heavy metal concentrations in some macrobenthic fauna

Environ Monit Assess (2011) 177:505–514DOI 10.1007/s10661-010-1651-9

Heavy metal concentrations in some macrobenthic faunaof the Sundarbans mangrove forest, south west coastof 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 somemacrobenthic fauna have been reported for thefirst time from the Sundarbans mangrove forest,south west coast of Bangladesh, in the northernpart of Bay of Bengal. The concentration of Fe,Cu, Zn, Cd and Pb in macrobenthos ranged from235 ± 10.11 to 1,051 ± 38.42, 3.66 ± 0.89 to7.55 ± 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 μg/g, respectively. Significant variations (p ≤0.05) in heavy metal concentrations have beenobserved among the mud crab, mudskipper andgastropod. However, heavy metal burdens did notvary significantly among the hermit and horseshoecrabs. In mud crab, horseshoe crab and gastropod,heavy metal concentrations were recorded in thesequence: Fe > Zn > Pb > Cu > Cd. Hermitcrab and mudskipper contained heavy metals inthe order of Fe > Zn > Cu > Pb > Cd. Fe and Zn

K. Ahmed (B)Department of Fisheries,University of Dhaka,Dhaka 1000, Bangladeshe-mail: [email protected]

Y. Mehedi · R. Haque · P. MondolFisheries and Marine Resource Technology Discipline,Khulna University, Khulna 9208, Bangladesh

concentrations were found significantly (p ≤0.05) higher in macrobenthos. The lead (Pb) con-centration found in the edible portion of mac-robenthos exceeded the international permissiblelimits certified by the WHO. Bioconcentrationfactors >1.00 obtained for Fe (17.05 in mudskip-per) and Cd (1.87 in gastropod) indicated thatthese metals were highly bioaccumulated and bio-magnified in benthic fauna of Sundarbans. Thefindings of this study refer to the potential impactof heavy metals in the mangrove ecosystem ofBangladesh.

Keywords Heavy metals · Macrobenthos ·Bioaccumulation · Sundarbans mangrove forest

Introduction

The Sundarbans mangrove forest, covering about10,000 km2 of land and water, is a part ofthe world’s largest delta (80,000 km2) formedfrom sediments deposited by three great rivers—the Ganges, Brahmaputra and Meghna (GMB,Seidensticker and Hai 1983). Mangrove is oneof the biologically productive natural ecosystems(Blower 1985). The coastal area of Bangladeshis suitable for molluscan habitats (Ahmed 1990)and it is documented that the intertidal belt ofthe Sundarbans Reserve Forest (SRF) supports

506 Environ Monit Assess (2011) 177:505–514

diverse macrobenthic fauna (Mishra et al. 1983;Subba Rao et al. 1983; Chaudhury et al. 1984;Chakraborty et al. 1986). Sediments of the GMBriver system in the Bengal Basin have the poten-tial to trap contaminants because of their grainsize and mineralogy (Haque et al. 2006). Amongthe contaminants, the accumulation of toxic met-als to hazardous levels in aquatic biota has be-come a problem of increasing concern (Mukherjeeet al. 2004; Tsangaris et al. 2007). Heavy metals,being non-biodegradable, can accumulate in thefood chain, producing their toxic effects at pointsafter being removed far away from the source ofpollution (Tilzer and Khondker 1993). Even atvery low sub-lethal concentrations, certain heavymetals can seriously hamper the basic metabolicfunctions of life.

Several researchers (Sarkar et al. 1999, 2002;Bhattacharya et al. 2003) have reported the bioac-cumulation of heavy metals in some biota of Hugliestuary, India. Studies on aquatic pollution, par-ticularly in marine ecosystems, have received rel-atively less attention (Duarte 2000; Naeem 2006).To date, in Bangladesh, a few attempts havebeen made to study the heavy metal pollutionin the coastal and mangrove areas. However, inBangladesh, tests to measure the levels of thepresence of few heavy metals in some marinefishes of the Bay of Bengal have been carriedout (Sharif et al. 1991, 1993a, b). The texture,mineralogy of sediments and distribution of heavymetals in the surface sediments from the GMBriver system have been reported by Datta andSubramanian (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 inves-tigate the concentrations of heavy metals in thewater and sediments of Sundarbans mangrove for-est. However, to date, except Haque et al. (2006),no research work has been carried out on theheavy metal concentrations in benthic fauna inthe rivers and estuaries of Sundarbans mangroveforest, Bangladesh. In view of this, the presentstudy has been carried out to investigate the con-centrations and bioconcentration factors (BCF) ofheavy metals in some macrobenthic fauna of theSundarbans mangrove forest, Bangladesh.

Materials and methods

Study area

The Sundarbans mangrove forest (89◦00′ and89◦55′ E and 21◦30′ and 22◦30′ N) is locatedin the estuary of the river Ganges in southwestBangladesh and the south-western region of theState of West Bengal in India. The forest meetsthe Bay of Bengal in the south. The forest coversan area of 577,000 ha (70%) of which 401,600 hais land and the remaining 175,600 ha are underwater in the form of rivers, canals and creekswith width varying from a few meters to sev-eral kilometers. Some of these are purely tidalin nature and not connected with any source offreshwater. Most creeks and canals flow into thelarge rivers which are interconnected (Chaffeyet al. 1985). Recently, the Sundarbans mangroveforest has been declared as a UNESCO worldheritage site and a management plan has beenmade 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 Sundarbansmangrove forest (Fig. 1). It is the estuarycircumscribed by the Sundarbans and formedby the rivers Passur and Shibsa and is located87 km away from the Mongla Port. It is a veryimportant point for ecological studies because theinland and on-shore water flows are crisscrossed,ultimately inundating the Sundarbans mangroveforest.

Samples were collected from the intertidal zoneduring low tides and only shallow water mac-robenthos of the continental shelf were consid-ered. Samples were collected by cast net andalso from the fishermen while they were catch-ing crabs by using bait. Different macrobenthossamples and their average lengths are given inTable 1. Samples were preserved according toUNEP/FAO/IAEA/IOC (1984). After collectionof the samples, mud and other organisms wereremoved by washing them with sea water at the

Environ Monit Assess (2011) 177:505–514 507

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

sampling site. Samples were kept overnight in asea water tank for defaecation.

Analytical procedure

The softer parts of the body of the samples wereseparated and dried at room temperature andweighted. After washing, the samples were driedin an oven at 55◦C to an anhydrous state untila constant weight was obtained. The dried sam-ples were then ground with the help of a glassmortar and sieved thoroughly to produce a ho-mogeneous powder. The powdered samples werefinally stored in bottles and preserved in desicca-tors for further analysis.

One gram of each powdered sample was keptin 50-ml Pyrex beaker and placed in the mufflefurnace at 50◦C, 450◦C and 550◦C for 10 min, 1 hand 8 h, respectively, by raising the temperaturefor complete ashing. Ashed samples were thendigested with 2 ml of concentrated HNO3 on awater 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 ineach beaker and heated for sometime. Then, 3 mlof deionized water were added and warmed ona water bath for a few minutes. Blank digestionwas also made to quantify possible contamination.After cooling, the digested samples, along withthe blanks, were filtered by using filter paper(Whatman 541) and made the filtrate up to 10 mlwith deionized water. Prior to analysis, severaldilutions of the digested samples were made.

Table 1 Average length (in centimeters) of macrobenthosstudied

Macrobenthos Average length (cm)

Gastropod (Assiminea brevicula) 0.045Hermit crab (Eupagurus sp.) 2.50Mud skipper (Gobius boddarti) 16Mud crabs (Scylla serrata) 15Horseshoe crabs 30

(Carcinoscorpius rotundicauda)


0200400600800

10001200

HermitCrab

HorseshoeCrab

Mud Crab Gastropod MudSkipper

Fe (

µg g

-1)

Fig. 2 Iron (Fe) concentration (mean ± SD) in the studiedmacrobenthos

The quantitative measurement of Fe, Cu, Zn,Pb and Cd were carried out using air–acetyleneflame with a combination of single-element hol-low cathode lamps and Perkin Elmer 560 AtomicAbsorption Spectrophotometer at the ChemistryDivision, Atomic Energy Center, Dhaka. Thestandard solution of the elements Fe, Cu, Zn, Pband Cd was procured from Fisher Scientific Com-pany, USA. The standard solution was preparedbefore each analysis. The analytical quality of thework was checked by analysis of standard ref-erence materials NBS-SRM-1573, tomato leaves,and NBS-SRM-1566, oyster tissue, prepared bythe National Bureau of Standards, Washington,DC, USA. The analytical procedures were alsocalibrated against the above standard referencematerials. The average recovery ranged between94% and 107%.

The BCF of the heavy metals in the macroben-thos samples were obtained as worked out byVassiliki and Konstantina (1984) and Falusiand Olanipekun (2007) by using the followingformula:

BCF = Corg/

Csed

0

2

4

6

8

10

HermitCrab

HorseshoeCrab

Mud Crab Gastropod MudSkipper

Cu

(µg

g-1)

Fig. 3 Cupper (Cu) concentration (mean ± SD) in thestudied macrobenthos

where BCF is the bioconcentration factor, Corg isthe concentration of metal in the organism andCsed is the concentration of the same metal in theambient environment (i.e. sediment).

Statistical analysis

Statistical comparison among means was per-formed by univariate analysis by SPSS softwareversion 12.0 (SPSS Inc., Chicago, IL, USA).Differences were significant at p ≤ 0.05.

Results

Iron (Fe) content in mudskipper was highest(1,051 ± 38.42 μg/g) and lowest in gastropod(235 ± 10.11 μg/g) among the five macrobenthosstudied (Fig. 2). The concentration of Fe observedin mud crab was 595.29 ± 25.72 μg/g, in horseshoecrab was 480.66 ± 22.54 μg/g and in hermit crabwas 375 ± 17.23 μg/g. Among the five benthos,hermit crab contained the highest Cu (7.55 ±1.29 μg/g) and gastropod contained the lowest(3.66 ± 0.89 μg/g). Cu content in mud crab andin horseshoe crab was 6.28 ± 2.13 and 5.66 ±1.36 μg/g, respectively, and in mudskipper, it wasrecorded to be higher (7.23 ± 1.1 μg/g) than incrabs (Fig. 3). Another essential trace elementZn content was observed highest in gastropod(110 ± 8.82 μg/g) and lowest (76.8 ± 8.55 μg/g) inhorseshoe crab. Among the rest, the mudskippercontained the highest (98.5 ± 6.49 μg/g) followedby the hermit crab (95.5 ± 5.25 μg/g) and mud crab(85.5 ± 9.27 μg/g; Fig. 4).

The highest concentration of cadmium (Cd)was recorded in gastropod (0.859 ± 0.2 μg/g)

0

50

100

150

Hermit

Crab

Horseshoe

Crab

Mud Crab Gastropod Mud

Skipper

Zn

(µg

g-1)

Fig. 4 Zinc (Zn) concentration (mean ± SD) in thestudied macrobenthos


00.20.40.60.8

11.2

Cd

(µg

g-1)

Hermit

Crab

Horseshoe

Crab


Skipper

Fig. 5 Cadmium (Cd) concentration (mean ± SD) in thestudied macrobenthos

and the lowest was in horseshoe crabs (0.46 ±0.11 μg/g), whereas, in mudskipper, mud crab andhermit crab, it was 0.725 ± 0.21, 0.551 ± 0.13 and0.462 ± 0.12 μg/g, respectively (Fig. 5). Besides,in mud crabs, lead (Pb) content was the highest(6.77 ± 2.1 μg/g) and the lowest was recordedin hermit crab (4.66 ± 1.17 μg/g). However, thehorseshoe crab (5.8 ± 1.99 μg/g) and gastropods(6.5 ± 0.74 μg/g) contained higher Pb than that ofthe mudskipper (4.99 ± 0.82 μg/g; Fig. 6).

The metal concentrations varied within thesame species. Fe content was highest among allthe five metals irrespective of species, whereas Cdcontent was lowest in the horseshoe crab (0.46 ±0.11 μg/g). In mud crab, horseshoe crab and gas-tropod, metal concentrations were found in theorder of Fe > Zn > Pb > Cu > Cd, and in thehermit 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 mac-robenthos and the highest value was observed inmudskipper (17.05).

0

2

4

6

8

10

Pb (

µg g

-1)

Hermit

Crab

Horseshoe

Crab


Skipper

Fig. 6 Lead (Pb) concentration (mean ± SD) in thestudied macrobenthos

Discussion

The coastal region of the Bay of Bengal is apotential area of heavy metal pollution as it is thepoint of discharge for majority of the rivers of thesubcontinent that carry industrial effluents andwastes to the sea. Sediments may act as indicatorsof heavy metal burden in a coastal environment,as they are the principal reservoir for heavy metals(Fitchko and Hutchison 1975). Mangroves act assediment trap and hence mangrove macrobenthosare susceptible to potential heavy metal pollution.Fe content in molluscs (gastropods) from the Sun-darbans mangrove forest varied from 224.0 ± 37to 485.3 ± 339 μg/g (Haque et al. 2006). Fe con-tent in molluscs from New Caledonia was foundto be 258 ± 79 μg/g (Bustamante et al. 2000).The average concentration of Fe in molluscs was1,338 μg/g (Páez-Osuna et al. 1993). Fe content ingastropods of Sundarbans mud flat of India washighest among the heavy metals and it varied sea-sonally from 442 to 1,216 μg/g dry weight (Sarkaret al. 2002). The findings of the present studyconform to the above studies. The highest con-centration of Fe found in the present study mightbe due to ship breaking and repairing activities ofKhulna Shipyard and boat and barge building andrepairing activities of Khalishpur, Bangladesh.

In Kuwait’s marine environment, the highestconcentration of Cu (12.5 μg/g) was observed inclams as sediment of that region is enriched withthis pollutant (Zorba et al. 1992). The concentra-tion of Cu fluctuates seasonally within the rangeof 3.0 to 6.6 μg/g in Patella sp. and 0.8 to 2.0 μg/gin Fucus sp. (Miramand and Bentley 1992). Cuconcentration in molluscs (bivalves) from theDhaleswari and Shitalakhya rivers, Bangladeshwere reported to vary seasonally from 7.55 to11.5 and 5.47 to 8.19 μg/g, respectively (Ahmedet al. 2009, 2010). Seasonal variations of Cu inmolluscs of Sundarbans were moderate and theconcentrations were high during the winter seasonwith the maximum mean concentration (38.51 ±15 μg/g) found downstream (Haque et al. 2006).Higher concentration of Cu (185 μg/g dry weight)was reported in gastropods of Sagar Island, India(Sarkar et al. 2002), whereas much lower con-centration of Cu in different tissues in bivalve(Marcia pinguis) was reported from the same


Table 2 Bioconcentration factor (BCF) of heavy metals in macrobenthos

Sediment Hermit crab Horseshoe crab Mud crab Gastropod Mud skipper

BC BCF BC BCF BC BCF BC BCF BC BCF

Fe 61.66a 375 6.08 480.66 7.80 595.29 9.65 235 3.81 1,051 17.05Cu 129.8a 7.55 0.06 5.66 0.04 6.28 0.05 3.66 0.03 7.23 0.06Zn 730b 95.5 0.13 76.8 0.11 85.5 0.12 110 0.15 98.5 0.13Cd 0.46b 0.462 1.00 0.46 1.00 0.551 1.20 0.859 1.87 0.725 1.58Pb 300b 4.66 0.02 5.8 0.02 6.77 0.02 6.5 0.02 4.99 0.02

BC heavy metal concentration in the body (in microgram per gram), BCF bioconcentration factoraAhmed et al. (2002)bAhmed et al. (2003)

location (Saha et al. 2006). In mud crab (Scyllaserrata), highest Cu (341.04 μg/g) content was re-ported from Malanch region of Indian Sundarbans(Banerjee et al. 2006). Cu concentrations foundin the macrobenthos of Bangladesh Sundarbanswere lower than those of the Indian Sundarbans.The enrichment of Cu in macrobenthic faunamight be due to the offshore input of Cu in waterand sediments. Cu is intimately related to theaerobic degradation of organic matter (Das andNolting 1993). High litter falls in mangroves andtheir degradation might cause the high level of Cuaccumulation in the macrobenthos.

The average concentration of Zn in mangrovemolluscs (Nerita lineata) in Cleveland Bay was50 μg/g (Jones et al. 2000). The concentration ofZn in sediment and water was found to be 80.6to 730 μg/g and 0.002 to 0.154 μg/L, respectively,in upstream river of Sundarbans mangrove forest(Ahmed et al. 2003). The concentration of Znin molluscs from the Basundia and Hironpoint,Bangladesh were 29.32 ± 7.0 and 28.79 ± 6.7 μg/g,respectively (Haque et al. 2006). In S. serrata fromSundarbans mangrove forest, India, the highestconcentration of Zn was found to be 648.29 μg/g(Banerjee et al. 2006). In gastropods, Zn con-centration is reported to vary seasonally from 55to185 μg/g in the Indian Sundarbans (Sarkar et al.2002). In the present study, the concentrations ofZn conform to the above findings.

Cd concentration in molluscs (bivalves)seasonally varied from 0.52 to 0.8 μg/g from theDhaleswari River and from 1.09 to 1.21 μg/g fromthe Shitalakhya River, Bangladesh (Ahmed et al.2009, 2010). The mean concentration of Cd inmolluscs from New Caledonia was 16 ± 6.5 μg/g(Bustamante et al. 2000). Seasonal and inter-

species variations in Cd concentrations (belowdetectable level to 80 μg/g) of gastropods werereported from Indian Sundarbans (Sarkar et al.2002). Accumulation of Cd in clam (0.18 to0.32 μg/g) was reported to depend on thebioavailability of Cd in sea water and sediment(Zorba et al. 1992). Cd uptake rate increases withtemperature and low salinity in Crassotrea viginica(Zaroogian 1980) and Saccostrea echinata(Burden-Jones and Denton 1984). Molluscs mayaccumulate Cd from littoral algae (Davies et al.1991). The concentration of Cd in the presentstudy is similar to the findings of Ahmed et al.(2009, 2010), Sarkar et al. (2002) and Bustamanteet al. (2000).

In molluscs (bivalves), the variations in Pbconcentration ranged from 7.03 to 12.18 μg/gin Dhaleswari River, Bangladesh (Ahmed et al.2009), whereas, this range was 2.02–19.69 μg/gin molluscs from Bangladesh Sundarbans (Haqueet al. 2006). These variations in Pb were evi-dently due to the seasonal changes and also to theinfluence of temperature and salinity (Zorba et al.1992). The high Pb concentrations in the presentinvestigation might be due to the discharge of var-ious amounts of disposable solids, metal rust andlubricants from the scrapping of ships and indus-trial 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 absorbedin calcium carbonate skeletons. This accumulationis principally viewed as a detoxification mecha-nism. The WHO certified limits of Cd, Pb and Zn


for marine fauna in wet weight basis is 0.5, 2.0 and1,000.0 μg/g, respectively (Kakulu et al. 1987). Thehigher bioaccumulation of Cd and Pb observed inthe present investigation might be due to the shipbreaking operations and industrial activities anddischarges of various amounts of enriched toxicsubstances to the Sundarbans area.

The certified values of Fe, Cu, Cd and Pbfor the unpolluted marine sediments are 4,100,33.0, 0.11 and 19.0 μg/g, respectively (GESAMP1982). In Sundarbans, Cd and Fe levels in sedi-ment were beyond the limits but concentrationsof other trace elements had exceeded the certifiedvalue given by GESAMP (1982) and Ahmed et al.(2003). The soil pH varies from 7.0 to 8.0 through-out the Sundarbans (Hussain and Acharya 1994).Some salts of heavy metals, such as copper, zincand trivalent chromium, precipitate in weakly al-kaline medium and thereby enlarge the silt de-posits of the water body. The presence of thesecompounds, even relatively in low concentration,is harmful for aquatic biota. It is generally ac-cepted that metals are taken up by aquatic biota ina passive process, down a concentration gradientinto tissues (Simkiss and Taylor 1989). This canoccur despite the presence of much higher con-centrations of the elements in the tissues than inthe external medium, as the metals in the tissuesare bound to a wide range of biochemical sites(Manson et al. 1988). In few instances, uptake mayalso 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 andShibsha which flows along the SRF and eventuallyflows to the Bay of Bengal (Ahmed et al. 2003).Baleshwar and Poshur rivers and their tributariesand distributaries are connected with the Ganges.As a result, these rivers and their tributaries re-ceive flow of freshwater as well as pollutants fromthe Ganges. The Bhairab River has become animportant artery receiving untreated water fromindustrial discharge. Khulna shipyard and fish-processing unit discharge their effluent into theRupsha River. Khulna newsprint mill, Goalparapower plant, jute, hardboard and steel mills alsodischarge their untreated wastes into BhairabRiver (Ahmed et al. 2003). These pollutants find

there way to the SRF through the Poshur–Shibshariver system to well below Mongla Port, one ofBangladesh’s major ports and is itself a significantsource of water pollution. The port-based indus-tries are established on the side of Poshur River.The maritime route of Mongla Port along PoshurRiver, which runs through SRF, is one of thesources of pollution. Oil pollution is reported toaffect the SRF (Grepin 1995). The tidal currentcauses the quick transport and dispersion of pol-lutants in the mangrove area (Khan et al. 1998).Another important issue is the extent to whichpollution from the Hugli River in India reachesthe Sundarbans ecosystem. The regular flushingby tidal water had evidently taken most wastes outto sea. This implies that, with flood tides in theSundarbans, there is a possibility that pollutiondischarged from the Hugli estuary into the seacould be carried far into the SRF.

According to Vassiliki and Konstantina (1984),a BCF value of <1 is expected for most ofthe metals, otherwise bioaccumulation of metalsby organisms will occur (Falusi and Olanipekun2007). Cu, Pb and Zn had BCF values in therange of 0.02 to 0.15, which are considered safeas they are <1.00. BCF values of Fe exceededthis threshold and found to be ranging from 3.81to 17.05 in all the macrobenthos, while BCF val-ues of Cd exceeded the threshold in mud crab,mudskipper and gastropod. High BCF values forFe and Cd indicate that these metals were highlybioaccumulated and biomagnified in the mac-robenthic fauna of Sundarbans mangrove forest,Bangladesh. Higher heavy metal accumulationsin macrobenthos refer to potential heavy metalpollution of Sundarbans benthic fauna. This infor-mation is crucial for the development of policiesconcerning the use and disposal of toxic materialin the aquatic environment.

References

Ahmed, A. T. A. (1990). Studies on the identity and abun-dance of molluscan fauna of the Bay of Bengal (pp. 85).Contract Research Project, Bangladesh AgriculturalResearch Council, Bangladesh.

Ahmed, M. K. (2000). An assessment of trace metal pollu-tion in coastal areas of Bangladesh. Paper presentedin the International Symposium held in Tokyo from


3–10 December 2000 on “Coastal Pollution and Nutri-ent Cycles” Organized by United Nations University.

Ahmed, M. K., Ahmed, S., Rahman, S., Haque, M. R.,& Islam, M. M. (2009). Heavy metal concentrationsin water, sediments and their bio-accumulations infreshwater fishes and mussel in Dhaleswari River. Ter-restrial and Aquatic Environmental Toxicology, 3(1),33–41.

Ahmed, M. K., Bhowmik, A., Rahman, S., Haque, M. R.,& Hasan, M. M. (2010). Heavy metal concentrations inwater, sediments and their bio-accumulations in fresh-water fishes and oyster in Shitalakhya River. AsianJournal of Water and Environmental Pollution, 7(1),77–90.

Ahmed, M. K., Mehedi, M. Y., Hauqe, M. R., & Ahmed,F. (2002). Heavy metal concentration in water andsediment of Sundarbans mangrove forest, Bangladesh.Asian Journal of Microbiology Biotechology and Envi-ronmental Science, 4(2), 171–179.

Ahmed, M. K., Mehedi, M. Y., Hauqe, M. R., & Ghosh,R. K. (2003). Concentration of heavy metals in twoupstream rivers sediment of the Sundarban mangroveforest. Asian Journal of Microbiology Biotechologyand Environmental Science, 5(1), 41–47.

Banerjee, K., Mitra, A., Chakraborti, R., Das, A., &Mukherjee, D. (2006). Heavy metal concentrations inedible crab Scylla serrata in the Malancha region ofIndia Sundarbans. In A. Kumar (Ed.), Heavy metalpollution research (pp. 210–218). Delhi: Daya Publish-ing House.

Bhattacharya, B., Sarkar, S. K., & Mukherjee, N. (2003).Organochlorine pesticide residues in sediments ofa tropical mangrove estuary, India: Implications formonitoring. Environment International, 29, 587–592.

Biswas, S. K., Sharif, A. K. M., Alamgir, M., & Choudhury,D. A. (1998). Mercury level of some marine fishesfrom the Bay of Bengal. The Journal of NOAMI,15(2), 1–5.

Blower, J. (1985). Sundarbans forest inventory project,Bangladesh. Wildlife conservation in the Sundar-bans (p. 39). Project Report 151, Overseas Develop-ment Administration, Land Resources DevelopmentCentre, Surbiton, UK.

Burden-Jones, C., & Denton, G. W. (1984). Metals in ma-rine organisms from the Great Barrier Reef Province.Final Report, Part 1, Baseline Survey, Department ofMarine Biology, James Cook University, Townsville.

Bustamante, P., Grigioni, S., Boucher-Rodoni, R.,Caurant, F., & Miramand, P. (2000). Bioaccumulationof 12 trace elements in the tissues of nautilus Nautilusmacromphalus from New Caledonia. Marine PollutionBulletin, 40(8), 688–696.

Chaffey, D. R., Miller, F. R., & Sandom, J. H. (1985). A for-est inventory of the Sundarbans, Bangladesh (pp. 196).Main report, Overseas Development Administration,England.

Chakraborty, S. K., Chaudhury, A., & Deb, M. (1986). De-capod brachyura from Sunderban mangrove estuarinecomplex, India. Journal of Bengal Natural History So-ciety, 5, 55–68.

Chaudhury, A., Das, A., Bhattacharya, S., & Bhunia, A.(1984). A quantitative assessment of benthic macro-fauna in the intertidal mudflats of Sagar Island, Sun-derban India (pp. 298–310). In Proceedings of theAsian symposium on mangroves, environment researchand management, Kuala Lumpur, Malaysia.

Das, J. D., & Nolting, R. F. (1993). Distribution oftrace metals in sediments and pore waters in the N.W. Mediterranean Sea. NIOZ (pp. 10). EROS-200Project.

Datta, D. K., & Subramanian, V. (1998). Distribution andfractionation of heavy metals in the surface sedimentsof the Ganges–Brahmaputra–Meghna river system inthe Bengal Basin. Environmental Geology, 36(1/2),93–101.

Davies, C. A., Tomlinson, K., & Stephenson, T. (1991).Heavy metals in River Tees estuary sediments. Envi-ronmental Technology, 12, 961–972.

Diaz, S., Martin-Gonzalez, A., & Carlos Gutierrez, J.(2006). Evaluation of heavy metal acute toxicity andbioaccumulation in soil ciliated protozoa. Environ-ment International, 32(6), 711–717.

Duarte, C. M. (2000). Marine biodiversity and ecosystemservices: An elusive link. Journal of Experimental Ma-rine Biology and Ecology, 250, 117–131.

FAO/UNDP (1998a). Integrated resource managementplan of the Sundarbans Reserved Forest (Vol. 1, p.323). Project BGD/84/056.

FAO/UNDP (1998b). Appendices of the integrated resourcemanagement plan for the Sundarbans Reserved Forest(Vol. 2, p. 263). Project BGD/84/056.

Falusi, B. A., & Olanipekun, E. O. (2007). Bioconcentra-tion factors of heavy metals in tropical crab (Carcinussp) from River Aponwe, Ado-Ekiti, Nigeria. Journalof Applied Sciences & Environmental Management,11(4), 51–54.

Fitchko, J., & Hutchison, T. (1975). A comparative study ofheavy metal concentration in river mouth sedimentsaround the Great Lakes. Journal of Great Lakes Re-search, 1, 46–78.

GESAMP (1982). Joint group of experts on the scien-tific aspects of marine pollution, review of potentiallyharmful substances—Cadmium, lead and tin. Rep.Stud. GESAMP, 22, 116 and UNEP Reg. Seas. Rep.Stud., 56, 85.

Grepin, G. (1995). Mangrove ecology. Draft finalreport, FAO/UNDP Project BGD/84/056. Integratedresource development of the Sundarbans reservedforest, Khulna, Bangladesh.

Haque, M. R., Ahmed, M. K., Ahmed, M. J. U., &Chowdhury, M. D. A. (2006). Heavy metal concentra-tions in some selected macro-benthic fauna of the Sun-darbans mangrove forest, Bangladesh. Pakistan Jour-nal of Oceanography, 2(2), 81–98.

Haque, M. R., Ahmad, J. U., Chowdhury, M. D. A.,Ahmed, M. K., & Rahman, M. S. (2004). Seasonalvariation of heavy metals concentration in sedimentsof the rivers and estuaries of Sundarban mangroveforest. Asian Journal of Microbiology, Biotechnologyand Environmental Science, 6(2), 175–185.


Haque, M. R., Ahmad, J. U., Chowdhury, M. D. A.,Ahmed, M. K., & Rahman, M. S. (2005). Seasonalvariation of heavy metals concentration in surface wa-ter of the rivers and estuaries of Sundarban mangroveforest. Pollution Research, 24(2), 463–472.

Haque, M. R., Ullah, S. M., Ahmed, M. K., & Azad, M. S.(2003). Seasonal variation in physico-chemical para-meters of water and sediment in the rivers of Sundar-ban mangrove forest. The Journal of NOAMI, 24(2),463–472.

Holmgren, S. (1994). An environmental assessment of theBay of Bengal region (pp.79–112). BOBP/REP/67.

Hussain, Z., & Acharya, G. (1994). Mangroves of the Sun-darbans, Volume II: Bangladesh (pp. 257). Bangkok:IUCN.

Jones, G. B., Mercurio, P., & Olivier, F. (2000). Zinc infish, crabs, oysters and mangrove flora and fauna fromCleveland Bay. Marine Pollution Bulletin, 41(7–12),345–352.

Kakulu, S. E., Osibanjo, O., & Ajayi, S. O. (1987). Tracemetal contents of fish and shellfish of the Niger Deltaarea 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 oftrace metals in the GBM Estuary. Journal of RemoteSensing and Environment, 2, 103–113.

Manson, A. Z., Jenkins, K. D., & Sullivan, P. A. (1988).Mechanisms of trace metal accumulation in the poly-chaete Neanthes arenaceodentata. Journal of the Ma-rine Biological Association of the United Kingdom, 68,61–80.

Miramand, P., & Bentley, D. (1992). Heavy metal concen-trations in two biological indicators (Patella vulgataand Fucas serratus) collected near the French nuclearfuel reprocessing plant of La Hague. Science of theTotal Environment, 111, 135–149.

Mishra, A., Soota, T. D., & Chaudhury, A. (1983). Onsome polychaetes from Gangetic delta, West Bengal,India. Records of the Zoological Survey of India, 5,41–54.

Mukherjee, S., Mukherjee, S., Bhattacharyya, P., &Duttagupta, A. K. (2004). Heavy metal levels and es-terase variations between metal-exposed and unex-posed duckweed Lemna minor: Field and laboratorystudies. Environment International, 30(6), 811–814.

Naeem, S. (2006). Expanding scales in biodiversity-basedresearch: Challenges and solutions for marine systems.Marine Ecology Progress Series, 311, 273–283.

Páez-Osuna, F., Osuna-López, J. I., Izaguirre-Fierro, G., &Zazueta-Padilla, H. M. (1993). Heavy metals in clamsfrom a subtropical coastal lagoon associated with anagricultural drainage basin. Bulletin of EnvironmentalContamination and Toxicology, 50, 915–921.

Patra, R. C., Swarup, D., Sharma, M. C., & Naresh, R.(2006). Trace mineral profile in blood and hair fromcattle environmentally exposed to lead and cadmiumaround different industrial units. Journal of VeterinaryMedicine. Series A, Animal Physiology, Pathology andClinical Veterinary Medicine, 53(10), 511–517.

Rainbow, P. S. (1995). Physiology, physicochemistry andmetal uptake—A crustacean perspective. Marine Pol-lution Bulletin, 31, 55–59.

Saha, M., Sarkar, S. K., & Battacharya, B. (2006). Inter-specific variation in heavy metal body concentrationsin biota of Sunderban mangrove wetland, northeastIndia. Environment International, 32, 203–207.

Sarkar, S. K., Bhattacharya, B., Bandopadhaya, G., Giri,S., & Debnath, S. (1999). Tropical coastal organism asqualitative indicators of mercury and organomercuryfor sustainable use of living resources. Environment,Development and Sustainability, 1, 135–147.

Sarkar, S. K., Bhattacharya, B., Debnath, S., Bandopad-haya, G., & Giri, S. (2002). Heavy metals in biota fromSundarban wetland ecosystem, India: Implications tomonitoring and environmental assessment. AquaticEcosystem Health & Management, 5(4), 467–472.

Seidensticker, J., & Hai, M. A. (1983). The Sundar-bans wildlife management plan: Conservation in theBangladesh 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 concentra-tion in ten species of freshwater fish of Bangladesh.Science of the Total Environment, 138(1–3), 177–186.

Sharif, A. K. M., Mustafa, A. I., Amin, N. M., & Shafiullah,S. (1991). Trace metals in tropical marine fish from theBay of Bengal. Science of the Total Environment, 107,135–142.

Sharif, A. K. M., Mustafa, A. I., Amin, N. M., & Shafiullah,S. (1993a). Lead and cadmium contents in ten speciesof tropical marine fish from the Bay of Bengal. Scienceof the Total Environment, 133, 193–199.

Simkiss, K., & Taylor, M. G. (1989). Metal fluxes across themembranes of aquatic organisms. Review of AquaticScience, 1, 173–188.

Sprocati, A. R., Alisi, C., Segre, L., Tasso, F., Galletti,M., & Cremisini, C. (2006). Investigating heavy metalresistance, bioaccumulation and metabolic profile of ametallophile microbial consortium native to an aban-doned mine. Science of the Total Environment, 366(2–3), 649–658.

Subba Rao, N. V., Dey, A. & Barua, S. (1983). Studieson the malacofauna of Mooriganga estuary, Sunder-ban, West Bengal. Bulletin of the Zoological Survey ofIndia, 5, 47–56.

Tilzer, M. M., & Khondker, M. (1993). Hypertrophic andpolluted freshwater ecosystems: Ecological basis forwater resource management (pp. 91–96). Departmentof Botany, Dhaka University, Bangladesh.

Tsangaris, C., Papathanasiou, E., & Cotou, E. (2007). As-sessment of the impact of heavy metal pollution froma ferro-nickel smelting plant using biomarkers. Eco-toxicology and Environmental Safety, 66(2), 232–243.

UNEP/FAO/IAEA/IOC (1984). Sampling of selected ma-rine organisms and sample preparation for trace metalanalysis. Reference method for marine pollution studiesNo 7 Rev 2.

Vassiliki, K., & Konstantina, A. D. (1984). Transfer fac-tors of heavy metals in aquatic organisms of different


trophic levels. Bulletin of Environmental Contamina-tion and Toxicology.

Zaroogian, G. E. (1980). Crassostrea virginica as an indi-cator of cadmium pollution. Marine Biology, 58, 275–284.

Zorba, M. A., Jacob, P. G., Al-Bloushi, A., & Al-Nafisi, R.(1992). Clams as pollution bioindicators in Kuwait’smarine environment: Metal accumulation and depu-ration. Science of the Total Environment, 120(3), 185–204.

heavy metal concentrations in some macrobenthic fauna

Documents