Sardine and anchovy as bioindicators of metal content in Greek coastal waters


Published: Jun 21, 2022
Keywords:
metal pollution sardine anchovy bioindicators site-specific variations.
KATERINA SOFOULAKI
https://orcid.org/0000-0002-9276-2541
IOANNA KALANTZI
CHRISTINA ZERI
ATHANASIOS MACHIAS
SPIROS A. PERGANTIS
MANOLIS TSAPAKIS
https://orcid.org/0000-0002-9305-8441
Abstract

Metal and element concentrations (Li, Na, Mg, P, Ca, V, Mn, Fe, Co, Ni, Cu, Zn, Ga, As, Se, Rb, Sr, Mo, Pd, Cd, Cs, Ba, Hg, Tl, Pb, U) were monitored in the tissues of sardine (Sardina pilchardus) and anchovy (Engraulis encrasicolus) from six Greek coastal areas subjected to different natural and anthropogenic forcings in order to be assessed as bioindicator species of marine metal pollution. Sardine and anchovy provided a thorough view of the metal pollution load of each site in accordance with local pollution sources. The wide range of pressures applied in Elefsina Gulf and Thermaikos Gulf are depicted in the large number and the kind of elements reaching maximum concentrations among the sites (e.g. Pb, Cu, Hg, As in Elefsina Gulf, and Cd, Ni, P in Thermaikos Gulf) while in the rest of the sites (Amvrakikos Gulf, Strymonian Sea, Thracian Sea, Artemisium Straits), few elements were found at maximum levels. Statistically significant site-specific differences in metal content were detected. The differentiation in metal content of the fish tissues among the sites could be attributed to anthropogenic pressures, different background levels and environmental conditions. Sardine and anchovy can be evaluated as appropriate, reliable and useful bioindicator species of marine metal pollution.

Article Details
  • Section
  • Research Article
Downloads
Download data is not yet available.
References
Afandi, I., Talba, S., Benhra, A., Benbrahim, S., Chfiri, R. et al., 2018. Trace metal distribution in pelagic fish species from the north-west African coast (Morocco). International Aquatic Research, 10 (2), 191-205.
Ahdy, H.H.H., Abdallah, A.M., Tayel, F.T., 2007. Assessment of heavy metals and nonessential content of some edible and soft tissues. Egyptian Journal of Aquatic Research, 33, 85-97.
Albanis, T.A., Hela, D., Papakostas, G., Goutner, V., 1996. Concentration and bioaccumulation of organochlorine pesticide residues in herons and their prey in wetlands of Thermaikos Gulf, Macedonia, Greece. Science of the Total Environment, 182 (1), 11-19.
Basilone, G., Gargano, A., Corriero, A., Zupa, R., Santamaria, N. et al., 2018. Liver melanomacrophage centres and CYP1A expression as response biomarkers to environmental pollution in European anchovy (Engraulis encrasicolus) from the western Mediterranean Sea. Marine Pollution Bulletin, 131, 197-204.
Bat, L., Kaya, Y., Öztekin, H.C., 2014. Heavy metal levels in the Black Sea anchovy (Engraulis encrasicolus) as biomonitor and potential risk of human health. Turkish Journal of Fisheries and Aquatic Sciences, 14, 845-851.
Bonanno, G., Orlando-Bonaca, M., 2018. Perspectives on using marine species as bioindicators of plastic pollution. Marine Pollution Bulletin, 137, 209-221.
Boubonari, T., Malea, P., Kevrekidis, T., 2008. The green seaweed Ulva rigida as a bioindicator of metals (Zn, Cu, Pb and Cd) in a low-salinity coastal environment. Botanica Marina, 51 (6), 472-484.
Bradi, B.H. (Ed.), 2005. Heavy Metals in the Environment: Origin, Interaction and Remediation. Vol. 6. Elsevier Academic Press, Neubrucke, 269 pp.
Caçador, I., Costa, J.L., Duarte, B., Silva, G., Medeiros, J.P. et al., 2012. Macroinvertebrates and fishes as biomonitors of heavy metal concentration in the Seixal Bay (Tagus estuary): Which species perform better? Ecological Indicators, 19, 184-90.
Castro-González, M.I., Méndez-Armenta, M., 2008. Heavy metals: Implications associated to fish consumption. Environmental Toxicology and Pharmacology, 26 (3), 263-271.
Christophoridis, C., Dedepsidis, D., Fytianos, K., 2009. Occurrence and distribution of selected heavy metals in the surface sediments of Thermaikos Gulf, N. Greece. Assessment using pollution indicators. Journal of Hazardous Materials, 168 (2), 1082-1091.
Clarke, K.R., Warwick, R.M., 1994. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. Natural Environment Research Council, Plymouth Marine Laboratory, 144 pp.
Copat, C., Brundo, M.V., Arena, G., Grasso, A., Conti, G.O. et al., 2012a. Seasonal variation of bioaccumulation in Engraulis encrasicolus (Linneaus, 1758) and related biomarkers of exposure. Ecotoxicology and Environmental Safety, 86, 31-37.
Copat, C., Bella, F., Castaing, M., Fallico, R., Sciacca, S. et al. 2012b. Heavy metals concentrations in fish from Sicily (Mediterranean Sea) and evaluation of possible health risks to consumers. Bulletin of Environmental Contamination and Toxicology, 88 (1), 78-83.
Copat, C., Arena. G., Fiore, M., Ledda, C., Fallico, R. et al., 2013. Heavy metals concentrations in fish and shellfish from eastern Mediterranean Sea: Consumption advisories. Food and Chemical Toxicology, 53, 33-37.
Cunningham, P.A., Sullivan, E.E., Everett, K.H., Kovach, S.S., Rajan, A. et al., 2019. Assessment of metal contamination in Arabian/Persian Gulf fish: A review. Marine Pollution Bulletin, 143, 264-283.
Djedjibegovic, J., Larssen, T., Skrbo, A., Marjanovic, A., Sober, M., 2012. Contents of cadmium, copper, mercury and lead in fish from the Neretva River (Bosnia and Herzegovina) determined by inductively coupled plasma mass spectrometry (ICP-MS). Food Chemistry, 131, 469-476.
Doray, M., Petitgas, P., Huret, M., Duhamel, E., Romagnan, J.B. et al., 2018. Monitoring small pelagic fish in the Bay of Biscay ecosystem, using indicators from an integrated survey. Progress in Oceanography, 166, 168-188.
EEA [European Environment Agency], 2015. WISE WFD Database. http://www.eea. europa.eu/data-and-maps/data/ wise wfd (Accessed 12 June 15).
Galitsopoulou, A., Georgantelis, D., Kontominas, M., 2012. The influence of industrial-scale canning on cadmium and lead levels in sardines and anchovies from commercial fishing centres of the Mediterranean Sea. Food Additives & Contaminants: Part B, 5 (1), 75-81.
Ganias, K. (Ed.), 2014. Biology and Ecology of Sardines and Anchovies. CRC Press, Boca Raton, 394 pp.
Guerranti, C., Grazioli, E., Focardi, S., Renzi, M., Perra, G., 2016. Levels of chemicals in two fish species from four Italian fishing areas. Marine Pollution Bulletin, 111 (1), 449-452.
Harris, J.H., 1995. The use of fish in ecological assessments. Austral Ecology, 20 (1), 65-80.
Hayase, D., Horai, S., Isobe, T., William, T., Takahashi, S. et al., 2009. Monitoring trace elements in coastal waters using sardine as a bioindicator. p. 167-175. In: Interdisciplinary Studies on Environmental Chemistry-Environmental Research in Asia. Obayashi, Y., Isobe, T., Subramanian A., Suzuki S., Tanabe S. (Eds). TERRAPUB, Japan.
Kalantzi, I., Black, K.D., Pergantis, S.A., Shimmield, T.M., Papageorgiou, N. et al., 2013. Metals and other elements in tissues of wild fish from fish farms and comparison with farmed species in sites with oxic and anoxic sediments. Food Chemistry, 141, 680-694.
Kalogeropoulos, N., Karavoltsos, S., Sakellari, A., Avramidou, S., Dassenakis, M. et al., 2012. Heavy metals in raw, fried and grilled Mediterranean finfish and shellfish. Food and Chemical Toxicology, 50, 3702-3708.
Karageorgis, A.P., Sioulas, A., Anagnostou, C.L., 2002. Use of surface sediments in Pagasitikos Gulf, Greece, to detect anthropogenic influence. Geo-Marine Letters, 21 (4), 200- 211.
Karageorgis, A.P., 2007. Geochemical study of sediments from the Amvrakikos Gulf lagoon complex, Greece. Transitional Waters Bulletin, 1 (3), 3-8.
Karageorgis, A.P., Botsou, F., Kaberi, H., Iliakis, S., 2020. Geochemistry of major and trace elements in surface sediments of the Saronikos Gulf (Greece): assessment of contamination between 1999 and 2018. Science of the Total Environment, 717, 137046.
Karaouzas, I., Kapetanaki, N., Mentzafou, A., Kanellopoulos, T.D., Skoulikidis, N., 2021. Heavy Metal Contamination Status in Greek Surface Waters; a review with application and evaluation of pollution indices. Chemosphere, 263, 128192.
Li, L., Zheng, B., Liu, L., 2010. Biomonitoring and bioindicators used for river ecosystems: definitions, approaches and trends. Procedia environmental sciences, 2, 1510-1524.
Longo, G., Trovato, M., Mazzei, V., Ferrante, M., Conti, G.O., 2013. Ligia italica (Isopoda, Oniscidea) as bioindicator of mercury pollution of marine rocky coasts. PloS one, 8 (3), e58548.
Lozano-Bilbao, E., Clemente, S., Espinosa, J.M., Jurado-Ruzafa, A., Lozano, G. et al., 2019. Inferring trophic groups of fish in the central-east Atlantic from eco-toxicological characterization. Chemosphere, 229, 247-255.
Maanan, M., 2008. Heavy metal concentrations in marine molluscs from the Moroccan coastal region. Environmental Pollution, 153, 176-183.
Malea, P., Mylona, Z., Kevrekidis, T., 2019. Trace elements in the seagrass Posidonia oceanica: Compartmentation and relationships with seawater and sediment concentrations. Science of the total environment, 686, 63-74.
Martín, P., Bahamon, N., Sabatés, A., Maynou, F., Sánchez, P. et al., 2008. European anchovy (Engraulis encrasicolus) landings and environmental conditions on the Catalan Coast (NW Mediterranean) during 2000–2005. Hydrobiologia, 612 (1), 185-199.
Maulvault, A.L., Anacleto, P., Barbosa, V., Sloth, J.J., Rasmussen, R.R. et al., 2015. Toxic elements and speciation in seafood samples from different contaminated sites in Europe. Environmental research, 143, 72-81.
Mehana, E.S.E., Khafaga, A.F., Elblehi, S.S., El-Hack, A., Mohamed, E. et al., 2020. Biomonitoring of heavy metal pollution using acanthocephalans parasite in ecosystem: an updated overview. Animals, 10 (5), 811.
Metian, M., Warnau, M., Chouvelon, T., Pedraza, F., Rodriguez y Baena, A.M. et al., 2013. Trace element bioaccumulation in reef fish from New Caledonia: Influence of trophic groups and risk assessment for consumers. Marine Environmental Research, 87-88, 26-36.
Nadal, M., Ferré-Huguet, N., Martí-Cid, R., Schuhmacher, M., Domingo, J.L., 2008. Exposure to Metals through the Consumption of Fish and Seafood by the Population Living Near the Ebro River in Catalonia, Spain: Health Risks. Human and Ecological Risk Assessment: An International Journal, 14, 780-795.
Nikolioudakis, N., Isari, S., Somarakis, S., 2014. Trophodynamics of anchovy in a non-upwelling system: direct comparison with sardine. Marine Ecology Progress Series, 500, 215-229.
Nunes, B.S., Travasso, R., Gonçalves, F., Castro, B.B., 2015. Biochemical and physiological modifications in tissues of Sardina pilchardus: spatial and temporal patterns as a baseline for biomonitoring studies. Frontiers in environmental science, 3, 7.
O’Callaghan, I., Harrison, S., Fitzpatrick, D., Sullivan, T., 2019. The freshwater isopod Asellus aquaticus as a model biomonitor of environmental pollution: A review. Chemosphere, 235, 498-509.
Paraskevopoulou, V., Zeri, C., Kaberi, H., Chalkiadaki, O., Krasakopoulou, E. et al., 2014. Trace metal variability, background levels and pollution status assessment in line with the water framework and Marine Strategy Framework EU Directives in the waters of a heavily impacted Mediterranean Gulf. Marine Pollution Bulletin, 87, 323-337.
Parra-Luna, M., Martín-Pozo, L., Hidalgo, F., Zafra-Gómez, A., 2020. Common sea urchin (Paracentrotus lividus) and sea cucumber of the genus Holothuria as bioindicators of pollution in the study of chemical contaminants in aquatic media. A revision. Ecological Indicators, 113, 106185.
Pavlidou, A., Simboura, N., Rousselaki, E., Tsapakis, M., Pagou, K., 2015. Methods of eutrophication assessment in the context of the water framework directive: examples from the Eastern Mediterranean coastal areas. Continental Shelf Research, 108, 156-168.
Pavlidou, A., Simboura, N., Pagou, Κ., Assimakopoulou, G., Gerakaris, V. et al., 2019. Using a holistic ecosystem-integrated approach to assess the environmental status of Saronikos Gulf, Eastern Mediterranean. Ecological Indicators, 96, 336-350.
Pitta, E., Zeri, C., Tzortziou, M., Dimitriou, E., Paraskevopoulou, V. et al., 2014. Dissolved organic matter cycling in eastern Mediterranean rivers experiencing multiple pressures. The case of the trans-boundary Evros River. Mediterranean Marine Science, 15 (2), 398-415.
Rainbow, P.S., 1995. Biomonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin, 31 (4-12), 183-192.
Rideout, K., Kosatsky, T., 2017. Fish for dinner? Balancing risks, benefits, and values in formulating food consumption advice. Risk Analysis, 37 (11), 2041-2052.
Romero, J., Martínez-Crego, B., Alcoverro, T., Pérez, M., 2007. A multivariate index based on the seagrass Posidonia oceanica (POMI) to assess ecological status of coastal waters under the water framework directive (WFD). Marine Pollution Bulletin, 55 (1), 196-204.
Saha, M., Sarkar, S. K., Bhattacharya, B., 2006. Interspecific variation in heavy metal body concentrations in biota of Sunderban mangrove wetland, northeast India. Environment International, 32, 203-207.
Salvaggio, A., Pecoraro, R., Copat, C., Ferrante, M., Grasso, A. et al., 2020. Bioaccumulation of Metals/Metalloids and Histological and Immunohistochemical Changes in the Tissue of the European Hake, Merluccius (Linneaus, 1758) (Pisces: Gadiformes: Merlucciidae), for Environmental Pollution Assessment. Journal of Marine Science and Engineering, 8 (9), 712.
Sarkar, S.K., Cabral, H., Chatterjee, M., Cardoso, I., Bhattacharya, A.K. et al., 2008. Biomonitoring of Heavy Metals Using the Bivalve Molluscs in Sunderban Mangrove Wetland, Northeast Coast of Bay of Bengal (India): Possible Risks to Human Health. Clean, 36 (2), 187-194.
Savoca, S., Bottari, T., Fazio, E., Bonsignore, M., Mancuso, M. et al., 2020. Plastics occurrence in juveniles of Engraulis encrasicolus and Sardina pilchardus in the Southern Tyrrhenian Sea. Science of The Total Environment, 718, 137457.
Scoullos, M., Dassenakis, M., Zeri, C., 1996. Trace metal behaviour during summer in a stratified Mediterranean system: The Louros estuary (Greece). Water, Air, & Soil Pollution, 88 (3), 269-295.
Scoullos, M., Dassenakis, M., Paraskevopoulou, V., Botsou, F., Sakellari, A. et al., 2015. Trace metals in seawater and sediments of the Gulf of Elefsis: (1977–2015). p. 11-12. In: Proceedings of the International Conference “Environmental Perspectives of the Gulf of Elefsis. A Mediterranean Case Study where Science meets Society”, Elefsis, Greece, 11-12 September 2015.
Simboura, N., Pavlidou, A., Bald, J., Tsapakis, M., Pagou, K. et al., 2016. Response of ecological indices to nutrient and chemical contaminant stress factors in Eastern Mediterranean coastal waters. Ecological Indicators, 70, 89-105.
Skoulikidis, N.T., 2009. The environmental state of rivers in the Balkans - a review within the DPSIR framework. Science of the Total Environment, 407 (8), 2501-2516.
Sofoulaki, K., Kalantzi, I., Machias, A., Mastoraki, M., Chatzifotis, S. et al., 2018. Metals and elements in sardine and anchovy: Species specific differences and correlations with proximate composition and size. Science of the Total Environment, 645, 329-338.
Sofoulaki, K., Kalantzi, I., Machias, A., Pergantis, S.A., Tsapakis, M., 2019. Metals in sardine and anchovy from Greek coastal areas: Public health risk and nutritional benefits assessment. Food and Chemical Toxicology, 123, 113-124.
Stamatis, N., Ioannidou, D., Christoforidis, A., Koutrakis, E., 2002. Sediment pollution by heavy metals in the Strymonikos and Ierissos gulfs, North Aegean Sea, Greece. Environmental Monitoring and Assessment, 80 (1), 33-49.
Strogyloudi, E., Pancucci-Papadopoulou, M.A., Papadopoulos, G.L., 2014. Metal and metallothionein concentrations in Paracentrotus lividus from Amvrakikos gulf (Ionian Sea- Greece). Environmental monitoring and assessment, 186 (9), 5489-5499.
Sylaios, G., Koutrakis, E., Kallianiotis, A., 2006. Hydrographic variability, nutrient distribution and water mass dynamics in Strymonikos Gulf (Northern Greece). Continental Shelf Research, 26 (2), 217-235.
Tsangaris, C., Cotou, E., Papathanassiou, E., Nicolaidou, A., 2010. Assessment of contaminant impacts in a semi-enclosed estuary (Amvrakikos Gulf, NW Greece): Bioenergetics and biochemical biomarkers in mussels. Environmental Monitoring and Assessment, 161 (1-4), 259-269.
Tsangaris, C., Kaberi, H., Catsiki, V.A., 2013. Metal levels in sediments and transplanted mussels in Pagasitikos Gulf (Aegean Sea, Eastern Mediterranean). Environmental Monitoring and Assessment, 185 (7), 6077-6087.
Tzempelikou, E., Zeri, C., Iliakis, S., Paraskevopoulou, V., 2021. Cd, Co, Cu, Ni, Pb, Zn in coastal and transitional waters of Greece and assessment of background concentrations: Results from 6 years implementation of the Water Framework Directive. Science of the Total Environment, 774, 145177.
USEPA [United States Environmental Protection Agency], 1991. Regional Guidance on Handling Chemical Concentration Data Near the Detection Limit in Risk Assessments. https://www.epa.gov/risk/regional-guidance- handling-chemical-concentration-data-near-detection- limit-risk-assessments (Accessed 7 June 2022)
USEPA [United States Environmental Protection Agency], 1996. Method 3052: Microwave assisted acid digestion of sediments, sludges, soils and oils. Test Methods for Evaluating Solid Waste, Physical/Chemical Methods - SW-846, Washington DC, 20 pp.
USEPA [United States Environmental Protection Agency], 2000. Guidance for assessing chemical contaminant data for use in fish advisories. Fish Sampling and Analysis, Volume 1, Third Edition, 485 pp.
Uysal, K., Emre, Y., Köse, E., 2008. The determination of heavy metal accumulation ratios in muscle, skin and gills of some migratory fish species by inductively coupled plasma-optical emission spectrometry (ICP-OES) in Beymelek Lagoon (Antalya/Turkey). Microchemical Journal, 90, 67-70.
Vasileiadou, K., Pavloudi, C., Kalantzi, I., Apostolaki, E.T., Chatzigeorgiou, G. et al., 2016. Environmental variability and heavy metal concentrations from five lagoons in the Ionian Sea (Amvrakikos Gulf, W Greece). Biodiversity Data Journal, 4, e8233.
Vlahogianni, T., Dassenakis, M., Scoullos, M.J., Valavanidis, A., 2007. Integrated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals’ pollution in coastal areas from the Saronikos Gulf of Greece. Marine Pollution Bulletin, 54 (9), 1361-1371.
Voutsinou‐Taliadouri, F., Balopoulos, E.T., 1991. Geochemical and physical oceanographic aspects of the Amvrakikos Gulf (Ionian Sea, Greece). Toxicological & Environmental Chemistry, 31 (1), 177-185.
Whitfield, A.K., Elliott, M., 2002. Fishes as indicators of environmental and ecological changes within estuaries: A review of progress and some suggestions for the future. Journal of Fish Biology, 61 (sA), 229-250.
Zhou, Q., Zhang, J., Fu, J., Shi, J., Jiang, G., 2008. Biomonitoring: An appealing tool for assessment of metal pollution in the aquatic ecosystem. Analytica Chimica Acta, 606 (2), 135-150.