Assessment of biomonitoring potential of contamination and bioavailability of heavy metals using red blood cockle Tegillarca granosa: Experimental field-based transplantation study
Abstract
This study evaluates the potential of red blood cockle Tegillarca granosa as a biomonitor for heavy metal contamination in coastal environments, with a focus on the differential bioaccumulation patterns across three sites: Teluk Kemang (TK), Pasir Panjang (PP), and Port Dickson (PD). Four major findings emerged from the analysis. First, T. granosa demonstrated significant variations in metal accumulation, with PD exhibiting the highest concentrations of Zinc (Zn), Copper (Cu), and Iron (Fe). This confirms the species' sensitivity to varying pollution levels and highlights PD as the most contaminated site among the three. Second, strong correlations between metal levels in the environment and their accumulation in the cockle’s soft tissues underscored its effectiveness in reflecting the bioavailability of contaminants, particularly for Zn and Cu. This finding validates the use of T. granosa as an effective bioindicator of environmental metal exposure. Third, the study highlighted the role of cockle shells as indicators of long-term exposure, with consistently higher metal concentrations observed at PD. This suggests persistent environmental contamination in this area and demonstrates the value of shell analysis in assessing chronic pollution. Finally, the stepwise multiple regression analysis revealed complex interactions between environmental media and bioaccumulation processes, emphasizing the need for a comprehensive approach to biomonitoring. These interactions indicate that bioaccumulation in T. granosa is influenced by multiple environmental factors, necessitating an integrated monitoring strategy. These findings support the use of T. granosa as a reliable indicator species for monitoring heavy metal pollution and assessing ecological risks in coastal ecosystems.
References
Al-Mutairi KA, Yap CK (2021) A review of heavy metals in coastal surface sediments from the Red Sea: health-ecological risk assessments. International Journal of Environmental Research and Public Health 18(6): 2798.
Aziz KHH, Mustafa FS, Omer KM, Hama S, Hamarawf RF, Rahman KO (2023) Heavy metal pollution in the aquatic environment: efficient and low-cost removal approaches to eliminate their toxicity: a review. RSC Advances 13(26): 17595–17610.
Bamanga A, Amaeze NH, Al-Anzi B (2019) Comparative investigation of total, recoverable, and bioavailable fractions of sediment metals and metalloids in the Lagos Harbour and Lagoon system. Sustainability 11(16): 4339.
Bazzi AO (2014) Heavy metals in seawater, sediments and marine organisms in the Gulf of Chabahar, Oman Sea. Journal of Oceanography and Marine Science 5(3): 20–29.
Birch G, Shalem Y, Lewtas KLM, Besley C (2019) Metal concentrations in Sydney cockle (Anadara trapezia) tissue and ambient sediment in a highly-modified estuary (Sydney estuary, Australia). Marine Pollution Bulletin 144: 299–308.
Cardellicchio N, Buccolieri A, Leo AD, Giandomenico S, Spada L (2008) Levels of metals in reared mussels from Taranto Gulf (Ionian Sea, Southern Italy). Food Chemistry 107(2): 890–896.
Carolin CF, Kumar PS, Saravanan A, Joshiba GJ, Naushad M (2017) Efficient techniques for the removal of toxic heavy metals from aquatic environment: a review. Journal of Environmental Chemical Engineering 5(3): 2782–2799.
Chee SY, Devakie M, Azizah MNS (2011) Phylogenetic study and barcoding of the blood cockle, Tegillarca granosa, found on the west coast of peninsular Malaysia using the COI gene. Genetics and Molecular Research 10(2): 1237–1244.
Cheggour M, Chafik A, Langston W, Burt GR, Benbrahim S, Texier H (2001) Metals in sediments and the edible cockle Cerastoderma edule from two Moroccan Atlantic lagoons: Moulay Bou Selham and Sidi Moussa. Environmental Pollution 115(2): 149–160.
Chen CY, Ward DM, Williams J, Fisher NS (2016) Metal bioaccumulation by estuarine food webs in New England, USA. Journal of Marine Science and Engineering 4(2): 41.
Chiarelli R, Roccheri MC (2014) Marine invertebrates as bioindicators of heavy metal pollution. Open Journal of Metal 4(4): 93–106.
Corrias F, Atzei A, Addis P, Secci M, Russo M, Angioni A (2020) Integrated environmental evaluation of heavy metals and metalloids bioaccumulation in invertebrates and seaweeds from different marine coastal areas of Sardinia, Mediterranean Sea. Environmental Pollution 266: 115048.
Dehbi M, Dehbi F, Kanjal MI, Tahraoui H, Zamouche, M, ... Mouni L (2023) Analysis of heavy metal contamination in macroalgae from surface waters in Djelfa, Algeria. Water 15(5): 974.
Díaz-de-Alba M, Schweitzer ME, Riaño MDG, Casanueva-Marenco MJ (2021) Comprehensive assessment and potential ecological risk of trace element pollution (As, Ni, Co, and Cr) in aquatic environmental samples from an industrialized area. International Journal of Environmental Research and Public Health 18(14): 7348.
Dinulislam A, Sulistiono S, Lumbanbatu DTF, Affandi R (2021) Heavy metals (Pb, Hg) in blood cockle (Anadara granosa) in Cengkok Waters, Banten Bay, Indonesia. IOP Conference Series: Earth and Environmental Science 744(1): 012012.
Fonti V, Dell’Anno A, Beolchini F (2015) Biogeochemical interactions in the application of biotechnological strategies to marine sediments contaminated with metals. New Biotechnology 14(1): 12–31.
Fraser H, Barnett A, Parker TH, Fidler F (2020) The role of replication studies in ecology. Ecology and Evolution 10: 5197–5207.
Galib SM, Sun J, Twiss SD, Lucas MC (2022) Personality, density and habitat drive the dispersal of invasive crayfish. Scientific Reports 12: 1114.
Halit AL, Azman S, Said MIM, Alias N, Ali N (2018) Cadmium and chromium accumulation in cockles along the estuary of Sungai Tampok and Sungai Sanglang. IOP Conference Series: Materials Science and Engineering 1049(1): 012043.
Harith H, Husain ML, Akhir MF (2016) Coastal oceanographic processes associated with blood cockle (Anadara granosa) induce spawning season in Kapar, Selangor, Malaysia. Journal of Ocean and Earth Science 1(4): 289–299.
Ismui MI, Mohamat-Yusuff F, Joni AAM, Noor NAM, Mukhtar A, Zulkifli SZ (2020) Health status of blood cockle's Tegillarca granosa (Arcidae: Bivalva) from three different farms along the Strait of Malacca. Marine Research in Indonesia 45(1): 39–46.
JASP Team (2024) JASP (Version 0.18.3) [Computer software]. University of Amsterdam, The Netherlands.
Jung KR, Stelzenmüller V, Prowe AEF (2006) Spatial distribution of heavy metal concentrations and biomass indices in Cerastoderma edule Linnaeus (1758) from the German Wadden Sea: an integrated biomonitoring approach. Journal of Experimental Marine Biology and Ecology 338(1): 81–95.
Lebrun JD, Geffard O, Urien N, François A, Uher E, Fechner LC (2015) Seasonal variability and inter-species comparison of metal bioaccumulation in caged gammarids under urban diffuse contamination gradient: Implications for biomonitoring investigations. Science of the Total Environment 511: 501–508.
Liu Q, Xu X, Zeng J, Shi X, Liao Y, ... Shou L (2019) Heavy metal concentrations in commercial marine organisms from Xiangshan Bay, China, and the potential health risks. Marine Pollution Bulletin 141: 215–226.
Lovejoy DB (1999) Heavy metal concentrations in water, sediments and mollusc tissues. Ekologija 9(2): 12–20.
Lü J, Cao L, Dou S (2017) Bioaccumulation of heavy metals and health risk assessment in three benthic bivalves along the coast of Laizhou Bay, China. Marine Pollution Bulletin 117(1–2): 98–110.
Marques A, Piló D, Carvalho S, Araújo O, Guilherme S, ... Pereira P (2018) Metal bioaccumulation and oxidative stress profiles in Ruditapes philippinarum – Insights towards its suitability as bioindicator of estuarine metal contamination. Ecological Indicators 95: 1087–1099.
Miedico O, Pompa C, Tarallo M, Chiaravalle AE (2013) Assessment of heavy metals in bivalves molluscs of Apulian region: a 3-years control activity of a EU laboratory. E3S Web of Conferences 1: 11006.
Mohamat-Yusuff F, Shari MAM, Joni AAM, Kusin FM, Mohamed KN, ... Arshad A (2021) Health status comparison of blood cockle (Tegillarca granosa) between low and high yield farms in Selangor and Johor. IOP Conference Series: Earth and Environmental Science 934(1): 012048.
Mubiana VK, Blust R (2007) Effects of temperature on scope for growth and accumulation of Cd, Co, Cu, and Pb by the marine bivalve Mytilus edulis. Marine Environmental Research 63(3): 219–235.
Mustafa SA, Al-Rudainy AJ, Salman NM (2024) Effect of environmental pollutants on fish health: an overview. Egyptian Journal of Aquatic Research 50(2): 225–233.
Nanda P (2014) Bioaccumulation of heavy metals and physiological response in Anabas testudineus on exposure to paper mill effluent. Journal of Environmental & Analytical Toxicology 5(1): 1000244.
Naser HA (2013) Assessment and management of heavy metal pollution in the marine environment of the Arabian Gulf: a review. Marine Pollution Bulletin 72(1): 6–13.
Noorddin I (1995) Trace element content of Malaysian cockles (Anadara granosa). Food Chemistry 54: 133–155.
Pereira J, Raikar SS, Bhatti AG, Fatarpekar PG, Nasnodkar MR (2023) Metal bioavailability, bioaccumulation, and toxicity assessment through sediment and edible biota from intertidal regions of the Aghanashini Estuary, India. Marine Environmental Research 191: 106172.
Pérez-López M, Alonso J, Nóvoa-Valiñas MC, Melgar MJ (2003) Assessment of heavy metal contamination of seawater and marine limpet, Patella vulgata L., from northwest Spain. Journal of Environmental Science and Health, Part A 38(12: 2845–2856.
Piras P, Chessa G, Cossu M, Fiori G, Piras P, Ledda G (2013) Lead and other heavy metals (cadmium and mercury) accumulation in bivalve mollusks (Mytilus galloprovincialis, Ruditapes spp., and Crassostrea gigas) sampled in Sardinia in 2008-2012. Italian Journal of Food Safety 2(3): 49.
Rouane-Hacene O, Boutiba Z, Belhaouari B, Guibbolini M, Francour P, Faverney CR (2015) Seasonal assessment of biological indices, bioaccumulation, and bioavailability of heavy metals in mussels Mytilus galloprovincialis from Algerian west coast, applied to environmental monitoring. Oceanologia 57(4): 362–374.
Roveta C, Annibaldi A, Afghan A, Calcinai B, Camillo CGD, ... Puce S (2021) Biomonitoring of heavy metals: The unexplored role of marine sessile taxa. Applied Sciences 11(2): 580.
Ruíz-Fernández AC, Wu RS, Lau T, Pérez-Bernal LH, Sánchez-Cabeza J, Chiu JMY (2018) A comparative study on metal contamination in Estero de Urias lagoon, Gulf of California, using oysters, mussels and artificial mussels: Implications on pollution monitoring and public health risk. Environmental Pollution 243: 197–205.
Ruíz-Jarabo I, Amanajás RD, Baldisserotto B, Mancera J M, Val AL (2020) Tambaqui (Colossoma macropomum) acclimated to different tropical waters from the Amazon basin shows specific acute-stress responses. Comparative Biochemistry and Physiology, Part A: Molecular & Integrative Physiology 245: 110706.
Saavedra Y, González A, Blanco J (2009) Inter-individual distribution of metal concentrations in four marine bioindicator organisms and its use for optimal sampling design of a monitoring system. International Journal of Environmental Analytical Chemistry 89(8–12): 559–568.
Saffian NS, Chen P, Ilias N, Hwai ATS (2020) Overview and challenges of blood cockle culture in Malaysia. IOP Conference Series: Earth and Environmental Science 414(1): 012020.
Samsi N, Asaf R, Sahabuddin S, Santi A, Wamnebo MI (2017) Gastropods as a bioindicator and biomonitoring water pollution. Aquaculture Indonesia 18(1): 54.
Szefer P, Gełdon J, Ali AAM, Páez‐Osuna F, Ruíz-Fernández AC, Galvan S (1998) Distribution and association of trace metals in soft tissue and byssus of Mytella strigata and other benthal organisms from Mazatlan Harbour, Mangrove Lagoon of the northwest coast of Mexico. Environmental International 24(3): 359–374.
Velez C, Pires A, Sampaio L, Cardoso P, Moreira A, ... Freitas R (2016) The use of Cerastoderma glaucum as a sentinel and bioindicator species: take-home message. Ecological Indicators 62: 228–241.
Villagrán DM, Severini MF, Biancalana F, Spetter CV, Fernández EM, Marcovecchio JE (2019) Bioaccumulation of heavy metals in mesozooplankton from a human-impacted south western Atlantic estuary (Argentina). Journal of Marine Research 77(1): 217–241.
Wu J, Rong S, Wang M, Lu R, Liu J (2022) Environmental quality and ecological risk assessment of heavy metals in the Zhuhai Coast, China. Frontiers in Marine Science 9: 898423.
Yap CK, Ismail A, & Tan SG (2004) Heavy metal (Cd, Cu, Pb, and Zn) concentrations in the green-lipped mussel Perna viridis (L.) collected from some wild and aquacultural sites on the west coast of Peninsular Malaysia. Food Chemistry 84: 569–570.
Yap CK, Ismail A, Tan SG, Omar H (2002) Concentration of Cu and Pb in the offshore and intertidal sediments of the west coast of Peninsular Malaysia. Environment International 28: 467–479.
Copyright (c) 2024 The Author(s)
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
