Relevance of biotic parameters in the assessment of the spatial distribution of gastrointestinal metal and protein levels during spawning period of European chub (Squalius cephalus L.)

Abstract

The present field study, conducted during the spawning period (April/May) of European chub (Squalius cephalus L.) from the Sava River in Croatia, indicates that seasonal changes of fish physiological state might cause variability in gastrointestinal metal (Cd, Cu, Fe, Mn and Zn), total cytosolic protein and metallothionein (MT) levels. During the period of fish spawning and increased metabolic activity, a significant relationship with chub hepatosomatic index was evident for Fe and Mn in gastrointestinal tissue (r = 0.35 and 0.26, respectively) and in cytosolic fraction (r = 0.32 and 0.41, respectively) and for Zn and Fe in the gut content (r = 0.36 and 0.31, respectively). Total cytosolic protein and MT concentrations followed the same spatial distribution as Fe and Mn in all gastrointestinal fractions and as Zn in the sub-cellular fractions, with higher levels at upstream locations. Due to the role of essential metals in metabolic processes and gonad development, increased feeding and spawning activity in April/May resulted in higher gastrointestinal essential metal (Fe, Mn and Zn) and MT concentrations, which probably follow an increase in Zn concentrations, known as the primary MT inducer. Therefore, biotic factors should be considered as important confounding factors in metal exposure assessment, while their influence on gastrointestinal metal and protein levels should be interpreted depending on the season studied.

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References

  1. Adams MS, McLean RB (1985) Estimation of largemouth bass, Micropterus salmoides Lacépède, growth using the liver somatic index and physiological variables. J Fish Biol 26:111–126

    Article  Google Scholar 

  2. Benedicto J, Martínez-Gómez C, Campillo J (2005) Induction of metallothioneins in Mullus barbatus as specific biomarker of metal contamination: a field study in the western Mediterranean. Cienc Mar 31(1B):265–274

    CAS  Google Scholar 

  3. Bury NR, Walker PA, Glover CN (2003) Nutritive metal uptake in teleost fish. J Exp Biol 206:11–23

    CAS  Article  Google Scholar 

  4. Campbell PG, 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). Aquat Toxicol 72(1–2):83–97

    CAS  Article  Google Scholar 

  5. Clearwater SJ, Baskin SJ, Wood CM, McDonald DG (2000) Gastrointestinal uptake and distribution of copper in rainbow trout. J Exp Biol 203(16):2455–2466

    CAS  Google Scholar 

  6. Creighton N, Twining J (2010) Bioaccumulation from food and water of cadmium, selenium and zinc in an estuarine fish, Ambassis jacksoniensis. Mar Pollut Bull 60:1815–1821

    CAS  Article  Google Scholar 

  7. Dragun Z, Raspor B (2005) Direct determination of Cd in NaCl containing metallothionein fractions of different red mullet tissues by graphite furnace atomic absorption spectrometry. J Anal At Spectrom 20(10):1121–1123

    CAS  Article  Google Scholar 

  8. Dragun Z, Roje V, Mikac N, Raspor B (2009a) Preliminary assessment of total dissolved trace metal concentrations in Sava River water. Environ Monit Assess 159(1):99–110

    CAS  Article  Google Scholar 

  9. Dragun Z, Podrug M, Raspor B (2009b) The assessment of natural causes of metallothionein variability in the gills of European chub (Squalius cephalus L.). Comp Biochem Physiol C 150:209–217

    Google Scholar 

  10. Duman F, Kar M (2012) Temporal variation of metals in water, sediment and tissues of the European chup (Squalius cephalus L.). Bull Environ Contam Toxicol 89(2):428–433

    CAS  Article  Google Scholar 

  11. Eastwood S, Couture P (2002) Seasonal variations in condition and liver metal concentrations of yellow perch (Perca flavescens) from a metal-contaminated environment. Aquat Toxicol 58:43–56

    CAS  Article  Google Scholar 

  12. 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 Environ Bull 17(6):705–712

    Google Scholar 

  13. Filipović Marijić V, Raspor B (2010) The impact of fish spawning on metal and protein levels in gastrointestinal cytosol of indigenous European chub. Comp Biochem Physiol C 152:133–138

    Google Scholar 

  14. Filipović Marijić V, Raspor B (2012) Site-specific gastrointestinal metal variability in relation to the gut content and fish age of indigenous European chub from the Sava River. Water Air Soil Pollut 223:4769–4783

    Article  Google Scholar 

  15. Giguère A, Campbell PGC, Hare L, McDonald DG, Rasmussen JB (2004) Influence of lake chemistry and fish age on cadmium, copper, and zinc concentrations in various organs of indigenous yellow perch (Perca flavescens). Can J Fish Aquat Sci 61(9):1702–1716

    Article  Google Scholar 

  16. Habeković D, Aničić I, Safner R (1993) Growth dynamics of the chub fish in the river Sava [Dinamika rasta klena u rijeci Savi, in Croatian]. Ribarstvo 48(3):79–88

    Google Scholar 

  17. Heidinger SD, Crawford SD (1977) Effects of temperature and feeding rate on the liver-somatic index of the largemouth bass, Micropterus salmoides. J Fish Res Board Can 34:633–638

    Article  Google Scholar 

  18. HRN EN 14011: 2005 (2005) Fish sampling by electric power [Uzorkovanje riba električnom strujom, in Croatian]

  19. Hylland K, Nissen-Lie T, Christensen PG, Sandvik M (1998) Natural modulation of hepatic metallothionein and cytochrome P4501A in flounder, Platichthys flesus L. Mar Environ Res 46(1–5):51–55

    CAS  Article  Google Scholar 

  20. Kamunde C, Clayton C, Wood CM (2002) Waterborne vs. dietary copper uptake in rainbow trout and the effects of previous waterborne copper exposure. Am J Physiol Regul Integr Comp Physiol 283(1):R69–R78

    CAS  Google Scholar 

  21. Krasnići N, Dragun Z, Erk M, Raspor B (2013) Distribution of selected essential (Co, Cu, Fe, Mn, Mo, Se, Zn) and nonessential (Cd, Pb) trace elements among protein fractions from hepatic cytosol of European chub (Squalius cephalus L.). Environ Sci Pollut Res 20(4):2340–2351

    Article  Google Scholar 

  22. Krča S, Žaja R, Čalić V, Terzić S, Grubešić MS, 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. Environ Toxicol Chem 26(12):2620–2633

    Article  Google Scholar 

  23. Lall SP (2002) The minerals. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Elsevier, San Diego, pp 259–308

    Google Scholar 

  24. Livingstone DR (1993) Biotechnology and pollution monitoring: use of molecular biomarkers in the aquatic environment. J Chem Technol Biotechnol 57:195–211

    CAS  Article  Google Scholar 

  25. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  26. Meyer JS, Adams WJ, Brix KV, Luoma SN, Mount DR, Stubblefield WA, Wood CM (2005) Toxicity of dietborne metals to aquatic organisms. SETAC, Pensacola

    Google Scholar 

  27. Miramand P, Lafaurie M, Fowler SW, Lemaire P, Guary JC, Bentley D (1991) Reproductive cycle and heavy metals in the organs of red mullet, Mullus barbatus (L.), from the northwestern Mediterranean. Sci Total Environ 103:47–56

    CAS  Article  Google Scholar 

  28. Olsson P-E, Haux C, Förlin L (1987) Variations in hepatic metallothionein, zinc and copper levels during an annual reproductive cycle in raibow trout, Salmo gairdneri. Fish Physiol Biochem 3(1):39–47

    CAS  Article  Google Scholar 

  29. Philips DJH (1980) Quantitative aquatic biological indicators. Applied Science, Barking

    Google Scholar 

  30. 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

    CAS  Article  Google Scholar 

  31. Raspor B, Paić M, Erk M (2001) Analysis of metallothioneins by the modified Brdička procedure. Talanta 55:109–115

    CAS  Article  Google Scholar 

  32. Roesijedi G (1992) Metallothioneins in metal regulation and toxicity in aquatic animals. Aquat Toxicol 22:81–114

    Article  Google Scholar 

  33. Rotchell JM, Clarke KR, Newton LC, Bird DJ (2001) Hepatic metallothionein as a biomarker for metal contamination: age effects and seasonal variation in European flounders (Pleuronectes flesus) from the Severn Estuary and Bristol Channel. Mar Environ Res 52:151–171

    CAS  Article  Google Scholar 

  34. Standard Operation Procedure (1999) Preparation of S50-fraction from fish tissue (unapproved rev. 01). In: 1st workshop in the frame of BEQUALM programme, 13.-14.9.1999. at the Norwegian Institute for Water Research (NIVA), Oslo

  35. Watanabe T, Kiron V, Satoh S (1997) Trace minerals in fish nutrition. Aquaculture 151:185–207

    CAS  Article  Google Scholar 

  36. Weber DN, Eisch S, Spieler RE, Petering DH (1992) Metal redistribution in largemouth bass (Micropterus salmoides) in response to restrainment stress and dietary cadmium: role of metallothionein and other metal-binding proteins. Comp Biochem Physiol C 101(2):255–262

    CAS  Article  Google Scholar 

  37. Wootton RJ (1990) Ecology of teleost fishes. Chapman & Hall, London

    Google Scholar 

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Acknowledgments

Financial support by the Ministry of Science, Education and Sport of Republic Croatia (project no. 098-0982934-2721) is acknowledged. The authors are also grateful for the valuable help in the field work to all EU FP6 SARIB Project participants and for the useful pieces of advice concerning metal determination on HR ICP-MS to Dr. Nevenka Mikac, Dr. Vibor Roje and Dr. Željka Fiket and on AAS to Dr. Zrinka Dragun. We appreciate the assistance of the Meteorological and Hydrological Service Office for reporting the data on hydrological parameters of the Sava River water.

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Correspondence to Vlatka Filipović Marijić.

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Filipović Marijić, V., Raspor, B. Relevance of biotic parameters in the assessment of the spatial distribution of gastrointestinal metal and protein levels during spawning period of European chub (Squalius cephalus L.). Environ Sci Pollut Res 21, 7596–7606 (2014). https://doi.org/10.1007/s11356-014-2666-5

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Keywords

  • Hepatosomatic index
  • Gut content
  • Essential metals
  • Cd
  • Metallothionein
  • Total cytosolic proteins