Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-30T20:14:58.489Z Has data issue: false hasContentIssue false
  • English
  • Français

Benthic organisms as ecological indicators for the status assessment of coastal ecosystems

Published online by Cambridge University Press:  24 August 2017

D. Komar ,
M. Dolenec ,
T. Dolenec ,
P. Vrhovnik ,
S. Lojen ,
G. Kniewald ,
S.S. Matešić ,
Ž. Lambaša Belak  and
M. Orlando-Bonaca
D. Komar*
Affiliation:
Geoexp, d. o. o., Company for Scientific Research and Developement in the Field of Geology, Geochemistry and Environmental Protection, Slap 21, 4290 Tržič, Slovenia ARGE Geopark Karawanken, Hauptplatz 7, 9135 Bad Eisenkappel, Austria
M. Dolenec
Affiliation:
Department of Geology, Faculty of Natural Sciences and Engineering, University of Ljubljana, Aškerčeva 12, 1000 Ljubljana, Slovenia
T. Dolenec
Affiliation:
Geoexp, d. o. o., Company for Scientific Research and Developement in the Field of Geology, Geochemistry and Environmental Protection, Slap 21, 4290 Tržič, Slovenia
P. Vrhovnik
Affiliation:
Geoexp, d. o. o., Company for Scientific Research and Developement in the Field of Geology, Geochemistry and Environmental Protection, Slap 21, 4290 Tržič, Slovenia Slovenian National Building and Civil Engineering Institute, Dimičeva ulica 12, 1000 Ljubljana, Slovenia
S. Lojen
Affiliation:
Department of Environmental Sciences, Jožef Stefan Institute, Jamova 39, 1000 Ljubljana, Slovenia Faculty of Environmental Sciences, University of Nova Gorica, Vipavska 13, 5000 Nova Gorica, Slovenia
G. Kniewald
Affiliation:
Ruđer Bošković Institute, Bijenička 54, 10000 Zagreb, Croatia
S.S. Matešić
Affiliation:
Department of Environment and Municipal Affairs, Trg Pavla Šubica I no. 2, 22000 Šibenik, Croatia
Ž. Lambaša Belak
Affiliation:
Department of Environment and Municipal Affairs, Trg Pavla Šubica I no. 2, 22000 Šibenik, Croatia
M. Orlando-Bonaca
Affiliation:
Marine Biology Station Piran, National Institute of Biology, Fornače 41, 6330 Piran, Slovenia
*
Correspondence should be addressed to: D. Komar, Geoexp, d. o. o., Company for Scientific Research and Development in the Field of Geology, Geochemistry and Environmental Protection, Slap 21, 4290 Tržič, Slovenia Email: [email protected], [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The presence of potentially toxic elements (PTE) was determined in different tissues of five selected marine organisms. The As, Cd, Cu, Mn, Mo, Ni, Pb and Zn concentrations were measured in the seagrass Cymodocea nodosa, the green alga Cladophora echinus, the red alga Gelidiella lubrica, the marine topshell Phorcus turbinatus and the littoral crab Carcinus aestuarii, as well as in seawater from Makirina Bay. The levels of As, Cd, Cu, Mn and Zn in the biota were found to exceed those in previously analysed sediments, indicating the bioaccumulation of these PTE. The biota-sediment accumulation factor (BSAF) and concentration factor (CF) varied among different organisms. As regards the five selected species, C. nodosa, C. echinus and G. lubrica proved to be the strongest accumulators of Mn, while P. turbinatus and C. aestuarii showed a high capacity to accumulate As, Cd, Cu and Zn. These species can be considered as good ecological indicators in the assessment of PTE pollution in marine littoral environments.

Keywords

Bioaccumulationpotentially toxic elements (PTE)coastal environmentenvironmental healthbiota-sediment accumulation factor (BSAF)contamination factor (CF)benthic organismsstable isotopes (δ15N)
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Special Issue 8: Special Section: European Marine Biology Symposium Papers 2018 , December 2018 , pp. 1907 - 1917
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Al-Busaidi, M., Yesudhason, P., Al-Waili, A., Al-Rahbi, W., Al-Harthy, K., Al-Mazrooei, N. and Al-Habsi, S. (2013) Accumulation of some potentially toxic metals and polycyclic aromatic hydrocarbons (PAHs) in marine clam Liochoncha ornata collected from the Omani Sea. International Journal of Fisheries and Aquaculture 5, 238–247.Google Scholar
Ali, R.A.S. and Bream, A.S. (2010) The effects of sewage discharge on the marine gastropod Gibbula sp., collected from the coast of Al-Hanyaa, Libya. Egyptian Academic Journal of Biological Sciences 2, 47–52.Google Scholar
Atanasov, V., Valkova, E., Kostadinova, G., Petkov, G., Yablanski, T.S., Valkova, P. and Dermendjieva, D. (2013) Manganese levels in water, sediment and algae from waterbodies with high anthropogenic impact. Agricultural Science and Technology 5, 206–211.Google Scholar
Avelar, W.E.P., Mantelatto, F.L.M., Tomazelli, A.C., Silva, D.M.L., Shuhama, T. and Lopes, J.L.C. (2000) The marine mussel Perna perna (Mollusca, Bivalvia, Mytilidae) as an indicator of contamination by heavy metals in the Ubatuba Bay, São Paulo, Brazil. Water, Air, and Soil Pollution 118, 65–72.Google Scholar
Bille, L., Binato, G., Cappa, V., Toson, M., Pozza, M.D., Arcangeli, G., Ricci, A., Angeletti, R. and Piro, A. (2015) Lead, mercury and cadmium levels in edible marine molluscs and echinoderms from the Veneto Region (north-western Adriatic Sea – Italy). Food Control 50, 362–370.Google Scholar
Bogdanović, T., Ujević, I., Sedak, M., Listeš, E., Šimat, V., Petričević, S. and Poljak, V. (2014) As, Cd, Hg and Pb in four edible shellfish species from breeding and harvesting areas along the eastern Adriatic Coast, Croatia. Food Chemistry 146, 197–203.Google Scholar
Bradl, H.B. (2005) Heavy metals in the environments: origin, interaction and remediation. Amsterdam: Elsevier.Google Scholar
Bustamante, P., Cosson, R.P., Gallien, I., Caurant, F. and Miramand, P. (2002) Cadmium detoxification processes in the digestive gland of cephalopods in relation to accumulated cadmium concentrations. Marine Environmental Research 53, 227–241.Google Scholar
Campanella, L., Conti, M.E., Cubadda, F. and Sucapane, C. (2001) Trace metals in seagrass, algae and molluscs from an uncontaminated area in the Mediterranean. Environmental Pollution 111, 117–126.Google Scholar
Catsiki, V.A. and Panayotidis, P. (1993) Copper, chromium and nickel in tissues of the Mediterranean seagrasses Posidonia oceanica and Cymodocea nodosa (Potamogetonaceae) from Greek coastal areas. Chemosphere 26, 963–978.Google Scholar
Conti, M.E., Bocca, B., Iacobucci, M., Finoia, M.G., Mecozzi, M., Pino, A. and Alimonti, A. (2010) Baseline trace metals in seagrass, algae, and mollusks in a Southern Tyrrhenian ecosystem (Linosa Island, Sicily). Archives of Environmental Contamination and Toxicology 58, 79–95.Google Scholar
Conti, M.E. and Cecchetti, G. (2003) A biomonitoring study: trace metals in algae and molluscs from Tyrrhenian coastal areas. Environmental Research 93, 99–112.Google Scholar
Conti, M.E., Tudino, M.B., Muse, J.O. and Cecchetti, G.F. (2002) Biomonitoring of heavy metals and their species in the marine environment: the contribution of atomic absorption spectroscopy and inductively coupled plasma spectroscopy. Trends in Applied Spectroscopy 4, 295–324.Google Scholar
Cravo, A., Bebianno, M.J. and Foster, P. (2004) Partitioning of trace metals between soft tissues and shells of Patella aspera. Environment International 30, 87–98.Google Scholar
Cubadda, F., Conti, M.E. and Campanella, L. (2001) Size-dependent concentrations of trace metals in four Mediterranean gastropods. Chemosphere 45, 561–569.Google Scholar
Dallinger, R. (1993) Strategies of metal detoxification in terrestrial invertebrates. In Dallinger, R. and Rainbow, P.S. (eds) Ecotoxicology of metals in invertebrates. Boca Raton, FL: Lewis Publisher, pp. 245–289.Google Scholar
Dolenec, M., Žvab, P., Mihelčić, G., Lambaša Belak, Ž., Lojen, S., Kniewald, G., Dolenec, T. and Rogan Šmuc, N. (2011) Use of stable nitrogen isotope signatures of anthropogenic organic matter in the coastal environment: a case study of the Kosirina Bay (Murter Island, Croatia). Geologia Croatica 64, 143–152.Google Scholar
Dolenec, T., Lojen, S., Kniewald, G., Dolenec, M. and Rogan, N. (2007) Nitrogen stable isotope composition as a tracer of fish farming in invertebrates Aplysina aerophoba, Balanus perforatus and Anemonia sulcata in central Adriatic. Aquaculture 262, 237–249.Google Scholar
Dolenec, T., Lojen, S., Lambaša, Ž. and Dolenec, M. (2006) Effects of fish loading on sea grass Posidonia oceanica at Vrgada Island (Central Adriatic): a nitrogen stable isotope study. Isotopes in Environmental and Health Studies 42, 77–85.Google Scholar
Dolenec, T., Vokal, B. and Dolenec, M. (2005) Nitrogen – 15 signals of anthropogenic nutrient loading in Anemonia sulcata as a possible indicator of human sewage impacts on marine coastal ecosystems: a case study of Pirovac Bay and the Murter Sea (Central Adriatic). Croatica Chemica Acta 78, 593–600.Google Scholar
Duysak, Ö. and Ersoy, B. (2014) A biomonitoring study: heavy metals in Monodonta turbinata (Mollusca: Gastropoda) from Iskenderun Bay, North-Eastern Mediterranean. Pakistan Journal of Zoology 46, 1317–1322.Google Scholar
El-Din, N.G.S. and El-Sherif, Z.M. (2013) Nutritional value of Cymodocea nodosa and Posidonia oceanica along the western Egyptian Mediterranean coast. Egyptian Journal of Aquatic Research 39, 153–165.Google Scholar
Engel, D.W. and Fowler, B.A. (1979) Factors influencing cadmium accumulation and its toxicity to marine organisms. Environmental Health Perspectives 28, 81–88.Google Scholar
Ergűl, H.A. and Aksan, S. (2013) Evaluation of non-essential element and micronutrient concentrations in seafood from the Marmara and Black Seas. Journal of Black Sea/Mediterranean Environment 13, 312–331.Google Scholar
Fry, B. (1988) Food web structure on Georges Bank from stable C, N, and S isotopic compositions. Limnology and Oceanography 33, 1182–1190.Google Scholar
Gavrilović, A., Srebočan, E., Petrinec, Z., Pompe-Gotal, J. and Prevendar-Crnić, A. (2004) Evaluation of concentrations of heavy metals in oysters and mussels of Mali Ston region. Our Sea 51, 50–58.Google Scholar
Ghrefat, H. and Yusuf, N. (2006) Assessing Mn, Fe, Cu, Zn and Cd pollution in bottom sediments of Wadi Al-Arab Dam, Jordan. Chemosphere 65, 2114–2121.Google Scholar
Gray, J.S. (2002) Biomagnification in marine systems: the perspective of an ecologist. Marine Pollution Bulletin 45, 46–52.Google Scholar
Gundacker, C. (2000) Comparison of heavy metal bioaccumulation in freshwater molluscs of urban river habitats in Vienna. Environmental Pollution 110, 61–71.Google Scholar
Hosseini, M., Bagher Nabavi, S.M., Pazooki, J. and Parsa, Y. (2014) The levels of toxic metals in blue crab Portunus segnis from Persian gulf. Journal of Marine Science: Research and Development 4, 1–5.Google Scholar
Jakimska, A., Konieczka, P., Skóra, K. and Namieśnik, J. (2011) Bioaccumuation of metals in tissues of marine animals, part I: the role and impact of heavy metals on organisms. Polish Journal of Environmental Studies 20, 1117–1125.Google Scholar
Jitar, O., Teodosiu, C., Oros, A., Plavan, G. and Nicoara, M. (2015) Bioaccumulation of heavy metals in marine organisms from the Romanian sector of the Black Sea. New Biotechnology 32, 369–378.Google Scholar
Khristoforova, N.K. and Chernova, E.N. (2005) Comparison of the content of heavy metals in brown algae and seagrasses. Doklady Biological Sciences 400, 61–63.Google Scholar
Kljaković-Gašpić, Z., Antolić, B., Zvonarić, T. and Barić, A. (2004) Distribution of cadmium and lead in Posidonia oceanica (l.) Delile from the middle Adriatic Sea. Fresenius Environmental Bulletin 13, 1210–1215.Google Scholar
Kljaković-Gašpić, Z., Ujević, I., Zvonarić, T. and Barić, A. (2007) Biomonitoring of trace metals (Cu, Cd, Cr, Hg, Pb, Zn) in Mali Ston Bay (eastern Adriatic) using the Mediterranean blue mussel (1998–2005). Acta Adriatica 48, 73–88.Google Scholar
Komar, D., Dolenec, M., Lambaša Belak, Ž., Matešić, S.S., Lojen, S., Kniewald, G., Vrhovnik, P., Dolenec, T. and Rogan Šmuc, N. (2015a) Geochemical characterization and environmental status of Makirina Bay sediments (northern Dalmatia, Republic of Croatia). Geologia Croatica 68, 79–92.Google Scholar
Komar, D., Dolenec, T., Dolenec, M., Vrhovnik, P., Lojen, S., Lambaša Belak, Ž., Kniewald, G. and Rogan Šmuc, N. (2015b) Physico-chemical and geochemical characterization of Makirina Bay peloid mud (N Dalmatia, Republic of Croatia) and its evaluation for potential use in balneotherapy. Indian Journal of Traditional Knowledge 14, 5–12.Google Scholar
Komar, D., Dolenec, T., Vrhovnik, P., Rogan Šmuc, N., Lojen, S., Kniewald, G., Matešić, S.S., Lambaša Belak, Ž. and Dolenec, M. (2014) Makirina bay peloid (N Dalmatia, Republic of Croatia) – its potential use in balneotherapy. Geologija 57, 167–175.Google Scholar
Kortatsi, B.K., Anku, Y.S.A. and Anornu, G.K. (2009) Characterization and appraisal of facets influencing geochemistry of groundwater in the Kulpawn sub-basin of the White Volta Basin, Ghana. Environmental Geology 58, 1349–1359.Google Scholar
Kumar Gupta, S. and Singh, J. (2011) Evaluation of mollusc as sensitive indicator of heavy metal pollution in aquatic system: a review. Official Journal of Institute of Integrative Omics and Applied Biotechnology 2, 49–57.Google Scholar
Lafabrie, C., Pergent, G., Kantin, R., Pergent-Martini, C. and Gonzales, J.L. (2007) Trace metals assessment in water, sediment, mussel and seagrass species – validation of the use of Posidonia oceanica as a metal biomonitor. Chemosphere 68, 2033–2039.Google Scholar
Lepoint, G., Dauby, P. and Gobert, S. (2004) Applications of C and N stable isotopes to ecological and environmental studies in seagrass ecosystems. Marine Pollution Bulletin 49, 887–891.Google Scholar
Li, L. and Huang, X. (2012) Three tropical seagrasses as potential bio-indicators to trace metals in Xincun Bay, Hainan Island, South China. Chinese Journal of Oceanology and Limnology 30, 212–224.Google Scholar
Llagostera, I., Perez, M. and Romero, J. (2011) Trace metal content in the seagrass Cymodocea nodosa: differential accumulation in plant organs. Aquatic Botany 95, 124–128.Google Scholar
Lojen, S., Spanier, E., Tsemel, A., Katz, T., Eden, N. and Angel, D.L. (2005) δ15N as a natural tracer of particulate nitrogen effluents released from marine aquaculture. Marine Biology 148, 87–96.Google Scholar
Maher, W. and Butler, E. (1988) Arsenic in the marine environment. Applied Organometallic Chemistry 2, 191–214.Google Scholar
Malea, P. and Haritonidis, S. (1999) Cymodocea nodosa (Ucria) Aschers. as a bioindicator of metals in Thermaikos Gulf, Greece, during monthly samplings. Botanica Marina 42, 419–430.Google Scholar
Malea, P. and Kevrekidis, T. (2013) Trace element (Al, As, B, Ba, Cr, Mo, Ni, Se, Sr, Tl, U and V) distribution and seasonality in compartments of the seagrass Cymodocea nodosa. Science of the Total Environment 463–464, 611–623.Google Scholar
McCutchan, J.H., Lewis, W.M., Kendall, C. and MacGrath, C.C. (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102, 378–390.Google Scholar
Miko, S., Koch, G., Mesić, S., Šparica-Miko, M., Šparica, M., Čepelak, R., Bačani, A., Vreča, P., Dolenec, T. and Bergant, S. (2008) Anthropogenic influence on trace element geochemistry of healing mud (peloid) from Makirina Cove (Croatia). Environmental Geology 55, 517–537.Google Scholar
Neff, J.M. (2002) Arsenic in the ocean. In Neff, J.M. (ed) Bioaccumulation in marine organisms. Effect of contaminants from oil-well produced water. Oxford: Elsevier, pp. 57–78.Google Scholar
Nemati, K., Abu Bakar, N.K., Abas, M.R. and Sobhanzadeh, E. (2011) Speciation of heavy metals by modified BCR sequential extraction procedure in different depths of sediments from Sunghai Buloh, Malaysia. Journal of Hazardous Materials 192, 402–410.Google Scholar
Nicolaidou, A. and Nott, J.A. (1998) Metals in sediment, seagrass and gastropods near a nickel smelter in Greece: possible interactions. Marine Pollution Bulletin 36, 360–365.Google Scholar
Noss, R.F. (1990) Indicators for monitoring biodiversity: a hierarchical approach. Conservation Biology 4, 355–264.Google Scholar
Oana, M.P. (2006) Chromium impact on marine ecosystem. Bulletin USAMV-CN 63, 379–384.Google Scholar
Pereira Majer, A., Varella Petti, M.A., Navajas Corbisier, T., Portella Ribeiro, A., Sawamura Theophilo, C.Y., de Lima Ferreira, P.A. and Lopes Figueira, R.C. (2014) Bioaccumulation of potentially toxic trace elements in benthic organisms of Admiralty Bay (King George Island, Antarctica). Marine Pollution Bulletin 79, 321–325.Google Scholar
Ponnusamy, K., Sivaperumal, P., Suresh, M., Arularasan, S., Munilkumar, S. and Pal, A.K. (2014) Heavy metal concentration from biologically important edible species of bivalves (Perna viridis and Modiolus metcalfei) from Vellar estuary, south east coast of India. Journal of Aquaculture Research and Development 5, 1–5.Google Scholar
Ravera, O., Beone, G.M., Trincherini, P.R. and Riccardi, N. (2007) Seasonal variations in metal content of two Unio pictorum mancus (Mollusca, Unionidae) populations from two lakes of different trophic state. Journal of Limnology 66, 28–39.Google Scholar
Ravera, O., Cenci, R., Beone, G.M., Dantas, M. and Lodigiani, P. (2003) Trace element concentrations in freshwater mussels and macrophytes as related to those in their environment. Journal of Limnology 62, 61–70.Google Scholar
Sanz-Lázaro, C., Malea, P., Apostolaki, E.T., Kalantzi, I., Marín, A. and Karakassis, I. (2012) The role of the seagrass Posidonia oceanica in the cycling of trace elements. Biogeosciences 9, 2497–2507.Google Scholar
Shakeri, A., Shakeri, R. and Mehrabi, B. (2015) Potentially toxic elements and persistent organic pollutants in water and fish at Shahid Rajaei Dam, north of Iran. International Journal of Environmental Science and Technology 12, 2201–2212.Google Scholar
Šparica, M., Koch, G., Belak, M., Miko, S., Šparica-Miko, M., Viličić, D., Dolenec, T., Bergant, S., Lojen, S., Vreča, P., Dolenec, M., Ogrinc, N. and Ibrahimpašić, H. (2005) Recent sediments of Makirina cove (Northern Dalmatia, Croatia): their origin viewed through a multidisciplinary approach. Geologia Croatica 58, 21–72.Google Scholar
Szefer, P., Ali, A.A., Ba-Haroon, A.A., Rajeh, A.A., Gełdon, J. and Nabrzyski, M. (1999) Distribution and relationships of selected trace metals in molluscs and associated sediments from the Gulf of Aden, Yemen. Environmental Pollution 106, 299–314.Google Scholar
Thangaradjou, T., Nobi, E.P., Dilipan, E., Sivakumar, K. and Susila, S. (2010) Heavy metal enrichment in seagrasses of Andaman Islands and its implication to the health of the coastal ecosystem. Indian Journal of Marine Sciences 39, 85–91.Google Scholar
Tornero, V. and Ribera d'Alcalà, M. (2014) Contamination by hazardous substances in the Gulf of Naples and nearby coastal areas: a review of sources, environmental levels and potential impacts in the MSFD perspective. Science of the Total Environment 466–467, 820–840.Google Scholar
Ujević, I., Vuletić, N., Lušić, J., Nazlić, N. and Kušpilić, G. (2015) Bioaccumulation of trace metals in mussel (Mytilus galloprovincialis) from Mali Ston Bay during DSP toxicity episodes. Molecules 20, 13031–13040.Google Scholar
US EPA (1999) National recommended water quality criteria – correction. https://www.epa.gov/wqc/national-recommended-water-quality-criteria-aquatic-life-criteria-table.Google Scholar
Ventura-Lima, J., Fattorini, D., Notti, A., Monserrat, J.M. and Regoli, F. (2009) Bioaccumulation patterns and biological effects of arsenic in aquatic organisms. In Gosselin, J.D. and Fancher, I.M. (eds) Environmental health risks: lead poisoning and arsenic exposure. New York, NY: Nova Science Publishers, pp. 1–24.Google Scholar
Verbovšek, T. (2011) A comparison of parameters below the limit of detection in geochemical analyses by substitution methods. RMZ – Materials and Geoenvironment 58, 393–404.Google Scholar
Vreča, P. and Dolenec, T. (2005) Geochemical estimation of copper contamination in the healing mud from Makirina Bay, central Adriatic. Environment International 31, 53–61.Google Scholar
WHO (2004) Manganese and its compounds: environmental aspects. http://apps.who.int/iris/handle/10665/42992.Google Scholar
Yap, C.K. and Cheng, W.H. (2013) Distributions of heavy metal concentrations in different tissues of the magrove snail Nerita lineata. Sains Malaysiana 42, 597–603.Google Scholar
Yuan, C., Shi, J., He, B., Liu, J., Liang, L. and Jiang, G. (2004) Speciation of heavy metals in marine sediments from the East China Sea by ICP-MS with sequential extraction. Environment International 30, 769–783.Google Scholar
Župan, I., Peharda, M., Dolenec, T., Dolenec, M., Žvab Rožič, P., Lojen, S., Ezgeta-Balić, D. and Arapov, J. (2014) Aquaculture assessment of Noah's ark (Arca noae Linnaeus, 1758) in the Central Adriatic Sea (Croatia). Journal of Shellfish Research 33, 433–441.Google Scholar