International Journal of Environmental Research University of Tehran ISSN: 1735-6865 EISSN: 2008-2304 Vol. 4, Num. 3, 2010, pp. 533-540

International Journal of Environmental Research, Vol. 4, No. 3, July-September, 2010, pp. 533-540

Article

Bioaccumulation of heavy metals in the tissue of the clam Galatea paradoxa and sediments from the volta estuary, Ghana

Adjei-Boateng , D . * , Obirikorang , K . A . and Amisah , S.

Department of Fisheries and Watershed Management, Faculty of Renewable Natural Resources, Kwame Nkrumah University of Science and Technology Kumasi, Ghana

Correspondence Address: * Department of Fisheries and Watershed Management, Faculty of Renewable Natural Resources, Kwame Nkrumah University of Science and Technology Kumasi, Ghana
adjeiboat@yahoo.com

Date of Submission: 22-Sep-2009
Date of Decision: 02-Mar-2010
Date of Acceptance: 12-Mar-2010

Code Number: er10060

Abstract

Keywords: Bioaccumulation, Heavy metals, Sediments, Galatea paradoxa

Introduction

Growing social concern about environmental qual-ity has been observed in recent years, both on a global and local scale. This is connected with convincing evi-dence that environmental pollution results in the deg-radation of ecosystems. Emissions of harmful sub-stances have negative effects on the natural environ-ment and human health (Gadzala-Kopciuch et al., 2004). When the consequences of environmental pollution become visible, it is often too late to prevent and chronic toxic effects, impossible to notice at the initial stage of the process, may manifest themselves after many years (Alloway and Ayres, 1998). That is the main reason why it is imperative to conduct periodic pollution moni-toring of aquatic environments. Initially, most monitor-ing programmes were based on the chemical analysis of major contaminants within the environment, until a number of difficulties became apparent (Jamile, 2001). Many authors found that by simply monitoring con-taminants in natural waters, they were unable to inte-grate the overall environmental conditions and their impacts on aquatic life and further found difficulty in quantifying very low contaminant concentrations commonly found in natural waters (Phillips and Rain-bow, 1994; Narbonne, 2000).

Bivalves have instead been used by several au-thors as indicators of aquatic pollution (Otchere, 2003, Ferreira et al., 2004, Kljakovic-Gaspic et al., 2007) mainly because they are widely distributed globally, easy to handle, sessile, filter feeders that have the ability to accumulate high metal concentrations with-out metabolising the metals appreciably (Gunther et al., 1999; Nasci et al., 1999; Olivier et al., 2002), pro-vide a time-integrated indication of environmental contamination (Regoli, 1998) and can concentrate pol-lutants in their tissues at concentrations greater than the ambient water (El-Shenawy, 2002). Sediments on the other hand are an important sink of a variety of pollutants, particularly heavy metals and may serve as an enriched source for benthic organisms (Wang et al., 2002) especially in estuarine ecosystems. Metals may be present in the estuarine system as dissolved species, as free ions or forming organic complexes with humic and fulvic acids. Additionally, many metals e.g. Pb associate readily with particulates and be-come adsorbed or co-precipitated with carbonates, oxyhydroxides, sulphides and clay minerals. Conse-quently, sediments accumulate contaminants and may act as long-term stores for metals in the environment (Spencer and MacLeod, 2002). Exposure of sediment-dwelling organisms to metals may then occur via up-take of interstitial waters, ingestion of sediment par-ticles and via the food chain. The occurrence of elevated concentrations of trace metals in sediments found at the bottom of the water column can be a good indicator of man-induced pollution rather than natural enrichment of the sediment by geological weathering (Davies et al. 1991, Chang et al. 1998; Opuene and Agbozu, 2008).

Anecdotal information suggests that the Volta basin might be receiving a considerable range of pol-luting effluents, particularly heavy metals from metal fabrication, the galvanized iron sheets which are prin-cipal roofing material in the settlements surrounding the Volta Estuary and agricultural industries along the Volta basin. It is in the light of the above reasons that this research evaluated the sediments and clams from the Volta estuary in Ghana as indicators of heavy metal pollution. This study investigated the levels of the metals in clam and sediment samples as well as rela-tionship between the concentrations in sediments and in the clams.

Materials and Methods

The study was carried out at Ada and Aveglo, at the Volta Estuary, in Ghana, from March 2008 to Sep-tember 2008. Ada located on Latitude 05°49' 18.6" N and longitude 000°38.46' 1"E and Aveglo latitude 05°53 28.2" N and longitude 000° 38' 24.7"E represent the most active clam fishing grounds of the Volta estuary [Figure - 1]. Riverbed sediment samples were collected on a monthly interval for 7 months using an Ekman grab at the two locations from March to September 2008. Sediment samples were collected from each sampling sites according to the standard procedures described in USEPA's sediment sampling guide (USEPA, 1994) and were kept in LDPE bottles pre-washed with 10% HC1 and stored in insulated iced chests for analysis in the laboratory. In the laboratory the sediment subsamples of 500g from each sampling location were placed in ceramic mortars for drying at 80°C for 48hrs to a constant weight (Phillips and Yim, 1981).The dried samples were then gently disaggregated and ample quantities of each sample were finely ground in ce-ramic mortars and stored in 250 ml acid-washed LDPE bottles. The ground samples were kept at 4°C in a re-frigerator for heavy metal (USEPA, 1994).

Clam samples were obtained from fishermen's catch form the two sampling stations at monthly intervals for 7 months and transported to the laboratory, sub-merged in river water, in insulated chests within 12 hours for processing and storage for heavy metal analyses. In the laboratory, clam samples were cleansed to remove the mud and any debris and then washed with double distilled water. For each site, clams of various sizes were obtained and grouped into three size classes of 10 individuals each based on shell lengths. The categorization was as follows: small (25-40mm), medium (41-55mm), and large (above 55mm). The various clam size classes were purged of ingested organic and inorganic particles before being analysed for heavy metal accumulation by keeping each size class in distilled water for a 24-hour depuration. After the depuration process, a sterile stainless steel knife was used to dislodge and remove the soft tissue of each clam from the shell (Chiu et al., 2000). The flesh of each subsample was oven-dried to a constant weight at 60°C for 72 hours (Ferreira et al., 2004). Each dry clam sample was weighed on a Sartorius BP 210 S mi-cro balance to the nearest 0.0001 g. Individuals of each size class were ground together into fine powder us-ing a porcelain pestle and mortar. Homogenised subsamples were stored in air-tight, acid-washed (0.1 M HCl) snap-top glass vials for heavy metals analyses (EnvironmentalAgency, 2008).

About 0.5g of the homogenized clam subsamples and the sediment samples were weighed into a 50 ml digestion tube and 1ml of distilled water, 2.0 ml per-chloric acid (HNO ₃ -HClO ₄ ) (1:1 vv) and 5.0 ml sulphuric acid (H ₂ SO ₄ ) were added. Each mixture was refluxed at 200^° C for 30 minutes in a clean fume chamber. The com-pletely digested subsamples were allowed to cool at room temperature, and the undigested portion of the sediments filtered off through a Whatmann Glass Microfibre filter paper (GF/C) to obtain a clear solution and diluted to 50 ml in volumetric flasks with double distilled water (Jin et. al., 1999; Otchere, 2003).

Concentrations of Zn, Fe and Mn were determined using a Buck Scientific Model VGP flame Atomic Absorption Spectrophotometer (AAS). All tissue and sediment analytical batches were accompanied by blanks at a minimum rate of one blank per 20 samples. Replicate analyses were conducted on 10% of the samples to evaluate the precision of the analytical tech-niques. The data were expressed as total concentra-tions (μg/g dry weight (dw).The Atomic Mercury Ana-lyzer (Model HG 5000) equipped with a mercury lamp at a wavelength 253.7nm was used for the determina-tion of total mercury in the clam soft tissue and sedi-ment samples. Responses were recorded on strip chart recorders as sharp peaks. The peak heights were used for computation of the total mercury concentrations in the clam and expressed as microgram per gram dry weight (μg/g dw). Total mercury concentrations were validated according to standard procedures described for Mercury analyser Model HG 5000 to check for pre-cision and accuracy. Monthly measurements of tem-perature, salinity, pH, Total Dissolved Solids (TDS), conductivity and Dissolved Oxygen (DO) were taken in-situ at both sampling sites over the 7-month period using a Hanna (HI 9028) multi-parameter probe.

Biota Sediment Accumulation Factor (BSAF) was calculated for each site and clam size class to evaluate the efficiency of metal bioaccumulation in the tissues of the organisms. BSAFs were calculated for each analyte for each month using the equation:

Spatial patterns of heavy metal concentrations in clams from the two sampling stations, between the sedi-ments of both sampling stations and between the clams and sediments of the two sampling stations were investigated using both the Kruskall-Wallis non-para-metric test for independent samples (p< 0.05) Descrip-tive statistics were executed using the GraphPad Prism 5 Software.

Results and Discussion

The water quality variables monitored at the two sites were fairly constant without much variation. At Ada, pH declined marginally from 6.99 in April to 6.48 in September. Temperature remained fairly stable at 29.22°C in May and 27.28°C in September. Dissolved Oxygen (DO) levels were relatively high in March (8.76 mg/L) but dropped to 2.48 mg/L in September. Salinity however remained constant at 0.03 Practical Salinity Units (PSU) throughout the sampling period. Total Dis-solved Solids (TDS) remained fairly constant with val-ues between 31 and 35 mg/L over the study period. Conductivity values were low, ranging between 60 and 70μS cm ^-1 . At Aveglo, pH was between 6.89 and 7.08 during the sampling period. Temperature remained fairly constant during the sampling period ranging between 27.19°C and 28.49°C. Dissolved Oxygen levels ranged from of 2.38 mg l-1 to 6.78 mg/L whilst TDS values were between 32 and 42 mg/L during the period. Conductiv-ity values were between 63 and 84μS cm ^-1 whilst salinity remained constant at 0.03 PSU.Concentrations of trace metals in whole soft tissue of the clams and sedi-ments from the two stations at the Volta estuary, col-lected from March to September 2008, are given in [Table - 1] and [Table - 2].

The peak Mn concentration of 867μg/g was re-corded in the whole soft tissue of the small-sized clams at the Ada in July 2008. The medium-sized clams re-corded Mn concentrations between 68μg/g in May and 336μg/g in August 2008. Manganese concentration in the tissues of the large-sized clams recorded a peak concentration of 212μg/g in July 2008. Zinc concentra-tions were relatively lower in the clams from both sta-tions, with a peak value of 49 μg/g recorded in the medium-size clams from the Aveglo station in May. Results from the analysis of Fe in the tissues of the medium-sized clams registered the highest value of 539μg/g in March although most of the concentration fell within the range of 79 and 307μg/g. Total Mercury concentrations in the clam tissues were low for the two stations varying narrowly between 0.029 and 0.074μg/g [Table - 2]. The concentrations of the studied metal in the clam and sediment samples are similar to those observed in areas under low pollution impact.

Manganese concentrations in the estuarine sedi-ments ranged between 39 and 390μg/g during the sam-pling period. Zinc concentrations in the sediments from the Aveglo sampling station were very low, similar to the concentrations recorded at Ada. Iron concentra-tions were relatively very high in the estuarine sedi-ments, with the lowest concentration of 696μg/g recorded in May 2008 and the highest value of 3476μg/ g in August of 2008. Total mercury concentrations in the sediments from the two sampling stations were far lower than the concentrations observed in the tissues of the clams of all the three size classes. The lowest concentration of Total mercury in estuarine sediments of 0.0069μg/g was observed in May 2008 at Ada and the highest of 0.0240 μg/g at Aveglo in April 2008.

Examination of the spatial patterns of trace metals in the different clam size classes (small vs. small, me-dium vs. medium and large vs. large) from the two sta-tions using the Kruskall-Wallis non-parametric test for independent samples (p< 0.05) showed that there were no statistically significant differences between the two stations at the Volta estuary regarding all the studied trace metals except variations in Fe concentration in the large-sized clams from Ada and Aveglo.No signifi-cant differences (p>0.05) were found between the con-centrations of Mn, Zn, Fe and Hg in the sediments from the two sampling sites during the study period, indicating a similar bioavailability of the heavy metals in the sediments of the two sampling stations.

Differences in heavy metal concentrations be-tween each clam size group and sediment samples from the two sampling stations were carried out using the Kruskall-Wallis non-parametric test for independent samples (p< 0.05). No significant differences (p>0.05) were observed in Manganese concentrations between the small-sized clams and sediment samples over the study period. Mn concentrations were higher in the sediment samples except during July and August. Sig-nificant variations were however observed in the Mn concentrations between the medium and large size clams and the sediment samples. Mn concentrations in the sediments were consistently higher than in the medium and large size clams over the sampling period. Zinc concentrations were significantly higher (p< 0.0001) in all the clam size classes compared to the sediment samples. Iron concentrations in the sediment samples were 10 and 18 times higher than the concen-trations in the small-sized clams in May and June respectively. Similar trends were observed between the sediments and the other size classes. Highly signifi-cant differences (p< 0.0001) were observed in all the size-classes and the sediment samples for Iron. Total mercury concentrations showed highly significant variations ((p< 0.0001) between all the clam size classes and the sediment samples. THg concentrations were approximately five times higher in the clam tissues.

Results from the Aveglo sampling station por-trayed a trend similar to Ada. Differences in Mn con-centrations between the clam and sediment samples were not significant (p>0.05) for all the clam size classes. Zn showed highly significant variations (p< 0.0001) between the all the size classes and the sediment. Dif-ferences in concentration were similar to the trend observed at the Ada sampling station. Highly signifi-cant differences (p< 0.001) existed between all the clam size classes and sediment samples for Fe. Iron concen-trations in sediments were significantly higher than in the clam samples; twenty times higher than the con-centration in the small-sized clams in August 2008. Highly significant differences (p< 0.0001) were recorded for total Mercury concentrations in the clam and sedi-ment samples. The differences in concentrations ranged between two to five times more in the clam tissues. The Biosediment Accumulation Factors (BSAFs), [Table - 3] for each site were calculated to evaluate the efficiency of metal uptake by the clams and to describe the accumulation of studied metals. Zinc was however excluded because it was not detected in the sediment samples for certain months at both sampling stations. On the basis of the calculated BSAFs metal enrich-ment in the tissues of the clams was rank in the follow-ing order Hg>Mn>Fe. The average BSAF values reveals mercury as having the highest BSAF values. Hg contamination levels were found to be higher in the clams than in the sediments, suggesting a higher rate of accumulation of Hg by G. paradoxa. This could be as a result of the water acting as an additional source of Hg accumulation in G. paradoxa. Fe and Mn con-centrations were generally lower in the clam tissues than in the sediments, suggesting that the levels of contamination of these metals in the estuary do not exceed the clams' capacity to regulate them. The inter-actions between metal geochemistry and animal physi-ology determine the differences in the bioavailability among heavy metals (Wang et al., 2002). The relation-ship between the concentrations of the studied con-taminants in the clam tissues and the sediments was not clear-cut, supporting the fact that several variables control both the bioavailability and accumulation of heavy metals in individuals exposed to contamination (Ansari et al., 2004, Martin-Diaz et al., 2006).

Heavy metal concentrations in the clam tissues did not vary significantly between the two sampling stations during the study period. This could be due to similarities in the bioavailability of the heavy metals to the clams (Ferreira et al., 2004); suspended particulate matter, food sources, and the homogeneity in environ-mental and hydro-graphic parameters at the two sam-pling stations.

With the exception of Mercury all the heavy met-als examined in this study are essential metals and have intracellular regulatory mechanisms to keep their con-centrations in equilibrium in the organisms (Ferreira et al., 2004). This could also explain the absence of any significant spatial variations in metal concentration between the two sampling sites. The similarity in metal concentrations in the sediments could also be attrib-uted to similarities in important factors such as miner-alogy and grain size (Trefry and Priestly, 1976).Analy-ses of the heavy metal concentrations in the clam and sediment samples revealed no distinct relationship between heavy metal levels in clam tissues and sedi-ments in which they thrive. Heavy metal accumulation in the clams may not be directly or solely derived from sediments as observed by Huanxin et al., (2000). Other sources of heavy metals in bivalve tissues are derived from living or dead suspended particles and from dis-solved metals in the water (Huanxin et al., 2000).

The relatively consistent monthly concentrations of Mn, Fe and Zn in whole soft tissues of G. paradoxa may well represent efficient metabolism and detoxify-ing processes that include transportation, transforma-tion, sequestration and/or excretion of excess metals (Connell et al., 1999). The results further suggest that the levels of contamination of these metals do not ex-ceed the clam's capacity of regulation (Amiard et al., 1985; Durou et al., 2005; Mensi et al. 2008).The rela-tively higher concentrations of Zn in the clam tissues compared to the concentrations in the sediments sug-gests a high rate of accumulation by the clams, a physi-ological mechanism induced by exposure or even a high relevance of the water as an additional source of contamination (Cardoso et. al., 2008). Although monthly concentrations of Fe in the sediments from both stations were generally higher than Mn, their bio-sediment accumulation factors (BSAFs) were gener-ally lower than that of Mn [Table - 4]. This phenomenon occurs because Fe is deposited much more quickly than Mn but is strongly bound to the sediments under estuarine conditions (Huanxin et al., 2000). It is, thus, not readily available to the clams. Mn on the other hand can be said to be released much more easily from sediments than Fe and thus more available to the clams accounting for the higher BSAFs for Mn. Hg has much higher monthly BSAF values probably because it is a non-essential trace metal, which is not metabolised in the tissues of the clam and thus accumulates in the clam tissues. Peak metal concentrations and BSAF values for most of the heavy metals were recorded just prior to or at the beginning of the spawning season lending credence to accumulation of heavy metals prior to spawning. Before the spawning period, proteins and carbohydrates contents, which have a high affinity for heavy metals, are accumulated for gonad tissue pro-duction, energetic storage and consumption (Latouche and Mix, 1982; Paez-Osuna et. al., 1995).The release of heavy metals from sediments is controlled by the com-plex dynamics of the heavy metals and the physical and chemical conditions of the environment. Hence, there was no clearly defined relationship between the heavy metal concentrations in the clam tissues and in the sedi-ments. Other factors of the environment are certainly implicated in this observation.

At the two sampling stations (Ada and Aveglo), very intense clam fishing commences at the onset of rainy season in March and ends at the start of the dry season in December each year. Introduction of heavy metals into the estuary during the intense fishing ac-tivities could come from sources such as fuels leak-ages and fumes from outboard motors and from the motorized air compressors used by the divers in the their clam fishing activities. Metals could also be in-troduced from sources such as the paint cover of the boats used in the fishing activities. In Tunisia, Chouba et al., (2007) also found higher levels of heavy metals in the mullet, Mugil cephalus during high rainfall periods and the times for most intense fishing activities. The elevated concentrations of heavy metals in this period might also be attributed partly to surface water run-off from the surrounding agricultural lands into the Volta estuary. The study did not observe any known point source of pollution. This provides evi-dence that even clams from areas with no known point sources of contamination may have measurable body burdens of heavy metals. This may probably be due to the processes of natural weathering and supply from locations further upstream.

The relatively high concentration of essential heavy metals in the clam and sediment samples, par-ticularly Manganese and Iron might be attributed to local hydrological conditions, weathering and the in-tensive leaching of mineralised rocks in the catchment area during rainstorms. The use of galvanized iron sheets as the principal roofing material in the settle-ments surrounding the Volta estuary could also ac-count for the high levels of Fe in the clams and sedi-ments. According to Otchere (2003), higher wet sea-son levels of Fe and Zn might as well be due to import from surrounding settlements as most roofing in Ghana are made of galvanized iron sheets, most of which are presently rusty. Many metals are also found in agricul-tural products such as fertilisers. Those present in fertilisers include Mn and Zn which eventually accu-mulate in agricultural soils and become exposed to wa-ter bodies and the organisms present in them through run-off during the rainy season (Otchere, 2003).

Conclusion

Analyses of the clam and sediment samples revealed no distinct relationship between heavy metal concen-trations in clam tissues and sediments in which they thrive indicating that heavy metal accumulation in clams may not be directly or solely derived from sediments but from other sources such as living or dead suspended particles and from dissolved metals in the water Con-centrations of the studied metals varied significantly between the clams and sediments for both stations though both samples showed different affinities for the studied metals. The results further suggest that the lev-els of contamination of these metals in the estuary do not exceed the clams' capacity of regulation.

Acknowledgements

The authors are grateful to the International Foun-dation for Science (IFS) for providing financial sup-port (A/4421-1) to conduct this research work, Volta Basin Research project (VBRP), University of Ghana for the use of facilities at Aquaculture Research Cen-tre, Ada, and the Department of Fisheries and Water-shed Management of the Kwame Nkrumah University of Science and Technology, Kumasi for logistical sup-port.^[36]

References

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