Skip to main content

Multielement analysis in the fish hepatic cytosol as a screening tool in the monitoring of natural waters

Environmental Monitoring and Assessment volume 185, pages 2603–2614 (2013)Cite this article

Abstract

The possibility of direct measurement of trace elements in hepatic cytosol of European chub (Squalius cephalus) by high-resolution inductively coupled plasma mass spectrometry (HR ICP-MS) after cytosol dilution with Milli-Q water and subsequent acidification was investigated. Due to low detection limits of this procedure, determination of 13 elements (As, Cd, Co, Cu, Fe, Mn, Mo, Pb, Sb, Sn, Sr, V and Zn) was possible in the chub hepatic cytosol, exhibiting excellent measurement repeatability in duplicates. Some of these elements were also measured by HR ICP-MS in acid digested cytosols (Cd, Co, Cu, Fe, Mn, Mo, Sr, V and Zn). Good agreement of the results obtained after sample dilution and sample digestion indicated that complex organic matrix of hepatic cytosol did not affect measurement reliability. Cytosolic concentrations of 13 trace elements in the chub liver were quantified in the following order: Fe, Zn>Cu>Mn>Mo>Sr, V, Cd>Co>As, Pb>Sn>Sb. Unlike Cd, Cu, Fe, Mn and Zn for which the cytosolic concentrations were previously reported after measurement by AAS, cytosolic concentrations of eight additional trace elements characteristic for the liver of chubs inhabiting the low contaminated river water were reported here for the first time (in nanogrammes per gramme)—Mo, 136.8–183.6; Sr, 32.7–63.0; V, 17.5–69.0; Co, 24.3–30.7; As, 9.9–29.5; Pb, 5.8–35.6; Sn, 5.5–12.4; and Sb, 0.9–2.6. The simultaneous measurement of large number of trace elements in the cytosolic fractions of fish tissues, which comprise potentially metal-sensitive sub-cellular pools, could be beneficial as a screening tool in the monitoring of natural waters, because it would enable timely recognition of increased fish exposure to metals.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1

References

  • Alhas, E., Oymak, S. A., & Karadede Akin, H. (2009). Heavy metal concentrations in two barb, Barbus xanthopterus and Barbus rajanorum mystaceus from Atatürk Dam Lake, Turkey. Environmental Monitoring and Assessment, 148(1–4), 11–18.

    Article  CAS  Google Scholar 

  • Barlas, N. (1999). A pilot study of heavy metal concentration in various environments and fishes in the Upper Sakarya River Basin, Turkey. Environmental Toxicology, 14(3), 367–373.

    Article  CAS  Google Scholar 

  • Campbell, P. G. C., Giguère, A., Bonneris, E., & Hare, L. (2005). Cadmium-handling strategies in two chronically exposed indigenous freshwater organisms—the yellow perch (Perca flavescens) and the floater mollusc (Pyganodon grandis). Aquatic Toxicology, 72(1–2), 83–97.

    Article  CAS  Google Scholar 

  • Campbell, P. G. C., Kraemer, L. D., Giguère, A., Hare, L., & Hontela, A. (2008). Subcellular distribution of cadmium and nickel in chronically exposed wild fish: inferences regarding metal detoxification strategies and implications for setting water quality guidelines for dissolved metals. Human and Ecological Risk Assessment, 14(2), 290–316.

    Article  CAS  Google Scholar 

  • Čelechovská, O., Svobodová, Z., Žlábek, V., & Macharáčková, B. (2007). Distribution of metals in tissues of the common carp (Cyprinus carpio L.). Acta Veterinaria Brno, 76(S8), 93–100.

    Article  Google Scholar 

  • Clements, W. H., & Rees, D. E. (1997). Effects of heavy metals on prey abundance, feeding habits, and metal uptake of brown trout in the Arkansas River, Colorado. Transactions of the American Fisheries Society, 126(5), 774–785.

    Article  CAS  Google Scholar 

  • Dautović, J., Roje, V., Kozar, S., Fiket, Ž., & Mikac, N. (2007). Dissolved trace metals in some rivers and lakes from the Republic of Croatia. In: Proceedings of 4th Croatian Conference on Waters with International Participation: Croatian Waters and European Union—Challenges and Possibilities, Opatija, Croatia, pp. 115–122.

  • Dragun, Z., Raspor, B., & Podrug, M. (2007). The influence of the season and the biotic factors on the cytosolic metal concentrations in the gills of the European chub (Leuciscus cephalus L.). Chemosphere, 69(6), 911–919.

    Article  CAS  Google Scholar 

  • Dragun, Z., Roje, V., Mikac, N., & Raspor, B. (2009a). Preliminary assessment of total dissolved trace metal concentrations in Sava River water. Environmental Monitoring and Assessment, 159(1–4), 99–110.

    Article  CAS  Google Scholar 

  • Dragun, Z., Podrug, M., & Raspor, B. (2009b). Combined use of bioindicators and passive samplers for the assessment of the river water contamination with metals. Archives of Environmental Contamination and Toxicology, 57(2), 211–220.

    Article  CAS  Google Scholar 

  • Dragun, Z., Podrug, M., & Raspor, B. (2009c). The assessment of natural causes of metallothionein variability in the gills of European chub (Squalius cephalus L.). Comparative Biochemistry and Physiology Part C, 150(2), 209–217.

    Google Scholar 

  • Dragun, Z., Kapetanović, D., Raspor, B., & Teskeredžić, E. (2011). Water quality of medium size watercourse under baseflow conditions: the case study of river Sutla in Croatia. Ambio, 40(4), 391–407.

    Article  CAS  Google Scholar 

  • European Parliament and the Council of the European Union (EPCEU) (2008). Directive 2008/105/EC of the European Parliament and of the Council on environmental quality standards in the field of water policy, amending and subsequently repealing Council Directives 82/176/EEC, 83/513/EEC, 84/156/EEC, 84/491/EEC, 86/280/EEC, and amending Directive 2000/60/EC of the European Parliament and of the Council, Official Journal of the European Communities L, 348/84.

  • Farag, A. M., Woodward, D. F., Brumbaugh, W., Goldstein, J. N., MacConnell, E., Hogstrand, C., & Barrows, F. T. (1999). Dietary effects of metals-contaminated invertebrates from the Coeur d’Alene River, Idaho, on cutthroat trout. Transactions of the American Fisheries Society, 128(4), 578–592.

    Article  CAS  Google Scholar 

  • Fidan, A. F., Ciğerci, İ. H., Konuk, M., Küçükkurt, İ., Aslan, R., & Dündar, Y. (2008). Determination of some heavy metal levels and oxidative status in Carassius carassius L., 1758 from Eber Lake. Environmental Monitoring and Assessment, 147(1–3), 35–41.

    Article  CAS  Google Scholar 

  • Filipović Marijić, V., & Raspor, B. (2008). Hepatic metallothionein and metal (Zn, Cu and Cd) variability in relation to reproductive cycle of Mullus barbatus and Merluccius merluccius from the Eastern Adriatic Sea. Fresenius Environmental Bulletin, 17(6), 705–712.

    Google Scholar 

  • Filipović Marijić, V., & Raspor, B. (2010). The impact of fish spawning on metal and protein levels in gastrointestinal cytosol of indigenous European chub. Comparative Biochemistry and Physiology Part C, 152(2), 133–138.

    Google Scholar 

  • Filipović, V., & Raspor, B. (2003). Metallothionein and metal levels in cytosol of liver, kidney and brain in relation to growth parameters of Mullus surmuletus and Liza aurata from the Eastern Adriatic Sea. Water Research, 37(13), 3253–3262.

    Article  Google Scholar 

  • Gandolfi, G., Zerunian, S., Torricelli, P., & Marconato, A. (1991). I pesci delle acque interne italiane (p. 617). Roma: Istituto Poligrafico e Zecca dello Stato.

    Google Scholar 

  • Giguère, A., Campbell, P. G. C., Hare, L., McDonald, D. G., & Rasmussen, J. B. (2004). Influence of lake chemistry and fish age on cadmium, copper, and zinc concentrations in various organs of indigenous yellow perch (Perca flavescens). Canadian Journal of Fisheries and Aquatic Sciences, 61(9), 1702–1716.

    Article  Google Scholar 

  • Giguère, A., Campbell, P. G. C., Hare, L., & Couture, P. (2006). Sub-cellular partitioning of cadmium, copper, nickel and zinc in indigenous yellow perch (Perca flavescens) sampled along a polymetallic gradient. Aquatic Toxicology, 77(2), 178–189.

    Article  Google Scholar 

  • Goto, D., & Wallace, W. G. (2010). Metal intracellular partitioning as a detoxification mechanism for mummichogs (Fundulus heteroclitus) living in metal-polluted salt marshes. Marine Environmental Research, 69(3), 163–171.

    Article  CAS  Google Scholar 

  • Harte, J., Holdren, C., Schneider, R., & Shirley, C. (1991). Toxics A to Z, a guide to everyday pollution hazards. Oxford: University of California Press.

    Google Scholar 

  • Holcombe, G. W., Benoit, D. A., Leonard, E. N., & McKim, J. M. (1976). Long-term effects of lead exposure on three generations of brook trout (Salvelinus fontinalis). Journal of the Fisheries Research Board Canada, 33(8), 1731–1741.

    Article  CAS  Google Scholar 

  • HRN EN 14011 (2005). Fish sampling by electric power [Uzorkovanje riba električnom strujom].

  • Kamunde, C., & MacPhail, R. (2008). Bioaccumulation and hepatic speciation of copper in rainbow trout (Oncorhynchus mykiss) during chronic waterborne copper exposure. Archives of Environmental Contamination and Toxicology, 54(3), 493–503.

    Article  CAS  Google Scholar 

  • Kraemer, L. D., Campbell, P. G. C., & Hare, L. (2005). Dynamics of Cd, Cu and Zn accumulation in organs and sub-cellular fractions in field transplanted juvenile yellow perch (Perca flavescens). Environmental Pollution, 138(2), 324–337.

    Article  CAS  Google Scholar 

  • Kraemer, L. D., Campbell, P. G. C., & Hare, L. (2006). Seasonal variations in hepatic Cd and Cu concentrations and in the sub-cellular distribution of these metals in juvenile yellow perch (Perca flavescens). Environmental Pollution, 142(2), 313–325.

    Article  CAS  Google Scholar 

  • Krča, S., Žaja, R., Čalić, V., Terzić, S., Grubešić, M. S., Ahel, M., & Smital, T. (2007). Hepatic biomarker responses to organic contaminants in feral chub (Leuciscus cephalus)—laboratory characterization and field study in the Sava River, Croatia. Environmental Toxicology and Chemistry, 26(12), 2620–2633.

    Article  Google Scholar 

  • Lapointe, D., & Couture, P. (2009). Influence of the route of exposure on the accumulation and subcellular distribution of nickel and thallium in juvenile fathead minnows (Pimephales promelas). Archives of Environmental Contamination and Toxicology, 57(3), 571–580.

    Article  CAS  Google Scholar 

  • Linde, A. R., Sánchez-Galán, S., Klein, D., García-Vázquez, E., & Summer, K. H. (1999). Metallothionein and heavy metals in brown trout (Salmo trutta) and european eel (Anguilla anguilla): a comparative study. Ecotoxicology and Environmental Safety, 44(2), 168–173.

    Article  CAS  Google Scholar 

  • Maitland, P. S., & Campbell, R. N. (1992). Freshwater fishes of the British Isles. London: HarperCollins Publishers.

    Google Scholar 

  • McGeer, J. C., Niyogi, S., & Smith, D. S. (2012). Cadmium. In M. Wood, A. P. Farrell, & C. J. Brauner (Eds.), Homeostasis and toxicology of non-essential metals, fish physiology series—vol. 31B (pp. 125–184). Amsterdam: Elsevier.

    Google Scholar 

  • Milačič, R., Ščančar, J., Murko, S., Kocman, D., & Horvat, M. (2010). A complex investigation of the extent of pollution in sediments of the Sava River. Part 1: selected elements. Environmental Monitoring and Assessment, 163(1–4), 263–275.

    Google Scholar 

  • Oymak, S. A., Karadede-Akin, H., & Dogan, N. (2009). Heavy metal in tissues of Tor grypus from Atatürk Dam Lake, Euphrates River-Turkey. Biologia, 64(1), 151–155.

    Article  CAS  Google Scholar 

  • Papagiannis, I., Kagalou, I., Leonardos, J., Petridis, D., & Kalfakakou, V. (2004). Copper and zinc in four freshwater fish species from Lake Pamvotis (Greece). Environment International, 30(3), 357–362.

    Article  CAS  Google Scholar 

  • Paris-Palacios, S., & Biagianti-Risbourg, S. (2006). Hepatocyte nuclear structure and subcellular distribution of copper in zebrafish Brachydanio rerio and roach Rutilus rutilus (Teleostei, Cyprinidae) exposed to copper sulphate. Aquatic Toxicology, 77(3), 306–313.

    Article  CAS  Google Scholar 

  • Podrug, M., & Raspor, B. (2009). Seasonal variation of the metal (Zn, Fe, Mn) and metallothionein concentrations in the liver cytosol of the European chub (Squalius cephalus L.). Environmental Monitoring and Assessment, 157(1–4), 1–10.

    Article  CAS  Google Scholar 

  • Podrug, M., Raspor, B., Erk, M., & Dragun, Z. (2009). Protein and metal concentrations in two fractions of hepatic cytosol of the European chub (Squalius cephalus L.). Chemosphere, 75(7), 843–849.

    Article  CAS  Google Scholar 

  • Sappal, R., Burka, J., Dawson, S., & Kamunde, C. (2009). Bioaccumulation and subcellular partitioning of zinc in rainbow trout (Oncorhynchus mykiss): cross-talk between waterborne and dietary uptake. Aquatic Toxicology, 91(4), 281–290.

    Article  CAS  Google Scholar 

  • Schüürmann, G., & Markert, B. (1998). Ecotoxicology, ecological fundamentals, chemical exposure, and biological effects. New York: Wiley. 900 pp.

    Google Scholar 

  • SOP (Standard Operating Procedure) (1999). Preparation of S50-fraction from fish tissue (unapproved rev. 01), 1st Workshop in the frame of BEQUALM programme, NIVA, Oslo.

  • United States Environmental Protection Agency (USEPA) (1999). Toxics Release Inventory, Washington DC, USA, Doc. 745-R-00-007 and National Primary Drinking Water Standards, USEPA Office of Water, Washington, DC, USA, Doc. 810-F, pp. 94–001.

  • Varian. (1988). Analytical methods for graphite tube atomizers. Publication No. 85-100848-00. Mulgrave: Varian Australia Pty Ltd.

    Google Scholar 

  • Varian. (1989). Flame atomic absorption spectrometry—analytical methods. Publication No. 85-100009-00. Mulgrave: Varian Australia Pty Ltd.

    Google Scholar 

  • Vostradovsky, J. (1973). Freshwater fishes. London: The Hamlyn Publishing Group Limited.

    Google Scholar 

  • Wallace, W. G., & Luoma, S. N. (2003). Subcellular compartmentalization of Cd and Zn in two bivalves. II. Significance of trophically available metal (TAM). Marine Ecology Progress Series, 257, 125–137.

    Article  CAS  Google Scholar 

  • Zhang, L., & Wang, W.-X. (2006). Significance of subcellular metal distribution in prey in influencing the trophic transfer of metals in a marine fish. Limnology and Oceanography, 51(5), 2008–2017.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The financial support by the Ministry of Science, Education and Sport of the Republic of Croatia (projects No. 098-0982934-2721 and 098-0982934-2715) is acknowledged. The samplings were carried out as a part of the European FP6 project Sava River Basin: Sustainable Use, Management and Protection of Resources (INCO-CT-2004-509160). The authors are thankful to all SARIB project participants for the help in the fish sampling and dissection and to Nesrete Krasnići, B.Sc. for valuable technical assistance in sample preparation.

Author information

Authors and Affiliations

  1. Division for Marine and Environmental Research, Laboratory for Biological Effects of Metals, Ruđer Bošković Institute, P.O. Box 180, 10002, Zagreb, Croatia

    Zrinka Dragun, Marijana Vuković & Biserka Raspor

  2. Division for Marine and Environmental Research, Laboratory for Inorganic Environmental Geochemistry, Ruđer Bošković Institute, P.O. Box 180, 10002, Zagreb, Croatia

    Željka Fiket

Authors
  1. Zrinka Dragun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Željka Fiket
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marijana Vuković
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Biserka Raspor
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zrinka Dragun.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dragun, Z., Fiket, Ž., Vuković, M. et al. Multielement analysis in the fish hepatic cytosol as a screening tool in the monitoring of natural waters. Environ Monit Assess 185, 2603–2614 (2013). https://doi.org/10.1007/s10661-012-2734-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10661-012-2734-6

Keywords

  • HR ICP-MS
  • Cytosol
  • European chub
  • Liver
  • Trace elements