Trace Element Concentrations in Soft Tissue and Shell of the Mangrove Oyster (Crassostrea Gasar Dautzenberg, 1891) from the Lake Zowla-Aného Lagoon Hydro System (Southern Togo)
The Lake Zowla-Aného lagoon hydro system, located on the southeast coast of Togo, is very exposed to metal contamination as it receives a huge amount of untreated domestic and industrial effluents from Aného City and the phosphorite treatment plant at Kpémé. This study aims to assess the concentrations of seven heavy metals and their bioaccumulation status in soft tissues and shells of the mangrove oyster (Crassostrea gasar) collected from this aquatic environment. Samples were collected in January, April and July 2017 at two stations and analyzed using flame atomic absorption spectrophotometry. Results indicate that the waters are contaminated by Cd, Pb and Cr with average concentrations that are significantly above WHO standards. At both locations, the contents of the trace elements (except Cr) in oysters’ soft tissues were significantly higher than those in the shells. In the soft tissues, the concentration of Cr, Cu, Zn, As, Cd, Hg, and Pb ranged (in mg·kg-1) from 4.33 to 23.14, 93.4 to 366.7, 455.68 to 1384.15, 0.11 to 1.34, 16.42 to 62.6, 0.05 to 0.473 and 0.39 to 21.08, respectively. Furthermore, statistical analyses showed marked differences in mean concentrations between sampling time on the one hand, and between sampling locations on the other hand (p < 0.05). The highest metal concentrations were recorded in oysters collected in June at Zalivé whereas the lowest values were recorded in April at Zowla. Based on BCF results in the lagoon system, the oyster C. gasar can be used as a biomonitor of Zn, Cd, Cu and Hg exposure. Finally, the Cd, Pb, As, Zn and Cu concentrations in soft tissues and were found to be significantly higher than the permissible limit for human consumption according to WHO and FAO and thus pose a threat to human health.
References
[1]
Rollins, H.B., Sandweiss, D.H., Brand, U. and Rollins, J.C. (1987) Growth Increment and Stable Isotope Analysis of Marine Bivalves: Implications for the Geoarchaeological Record of El Niño. Geoarchaeology, 2, 181-197. https://doi.org/10.1002/gea.3340020301
[2]
Stambaugh, J.E. (1988) The Ancient Roman City. Johns Hopkins University Press, Baltimore, MD.
[3]
EFSA (2014) Scientific Opinion on Health Benefits of Seafood (Fish and Shellfish) Consumption in Relation to Health Risks Associated with Exposure to Methylmercury. EFSA Journal, 12, Article 3761.
[4]
Tan, K., Ma, H. and Li, S. (2020) Bivalves as Future Source of Sustainable Natural Omega-3 Polyunsaturated Fatty Acids. Food Chemistry, 311, Article ID: 125907. https://doi.org/10.1016/j.foodchem.2019.125907
[5]
Wang, W.-X. and Lu, G.Y. (2017) Heavy Metals in Bivalve Mollusks. In: Cartus, S.A., Ed., Chemical Contaminants and Residues in Food, 2nd Edition, Woodhead Publishing, Sawston, 553-594. https://doi.org/10.1016/B978-0-08-100674-0.00021-7
[6]
Kucuksezgin, F., Kontas, A., Altay, O., Uluturhan, E. and Darilmaz, E. (2006) Assessment of MARINE Pollution in Izmir Bay: Nutrient, Heavy Metal and Total Hydrocarbon concentrations. Environment International, 32, 41-51. https://doi.org/10.1016/j.envint.2005.04.007
[7]
Miquel, M.G. (2001) Les effets des métaux lourds sur l’environnement et la santé. Office Parlementaire d’Evaluation des Choix Scientifiques et Technologiques. Rapport 261, Paris, France.
[8]
Chiffoleau, J.F., Auger, D. and Chartier, E. (2002) Dosage de certains métaux traces (Cd, Co, Cu, Fe, Ni, Pb, Zn) dissous dans l’eau de mer par absorption atomique après extraction liquide-liquide. IFREMER.
[9]
Turkmen, A., Turkmen, M., Tepe, Y. and Akyurt, I. (2005) Heavy Metals in Three Commercially Valuable Fish Species from Iskenderun Bay, Northern East Mediterranean Sea, Turkey. Food Chemistry, 91, 167-172. https://doi.org/10.1016/j.foodchem.2004.08.008
[10]
Lafabrie, C. (2007) Utilisation de Posidonia oceanica (L) Delile comme bio-indicateur de la contamination métallique. Università di Corsica Pasquale Paoli, Corte, Corsica.
[11]
Yáñez-Arancibia, A., Lara Domínguez, A.L. and Pauly, D. (1994) Coastal Lagoons as Fish Habitats. In: Kjerfve, K., Ed., Coastal Lagoon Processes, Elsevier, Amsterdam, 363-376. https://doi.org/10.1016/S0422-9894(08)70017-5
[12]
Kone, B., Cisse, G., Houenou, P.V., Obrist, B., Wyss, K., Odermatt, P. and Tanner, M. (2006) Health Risk Due to Lagoon Water Pollution in a West African Metropolis: Vulnerability and Resilience of Neighbouring Communities. Epidemiology, 17, S197. https://doi.org/10.1097/00001648-200611001-00499
[13]
Newton, A., Icely, J., Cristina, S., Brito, A., Cardoso, A.C., Colijn, F., Riva, S.D., Gertz, F., Hansen, J.W., Holmer, M., et al. (2014) An Overview of Ecological Status, Vulnerability and Future Perspectives of European Large Shallow, Semi-Enclosed Coastal Systems, Lagoons and Transitional Waters. Estuarine, Coastal and Shelf Science, 140, 95-122. https://doi.org/10.1016/j.ecss.2013.05.023
[14]
Bryan, G.W. (1971) The Effect of Heavy Metals (Other than Mercury) on Marine and Estuarine Organisms. Proceedings of the Royal Society B: Biological Sciences, 177, 389-410. https://doi.org/10.1098/rspb.1971.0037
[15]
Le, X.S., Le, V.N., Lu, V.D., Cao, T.T.T., Nguyen, T.P.H. and Tran, D.T. (2015) Assessment of Pollution Load into Thi Nai Lagoon, Viet Nam and Prediction to 2025. International Journal of Sciences, 4, 116-127. https://doi.org/10.18483/ijSci.741
[16]
DGSCN (2010) Quatrième recensement général de la population et de l’habitat, Résultats définitifs. Volume spéciale. Direction Générale de la Statistique et de la Comptabilité Nationale (DGSCN), Bureau Central du Recensement (BCR), Lomé, Togo.
[17]
Gnandi, K., Rezaie, B. and Edorh, A.P. (2009) The Geochemical Characterization of Mine Effluents from the Phosphorite Processing Plant of Kpémé (Southern Togo). Mine Water and the Environment, 28, 65-73. https://doi.org/10.1007/s10230-008-0058-0
[18]
Tchangbedji, G., Kili, K.A., Savariaul, M.J. and Lacout, J.L. (2003) Chemical and Structural Characterization of Natural Phosphate of Hahotoé (Togo). Bulletin of Chemistry Society of Ethiopia, 17, 139-147. https://doi.org/10.4314/bcse.v17i2.61659
[19]
Ouro-Sama, K., Solitoke, H.D., Tanouayi, G., Badassan, T.E.-E., Ahoudi, H., Nyametso, A.Y. and Gnandi, K. (2018) Spatio-Temporal Variation of the Physicochemical Parameters of Waters from the Hydrosystem Lake Togo-Lagoon of Aného (South-East of Togo). Journal of Scientific and Engineering Research, 5, 164-178.
[20]
Ouro-Sama, K., Solitoke, H.D., Tanouayi, G., Lazar, I.M., Bran, P., Nadejde, M., Ahoudi, H., Badassan, T.E.-E., Nyametso, A.Y., Gnandi, K. and Lazar, G.O. (2020) Spatial and Seasonal Variation of Trace Elements Contamination Level of the Waters from the Hydrosystem Lake Togo-Lagoon of Aného (South of Togo). SN Applied Sciences, 2, Article No. 811. https://doi.org/10.1007/s42452-020-2593-7
[21]
Solitoke, H.D., Ouro-Sama, K., Tanouayi, G., Badassan, T.E.-E., Ahoudi, H., Nyametso, A.Y., Avumadi, A.M.D. and Gnandi, K. (2018) Seasonal and Spatial Variability of Physicochemical Parameters of a Semi Enclosed Lagoon System: The Complex of Lake Zowla-Aného Lagoon. International Journal of Research in Environmental Studies, 5 56-69.
[22]
Solitoke, H.D., Ouro-Sama, K., Tanouayi, G., Badassan, T.E.-E., Ahoudi, H., Nyametso, A.Y., Avumadi, A.M.D. and Gnandi, K. (2018) Etude de la contamination métallique des sédiments d’un hydro système tropicale: Cas du système Lac Zowla-Lagune d’Aného (Sud-Togo). Environmental Water Sciences, Public Health & Territorial Intelligence Journal, 2, 41-51.
[23]
Ouro-Sama, K., Solitoke, H.D., Gnandi, K., Afiademanyo, K.M. and Bowessidjaou, E.J. (2014) évaluation et risques sanitaires de la bioaccumulation de métaux lourds chez des espèces halieutiques du système lagunaire togolais. VertigO-la revue électronique en sciences de l’environnement, 14, 2-18. https://doi.org/10.4000/vertigo.15093
[24]
Atanlé, K., Bawa, M.L., Kokou, K. and Djanéyé-Boundjou, G. (2012) Caractérisation physico-chimique et diversité phytoplanctonique des eaux du lac de Zowla (Lac Boko), Togo. International Journal of Biological and Chemical Sciences, 6, 543-558. https://doi.org/10.4314/ijbcs.v6i1.48
[25]
MERF/PNUD/FEM (2007) Etudes de vulnérabilité, Identification des principales mesures d’adaptation et des options prioritaires de riposte aux changements climatiques, secteur Zone Côtière, Rapport final. Ministère de l’Environnement et des Ressources Forestières/Programme des Nations Unis pour le Développement/Fonds pour l’Environnement Mondial.
[26]
ONUDI/NSE (2007) Réduction des rejets des mines de phosphates du Togo dans le GCLME, Projet de démonstration du Togo. Rapport final. Organisation des Nations Unies pour le Développement Industriel/North-South Environment (ONUDI/NSE).
[27]
Millet, B. (1983) Etude de quelques caractéristiques hydrologiques et hydrochimiques du système lagunaire du lac Togo: Années 1981 et 1982. Edition ORSTOM, Lomé.
[28]
Solitoke, H.D. (2012) Bioaccumulation des Eléments Traces chez deux bivalves de la lagune d’Aného (Senilia senilis, Linnaeus 1758 et Crassostrea gasar, Dautzenberg, 1891): Cas du Plomb, du Cadmium et de l’Arsenic Université de Lomé.
[29]
Marie, V. (2005) Etude de la réponse des métal-lothionéines chez les bivalves, Corbicula fluminea, Dreissena polymorpha et Crassostrea gigas, après exposition au cadmium et au zinc; Approches in situ et expérimentales. Université de Bordeaux Bordeaux, 1.
[30]
Tay, C.K., Asmah, R. and Biney, C.A. (2009) Trace Metal Levels in Water and Sediment from the Sakumo II and Muni Lagoons, Ghana. West African Journal of Applied Ecology, 16, 75-94. https://doi.org/10.4314/wajae.v16i1.55870
[31]
El Morhit, M. (2009) Hydrochimie, éléments traces métalliques et incidences écotoxicologiques sur les différentes composantes d’un écosystème estuarien (Bas Loukkos). Thèse de Doctorat, Université Mohammed V (Rabat), Maroc.
[32]
Sharif, R., Chong, E. and Chan, K.M. (2016) Human Health Risk Assessment of Heavy Metals in Shellfish from Kudat, Sabah. Malaysian Journal of Nutrition, 22, 301-305.
[33]
Denil, D.J., Fui, C.F. and Ransangan, J. (2017) Health Risk Assessment Due to Heavy Metals Exposure via Consumption of Bivalves Harvested from 384 Marudu Bay, Malaysia. Open Journal of Marine Sciences, 7, 494-510. https://doi.org/10.4236/ojms.2017.74035
[34]
Tessier, L. and Bonté, P. (2002) Suspended Sediment Transfer in Seine River Watershed, France: A Strategy Using Fingerprinting from Trace Elements. Science for Water Policy, 79-99.
[35]
Liu, W.X., Li, X.D., Shen, Z.G., Wang, D.C., Wai, O.W.H. and Li, Y.S. (2003) Multivariate Statistical Study of Heavy Metal Enrichment in Sediments of the Pearl River Estuary. Environmental Pollution, 121, 377-388. https://doi.org/10.1016/S0269-7491(02)00234-8
[36]
Probst, A., N’guessan, Y.M., Probst, J.L. and Bur, T. (2009) Trace Elements in Stream Bed Sediments from Agricultural Catchments (Gascogne Region, S-W France): Where Do They Come from? Science of the Total Environment, 407, 2939-2952. https://doi.org/10.1016/j.scitotenv.2008.12.047
[37]
Razaie-Boroon, M.H., Gnandi, K. and Tomety-Mensah, K.F. (2011) Presence and Distribution of Toxic Trace Elements in Water and Sediments of the Southern Togo Rivers Watershed, West Africa. Fresenius Environmental Bulletin, 20, 1853-1865.
[38]
OPED (2021) Rapport sur la situation des pesticides hautement dangereux (HHP) au Togo. Organisation Pour l’Environnement et le Développement durable (OPED).
[39]
Gnandi, K., Tozo, K., Amouzouvi, K., Baba, G., Tchangbédji, G., Killi, K. and Agbeko, K. (2006) Impact de l’exploitation minière sur la santé humaine: Cas de la fluorose dentaire chez les enfants autours de l’usine de traitement des phosphates de Kpémé (Sud-Togo). Journal de la Recherche Scientifique de l’Université de Lomé, Série A, 8, 195-205.
[40]
Mélila, M., Poutouli, W., Amouzou, K.S., Tchangbédji, G., Tchaou, M. and Doh, A. (2012) Evaluation de l’impact du rejet des déchets phosphates dans la mer sur la biodiversité marine dans trois localités côtières au Togo à partir des biomarqueurs du stress oxydatif chez Sphyraena barracuda (Heckel, 1843). International Journal of Biological and Chemical Sciences, 6, 820-831. https://doi.org/10.4314/ijbcs.v6i2.24
[41]
Kondo, K.F., Afiademanyo, K.M., Ouro-Sama, K., Solitoke, H.D. and Gnandi, K. (2021) Heavy Metal Contamination Levels in Clams (Galatea Paradoxa, Born 1778) and Surface Sediments from Mono River Estuary, Togo, and Its Health Implications. Journal of Biology, Agriculture and Healthcare, 11, 81-94.
[42]
Góngora-Gómez, A.M., García-Ulloa, M., Muñoz-Sevilla, N.P., Domínguez-Orozco, A.L., Villanueva-Fonseca, B.P., Hernández-Sepúlveda, J.A. and Izaguirre, R.O. (2017) Heavy-Metal Contents in Oysters (Crassostrea Gigas) Cultivated on the Southeastern Coast of the Gulf of California, Mexico. Hidrobiológica, 27, 219-227.
[43]
Metongo, B.S. (1991) Concentrations en métaux toxiques chez Crassostrea gasar (huître de mangrove) en zone urbaine lagunaire d’Abidjan (Côte d’Ivoire). Journal Ivoirien d’Océanologie et de Limnologie, 1, 33-45.
[44]
Jara-Marini, M.E., Soto-Jiménez, M.F. and Páez-Osuna, F. (2008) Trace Metal Accumulation Patterns in a Mangrove Lagoon Ecosystem, Mazatlan Harbour, SE Gulf of California. Journal of Environmental Science Health Part A, 43, 995-1005. https://doi.org/10.1080/10934520802059797
[45]
Benmessaoud, F., Kourradi, R., Menioui, M. and Stambouli, A. (2001) Concentration des métaux lourds chez la palourde Venerupis decussate (L) dans un estuaire marocain: l’oued Bou Regreg. Rabati, Rapportr de la commission interétat de la mer méditerranéenne, 36, 111.
[46]
Mirzaei, M.R., Azini, M.R. and Rad, T.A. (2016) Seasonal Variation of Heavy Metal in Seawater, Sediment and Hooded Oyster, Saccostrea cucullata, in Iranian Southern Waters (Chabahar Coast). Research in Marine Science, 1, 3-12.
[47]
Tuo, A.D., Soro, M.B., Trokourey, A. and Bokra, Y. (2020) Seasonal Variation in Trace Metal Contents in Oyster Crassostrea Gasar from the Milliardaires Bay, Côte d’Ivoire. International Journal of Chemical Studies, 8, 624-630. https://doi.org/10.22271/chemi.2020.v8.i2j.8838
[48]
Otchere, F.A. (2003) Heavy Metals Concentrations and Burden in the Bivalves (Anadara (Senilia) Senilis, Crassostrea Tulipa and Perna Perna) from Lagoons in Ghana: Model to Describe Mechanism of Accumulation/Excretion. African Journal of Biotechnology, 2, 280-287. https://doi.org/10.5897/AJB2003.000-1057
[49]
Metayer, G., Amiard, J.C., Amiard-Triquet, C. and Berthet, B. (1985) Facteurs biologiques et écologiques contrôlant le niveau d’éléments traces (Cd, Pb, Cu, Zn) chez les moules et huîtres de baie Bouregreg. Bulletin de la Socété des Sciences Naturelles de l’Ouest de la France, 7, 53-69.
[50]
Kourradi, R. (2007) Evaluation du degré de la pollution anthropique de l’estuaire de Bou Regreg et impact sur la biologie et la dynamique de Scrobicularia plana (Linné, 1758) et Solen marginatus (Linné, 1767). Université Mohammed V-Agdal Rabat, Maroc.
[51]
Solitoke, H.D., Afiademanyo, K.M., Ouro-Sama, K., Tanouayi, G., Badassan, T.E.-E. and Gnandi, K. (2020) Aspects of Population Dynamics of the Mangrove Oyster, Crassostrea Gasar Dautzenherg (1891) (Ostreida: Ostreidae) from the Lake Zowla-Aného Lagoon system in Togo. Journal of Fisheries and Aquaculture Research, 5, 93-106.
[52]
Furnestin, M.-L., Maurin, C., Lee, J.Y. and Raimbault, R. (1966) Eléments de planctonologie appliquée. Revue des Travaux, Institut des sciences et technologies, pêche maritime, 30.
[53]
Drif, F. (2012) Distribution des métaux traces chez les bivalves (Mollusques) dans le golfe d’Annaba (Nordest Algérien). Univrsité Badji Mokhtar, Annaba.
[54]
Cossa, D. and Bourget, I. (1980) Trace Elements in Mytilus edulis L. from Estuary and Gulf of St Lawrence, Canada: Lead and Cadmium Concentrations. Environmental Pollution Series A, Ecological and Biological, 23, 1-8. https://doi.org/10.1016/0143-1471(80)90091-4
[55]
Goldberg, E.D., Koide, M., Hodge, V., Flegal, A.R. and Martin, J. (1983) US Mussel Watch: 1977-1978 Results on Trace Metals and Radionuclides. Estuarine, Coastal and Shelf Science, 16, 69-93. https://doi.org/10.1016/0272-7714(83)90095-1
[56]
Amiard, J.C. (1988) Les mécanismes de transfert des polluants métalliques dans la chaine alimentaire aboutissant à l’huître et à la moule, mollusques filtreurs, formes chimiques de stockage, conséquences écotoxicologiques. Oceanus, 14, 283-287.
[57]
Cheggour, M., Chafik, A., Fisher, N.S. and Benbrahim, S. (2005) Metal Concentrations in Sediments and Clams in Four Moroccan Estuaries. Marine Environmental Research, 59, 119-137. https://doi.org/10.1016/j.marenvres.2004.04.002
[58]
Kraemer, L.D., Peter, G., Campbell, C. and Hare, L. (2006) Seasonal Variations in Hepatic Cd and Cu Concentrations and in the Sub-Cellular Distribution of These Metal in Juvenile Yellow Perch (Perca Flavescens). Environmental Pollution, 142, 313-325. https://doi.org/10.1016/j.envpol.2005.10.004
[59]
Huanxin, W., Lejun, Z. and Presly, B.J. (2000) Bioaccumulation of Heavy Metals in Oyster (Crassostrea Virginica) Tissue and Shell. Environmental Earth Sciences, 39, 1216-1226. https://doi.org/10.1007/s002540000110
[60]
Pourang, N., Richardson, C.A., Chenery, S.R.N. and Nasrollahzedeh, H. (2014) Assessment of Trace Elements in the Shell Layers and Soft Tissues of the Pearl Oyster Pinctada Radiata Using Multivariate Analyses: A Potential Proxy for Temporal and Spatial Variations of Trace Elements. Environmental Monitoring and Assessment, 186, 2465-2485. https://doi.org/10.1007/s10661-013-3553-0
[61]
Bray, D.J., Green, I., Golicher, D. and Herbert, R.J.H. (2015) Spatial Variation of Trace Metals within Intertidal Beds of Native Mussels (Mytilus Edulis) and Non-Native Pacific Oysters (Crassostrea Gigas): Implications for the Food Web? Hydrobiologia, 757, 235-249. https://doi.org/10.1007/s10750-015-2255-8
[62]
Onwuteaka, J., Edoghotu, A.J., Friday, U., Wokoma, O.F. and Bob-Manuel, F.G. (2015) Heavy Metals Contamination of the Sessile Bivalve, Crassostrea Gasar (Mangrove Oyster) in Ai Post Oil Spilled Brackish Water Creek of the NIGER Delta, Nigeria. Annals of Biological Research, 6, 72-77.
[63]
Sidoumou, Z., Gnassia-Barelli, M., Siau, Y., Morton, V. and Roméo, M. (2006) Heavy Metal Concentrations in Molluscs from the Senegal Coast. Environment International, 32, 384-387. https://doi.org/10.1016/j.envint.2005.09.001
[64]
Frías-espericueta, M.G., Osuna-lópez, I., Bañuelos-vargas, I., López-López, G., Muy-Rangel, M.D., Izaguirre-Fierro, G., Rubio-Carrasco, W., Meza-Guerrero, P.C. and Voltolina, D. (2009) Cadmium, Copper, Lead and Zinc Contents of the Mangrove Oyster, Crassostrea Corteziensis, of Seven Coastal Lagoons of NW Mexico. Bulletin of Environmental Contamination and Toxicology, 83, 595-599. https://doi.org/10.1007/s00128-009-9828-z
[65]
Páez-Osuna, F. and Osuna-Martínez, C.C. (2015) Bioavailability of Cadmium, Copper, Mercury, Lead, and Zinc in Subtropical Coastal Lagoons from the Southeast Gulf of California Using Mangrove Oysters (Crassostrea Corteziensis and Crassostrea Palmula). Archives of Environmental Contamination and Toxicology, 68, 305-316. https://doi.org/10.1007/s00244-014-0118-3
[66]
Alfonso, J.A., Handt, H., A, M., Vásquez, Y., Azocar, J. and Marcano, E. (2013) Temporal Distribution of Heavy Metal Concentrations in Oysters Crassostrea Rhizophorae from the Central Venezuela Coast. Marine Pollution Bulletin, 73, 394-398. https://doi.org/10.1016/j.marpolbul.2013.05.010
[67]
Cossa, D., Thibaud, Y., Romeo, M. and Gnassia-Barelli, M. (1990) Le mercure en milieu marin. Biogéochimie et écotoxicologie. Rapports Scientifiques et Techniques. Ifremer.
[68]
Windom, H.L. and Smith, R.G. (1972) Distribution of Iron, Magnesium, Copper, Zinc, and Silver in Oysters along the Georgia Coast. Journal Fisheries Research Board Canada, 29, 450-452. https://doi.org/10.1139/f72-075
[69]
Cossa, D. and Lassus, P. (1989) Le cadmium en milieu marin. Biogéochimie et écotoxicologie. Editions Ifremer, Plouzané, France
[70]
Dar, M.A., Belal, A.A. and Madkour, G. (2018) The Differential Abilities of Some Molluscs to Accumulate Heavy Metals within Their Shells in the Timsah and the Great Bitter Lakes, Suez Canal, Egypt. The Egyptian Journal of Aquatic Research, 44, 291-298. https://doi.org/10.1016/j.ejar.2018.11.008
[71]
Protasowicki, M., Dural, M. and Jaremek, J. (2008) Trace Metals in the Shells of Blue Mussels (Mytilus edulis) from the Poland Coast of Baltic Sea. Environmental Monitoring and Assessment, 141, 329-337. https://doi.org/10.1007/s10661-007-9899-4
[72]
Wolfe, D.A. (1970) Levels of Stable Zn and 65Zn in Crassostrea Virginica from North Carolina. Journal of the Fisheries Research Board of Canada, 27, 47-57. https://doi.org/10.1139/f70-006
[73]
Swaleh, M.M., Ruwa, R., Wainaina, M.N., Ojwang, L.M., Shikuku, S.L. and Maghanga, J.K. (2016) Heavy Metals Bioaccumulation in Edible Marine Bivalve Mollusks of Tudor Creek Mombasa Kenya. Journal of Environmental Science, Toxicology and Food Technology, 10, 2319-2402. https://doi.org/10.9790/2402-1008024352
[74]
Abdullah, M.H., Jovita, S. and Ahmad, Z.A. (2007) Heavy Metals (Cd, Cu, Cr, Pb and Zn) in Meretrix meretrix Roding, Water and Sediments from Estuaries in Sabah. N Borneo. International Journal of Environmental & Science Education, 2, 69-74.
