Bay of Bengal (Ahmed et al. 2003). Baleshwar and Poshur rivers and their tributaries and distributaries are connected with the Ganges. As a result, these rivers and their tributaries receive flow of freshwater as well as pollutants from the Ganges. The Bhairab River has become an important artery receiving untreated water from industrial discharge. Khulna shipyard and fishprocessing unit discharge their effluent into the Rupsha River. Khulna newsprint mill, Goalpara power plant, jute, hardboard and steel mills also discharge their untreated wastes into Bhairab River (Ahmed et al. 2003). These pollutants find

there way to the SRF through the PoshurShibsha river system to well below Mongla Port, one of Bangladeshs major ports and is itself a significant source of water pollution. The port-based industries are established on the side of Poshur River. The maritime route of Mongla Port along Poshur River, which runs through SRF, is one of the sources of pollution. Oil pollution is reported to affect the SRF (Grepin 1995). The tidal current causes the quick transport and dispersion of pollutants in the mangrove area (Khan et al. 1998). Another important issue is the extent to which pollution from the Hugli River in India reaches the Sundarbans ecosystem. The regular flushing by tidal water had evidently taken most wastes out to sea. This implies that, with flood tides in the Sundarbans, there is a possibility that pollution discharged from the Hugli estuary into the sea could be carried far into the SRF. According to Vassiliki and Konstantina (1984), a BCF value of <1 is expected for most of the metals, otherwise bioaccumulation of metals by organisms will occur (Falusi and Olanipekun 2007). Cu, Pb and Zn had BCF values in the range of 0.02 to 0.15, which are considered safe as they are <1.00. BCF values of Fe exceeded this threshold and found to be ranging from 3.81 to 17.05 in all the macrobenthos, while BCF values of Cd exceeded the threshold in mud crab, mudskipper and gastropod. High BCF values for Fe and Cd indicate that these metals were highly bioaccumulated and biomagnified in the macrobenthic fauna of Sundarbans mangrove forest, Bangladesh. Higher heavy metal accumulations in macrobenthos refer to potential heavy metal pollution of Sundarbans benthic fauna. This information is crucial for the development of policies concerning the use and disposal of toxic material in the aquatic environment.

References
Ahmed, A. T. A. (1990). Studies on the identity and abundance of molluscan fauna of the Bay of Bengal (pp. 85). Contract Research Project, Bangladesh Agricultural Research Council, Bangladesh. Ahmed, M. K. (2000). An assessment of trace metal pollution in coastal areas of Bangladesh. Paper presented in the International Symposium held in Tokyo from

512 310 December 2000 on Coastal Pollution and Nutrient Cycles Organized by United Nations University. Ahmed, M. K., Ahmed, S., Rahman, S., Haque, M. R., & Islam, M. M. (2009). Heavy metal concentrations in water, sediments and their bio-accumulations in freshwater fishes and mussel in Dhaleswari River. Terrestrial and Aquatic Environmental Toxicology, 3(1), 3341. Ahmed, M. K., Bhowmik, A., Rahman, S., Haque, M. R., & Hasan, M. M. (2010). Heavy metal concentrations in water, sediments and their bio-accumulations in freshwater fishes and oyster in Shitalakhya River. Asian Journal of Water and Environmental Pollution, 7(1), 7790. Ahmed, M. K., Mehedi, M. Y., Hauqe, M. R., & Ahmed, F. (2002). Heavy metal concentration in water and sediment of Sundarbans mangrove forest, Bangladesh. Asian Journal of Microbiology Biotechology and Environmental Science, 4(2), 171179. Ahmed, M. K., Mehedi, M. Y., Hauqe, M. R., & Ghosh, R. K. (2003). Concentration of heavy metals in two upstream rivers sediment of the Sundarban mangrove forest. Asian Journal of Microbiology Biotechology and Environmental Science, 5(1), 4147. Banerjee, K., Mitra, A., Chakraborti, R., Das, A., & Mukherjee, D. (2006). Heavy metal concentrations in edible crab Scylla serrata in the Malancha region of India Sundarbans. In A. Kumar (Ed.), Heavy metal pollution research (pp. 210218). Delhi: Daya Publishing House. Bhattacharya, B., Sarkar, S. K., & Mukherjee, N. (2003). Organochlorine pesticide residues in sediments of a tropical mangrove estuary, India: Implications for monitoring. Environment International, 29, 587592. Biswas, S. K., Sharif, A. K. M., Alamgir, M., & Choudhury, D. A. (1998). Mercury level of some marine fishes from the Bay of Bengal. The Journal of NOAMI, 15(2), 15. Blower, J. (1985). Sundarbans forest inventory project, Bangladesh. Wildlife conservation in the Sundarbans (p. 39). Project Report 151, Overseas Development Administration, Land Resources Development Centre, Surbiton, UK. Burden-Jones, C., & Denton, G. W. (1984). Metals in marine organisms from the Great Barrier Reef Province. Final Report, Part 1, Baseline Survey, Department of Marine Biology, James Cook University, Townsville. Bustamante, P., Grigioni, S., Boucher-Rodoni, R., Caurant, F., & Miramand, P. (2000). Bioaccumulation of 12 trace elements in the tissues of nautilus Nautilus macromphalus from New Caledonia. Marine Pollution Bulletin, 40(8), 688696. Chaffey, D. R., Miller, F. R., & Sandom, J. H. (1985). A forest inventory of the Sundarbans, Bangladesh (pp. 196). Main report, Overseas Development Administration, England. Chakraborty, S. K., Chaudhury, A., & Deb, M. (1986). Decapod brachyura from Sunderban mangrove estuarine complex, India. Journal of Bengal Natural History Society, 5, 5568.

Environ Monit Assess (2011) 177:505514 Chaudhury, A., Das, A., Bhattacharya, S., & Bhunia, A. (1984). A quantitative assessment of benthic macrofauna in the intertidal mudflats of Sagar Island, Sunderban India (pp. 298310). In Proceedings of the Asian symposium on mangroves, environment research and management, Kuala Lumpur, Malaysia. Das, J. D., & Nolting, R. F. (1993). Distribution of trace metals in sediments and pore waters in the N. W. Mediterranean Sea. NIOZ (pp. 10). EROS-200 Project. Datta, D. K., & Subramanian, V. (1998). Distribution and fractionation of heavy metals in the surface sediments of the GangesBrahmaputraMeghna river system in the Bengal Basin. Environmental Geology, 36(1/2), 93101. Davies, C. A., Tomlinson, K., & Stephenson, T. (1991). Heavy metals in River Tees estuary sediments. Environmental Technology, 12, 961972. Diaz, S., Martin-Gonzalez, A., & Carlos Gutierrez, J. (2006). Evaluation of heavy metal acute toxicity and bioaccumulation in soil ciliated protozoa. Environment International, 32(6), 711717. Duarte, C. M. (2000). Marine biodiversity and ecosystem services: An elusive link. Journal of Experimental Marine Biology and Ecology, 250, 117131. FAO/UNDP (1998a). Integrated resource management plan of the Sundarbans Reserved Forest (Vol. 1, p. 323). Project BGD/84/056. FAO/UNDP (1998b). Appendices of the integrated resource management plan for the Sundarbans Reserved Forest (Vol. 2, p. 263). Project BGD/84/056. Falusi, B. A., & Olanipekun, E. O. (2007). Bioconcentration factors of heavy metals in tropical crab (Carcinus sp) from River Aponwe, Ado-Ekiti, Nigeria. Journal of Applied Sciences & Environmental Management, 11(4), 5154. Fitchko, J., & Hutchison, T. (1975). A comparative study of heavy metal concentration in river mouth sediments around the Great Lakes. Journal of Great Lakes Research, 1, 4678. GESAMP (1982). Joint group of experts on the scientific aspects of marine pollution, review of potentially harmful substancesCadmium, lead and tin. Rep. Stud. GESAMP, 22, 116 and UNEP Reg. Seas. Rep. Stud., 56, 85. Grepin, G. (1995). Mangrove ecology. Draft final report, FAO/UNDP Project BGD/84/056. Integrated resource development of the Sundarbans reserved forest, Khulna, Bangladesh. Haque, M. R., Ahmed, M. K., Ahmed, M. J. U., & Chowdhury, M. D. A. (2006). Heavy metal concentrations in some selected macro-benthic fauna of the Sundarbans mangrove forest, Bangladesh. Pakistan Journal of Oceanography, 2(2), 8198. Haque, M. R., Ahmad, J. U., Chowdhury, M. D. A., Ahmed, M. K., & Rahman, M. S. (2004). Seasonal variation of heavy metals concentration in sediments of the rivers and estuaries of Sundarban mangrove forest. Asian Journal of Microbiology, Biotechnology and Environmental Science, 6(2), 175185.

Environ Monit Assess (2011) 177:505514 Haque, M. R., Ahmad, J. U., Chowdhury, M. D. A., Ahmed, M. K., & Rahman, M. S. (2005). Seasonal variation of heavy metals concentration in surface water of the rivers and estuaries of Sundarban mangrove forest. Pollution Research, 24(2), 463472. Haque, M. R., Ullah, S. M., Ahmed, M. K., & Azad, M. S. (2003). Seasonal variation in physico-chemical parameters of water and sediment in the rivers of Sundarban mangrove forest. The Journal of NOAMI, 24(2), 463472. Holmgren, S. (1994). An environmental assessment of the Bay of Bengal region (pp.79112). BOBP/REP/67. Hussain, Z., & Acharya, G. (1994). Mangroves of the Sundarbans, Volume II: Bangladesh (pp. 257). Bangkok: IUCN. Jones, G. B., Mercurio, P., & Olivier, F. (2000). Zinc in fish, crabs, oysters and mangrove flora and fauna from Cleveland Bay. Marine Pollution Bulletin, 41(712), 345352. Kakulu, S. E., Osibanjo, O., & Ajayi, S. O. (1987). Trace metal contents of fish and shellfish of the Niger Delta area of Nigeria. Environment International, 13, 247 251. Khan, Y. S. A., Hossain, M. S., Hossain, S. M. G. A., & Halimuzzaman, A. H. M. (1998). An environment of trace metals in the GBM Estuary. Journal of Remote Sensing and Environment, 2, 103113. Manson, A. Z., Jenkins, K. D., & Sullivan, P. A. (1988). Mechanisms of trace metal accumulation in the polychaete Neanthes arenaceodentata. Journal of the Marine Biological Association of the United Kingdom, 68, 6180. Miramand, P., & Bentley, D. (1992). Heavy metal concentrations in two biological indicators (Patella vulgata and Fucas serratus) collected near the French nuclear fuel reprocessing plant of La Hague. Science of the Total Environment, 111, 135149. Mishra, A., Soota, T. D., & Chaudhury, A. (1983). On some polychaetes from Gangetic delta, West Bengal, India. Records of the Zoological Survey of India, 5, 4154. Mukherjee, S., Mukherjee, S., Bhattacharyya, P., & Duttagupta, A. K. (2004). Heavy metal levels and esterase variations between metal-exposed and unexposed duckweed Lemna minor: Field and laboratory studies. Environment International, 30(6), 811814. Naeem, S. (2006). Expanding scales in biodiversity-based research: Challenges and solutions for marine systems. Marine Ecology Progress Series, 311, 273283. Pez-Osuna, F., Osuna-Lpez, J. I., Izaguirre-Fierro, G., & Zazueta-Padilla, H. M. (1993). Heavy metals in clams from a subtropical coastal lagoon associated with an agricultural drainage basin. Bulletin of Environmental Contamination and Toxicology, 50, 915921. Patra, R. C., Swarup, D., Sharma, M. C., & Naresh, R. (2006). Trace mineral profile in blood and hair from cattle environmentally exposed to lead and cadmium around different industrial units. Journal of Veterinary Medicine. Series A, Animal Physiology, Pathology and Clinical Veterinary Medicine, 53(10), 511517.

513 Rainbow, P. S. (1995). Physiology, physicochemistry and metal uptakeA crustacean perspective. Marine Pollution Bulletin, 31, 5559. Saha, M., Sarkar, S. K., & Battacharya, B. (2006). Interspecific variation in heavy metal body concentrations in biota of Sunderban mangrove wetland, northeast India. Environment International, 32, 203207. Sarkar, S. K., Bhattacharya, B., Bandopadhaya, G., Giri, S., & Debnath, S. (1999). Tropical coastal organism as qualitative indicators of mercury and organomercury for sustainable use of living resources. Environment, Development and Sustainability, 1, 135147. Sarkar, S. K., Bhattacharya, B., Debnath, S., Bandopadhaya, G., & Giri, S. (2002). Heavy metals in biota from Sundarban wetland ecosystem, India: Implications to monitoring and environmental assessment. Aquatic Ecosystem Health & Management, 5(4), 467472. Seidensticker, J., & Hai, M. A. (1983). The Sundarbans wildlife management plan: Conservation in the Bangladesh coastal zone. IUCN (p. 120). Gland, Switzerland. Sharif, A. K. M., Alamgir, M., Mustafa, A. I., Hossain, M. A., & Amin, M. N. (1993b). Trace element concentration in ten species of freshwater fish of Bangladesh. Science of the Total Environment, 138(13), 177186. Sharif, A. K. M., Mustafa, A. I., Amin, N. M., & Shafiullah, S. (1991). Trace metals in tropical marine fish from the Bay of Bengal. Science of the Total Environment, 107, 135142. Sharif, A. K. M., Mustafa, A. I., Amin, N. M., & Shafiullah, S. (1993a). Lead and cadmium contents in ten species of tropical marine fish from the Bay of Bengal. Science of the Total Environment, 133, 193199. Simkiss, K., & Taylor, M. G. (1989). Metal fluxes across the membranes of aquatic organisms. Review of Aquatic Science, 1, 173188. Sprocati, A. R., Alisi, C., Segre, L., Tasso, F., Galletti, M., & Cremisini, C. (2006). Investigating heavy metal resistance, bioaccumulation and metabolic profile of a metallophile microbial consortium native to an abandoned mine. Science of the Total Environment, 366(2 3), 649658. Subba Rao, N. V., Dey, A. & Barua, S. (1983). Studies on the malacofauna of Mooriganga estuary, Sunderban, West Bengal. Bulletin of the Zoological Survey of India, 5, 4756. Tilzer, M. M., & Khondker, M. (1993). Hypertrophic and polluted freshwater ecosystems: Ecological basis for water resource management (pp. 9196). Department of Botany, Dhaka University, Bangladesh. Tsangaris, C., Papathanasiou, E., & Cotou, E. (2007). Assessment of the impact of heavy metal pollution from a ferro-nickel smelting plant using biomarkers. Ecotoxicology and Environmental Safety, 66(2), 232243. UNEP/FAO/IAEA/IOC (1984). Sampling of selected marine organisms and sample preparation for trace metal analysis. Reference method for marine pollution studies No 7 Rev 2. Vassiliki, K., & Konstantina, A. D. (1984). Transfer factors of heavy metals in aquatic organisms of different

514 trophic levels. Bulletin of Environmental Contamination and Toxicology. Zaroogian, G. E. (1980). Crassostrea virginica as an indicator of cadmium pollution. Marine Biology, 58, 275 284.

Environ Monit Assess (2011) 177:505514 Zorba, M. A., Jacob, P. G., Al-Bloushi, A., & Al-Nafisi, R. (1992). Clams as pollution bioindicators in Kuwaits marine environment: Metal accumulation and depuration. Science of the Total Environment, 120(3), 185 204.