Assessment of general condition of fish inhabiting a moderately contaminated aquatic environment

Environmental Science and Pollution Research volume 20, pages4954–4968(2013)Cite this article

Abstract

The assessment of general condition of fish in the moderately contaminated aquatic environment was performed on the European chub (Squalius cephalus) caught in September 2009 in the Sutla River in Croatia. Although increases of the contaminants in this river (trace and macro elements, bacteria), as well as physico-chemical changes (decreased oxygen saturation, increased conductivity), were still within the environmentally acceptable limits, their concurrent presence in the river water possibly could have induced stress in aquatic organisms. Several biometric parameters, metallothionein (MT), and total cytosolic protein concentrations in chub liver and gills were determined as indicators of chub condition. Microbiological and parasitological analyses were performed with the aim to evaluate chub predisposition for bacterial bioconcentration and parasitic infections. At upstream river sections with decreased oxygen saturation (∼50 %), decreased Fulton condition indices were observed (FCI: 0.94 g cm−3), whereas gonadosomatic (GSI: 2.4 %), hepatosomatic (HSI: 1.31 %), and gill indices (1.3 %) were increased compared to oxygen rich downstream river sections (dissolved oxygen ∼90 %; FCI: 1.02 g cm−3; GSI: 0.6 %; HIS: ∼1.08 %; gill index: 1.0 %). Slight increase of MT concentrations in both organs at upstream (gills: 1.67 mg g−1; liver: 1.63 mg g−1) compared to downstream sites (gills: 1.56 mg g−1; liver: 1.23 mg g−1), could not be explained by induction caused by increased metal levels in the river water, but presumably by physiological changes caused by general stress due to low oxygen saturation. In addition, at the sampling site characterized by inorganic and fecal contamination, increased incidence of bacterial bioconcentration in internal organs (liver, spleen, kidney) was observed, as well as decrease of intestinal parasitic infections, which is a common finding for metal-contaminated waters. Based on our results, it could be concluded that even moderate contamination of river water by multiple contaminants could result in unfavourable living conditions and cause detectable stress for aquatic organisms.

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

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Adams SM, Shepard KL, Greeley MS, Jimenez BD, Ryon MG, Shugart LR, McCarthy JF (1989) The use of bioindicators for assessing the effects of pollutant stress on fish. Mar Environ Res 28:459–464

    Article  CAS  Google Scholar 

  2. Amiard J-C, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76:160–202

    Article  CAS  Google Scholar 

  3. Andres S, Ribeyre F, Tourencq J-N, Boudou A (2000) Interspecific comparison of cadmium and zinc contamination in the organs of four fish species along a polymetallic pollution gradient (Lot River, France). Sci Total Environ 248:11–25

    Article  CAS  Google Scholar 

  4. Baer KN, Thomas P (1990) Influence of capture stress, salinity and reproductive status on zinc associated with metallothionein-like proteins in the livers of three marine teleost species. Mar Environ Res 28:157–161

    Article  Google Scholar 

  5. Barton BA, Taylor BR (1996) Oxygen requirements of fishes in northern Alberta rivers with a general review of the adverse effects of low dissolved oxygen. Water Qual Res J Can 31:361–409

    CAS  Google Scholar 

  6. 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 

  7. Berg LS (1964) Freshwater fishes of the USSR and adjacent countries (translated from Russian), vol. 2, 4th edn. (Russian version published 1949). Academy of Sciences of the USSR, Jerusalem, p 496

    Google Scholar 

  8. Bremner I (1987) Nutritional and physiological significance of metallothionein. Experientia – Suppl 52:81–107

    CAS  Google Scholar 

  9. Burleson ML, Wilhelm DR, Smatresk NJ (2001) The influence of fish size on the avoidance of hypoxia and oxygen selection by largemouth bass. J Fish Biol 59:1336–1349

    Google Scholar 

  10. Cajaraville MP, Bebianno MJ, Blasco J, Porte C, Sarasquete C, Viarengo A (2000) The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Sci Total Environ 247:295–311

    Article  CAS  Google Scholar 

  11. Chapman LJ, Galis F, Shinn J (2000) Phenotypic plasticity and the possible role of genetic assimilation: hypoxia-induced trade-offs in the morphological traits of an African cichlid. Ecol Lett 3:387–393

    Article  Google Scholar 

  12. Chapman LJ, Albert J, Galis F (2008a) Developmental plasticity, genetic differentiation, and hypoxia-induced trade-offs in an African cichlid fish. Open Evol 2:75–88

    Article  Google Scholar 

  13. Chapman LJ, Chapman CA, Kaufman L, Witte F, Balirwa J (2008b) Biodiversity conservation in African waters: lessons of the Lake Victoria region. Vehr Internat Verein Limnol 30:16–34

    Google Scholar 

  14. Chesney EJ, Baltz DM, Thomas RG (2000) Louisiana estuarine and coastal fisheries and habitats: perspectives from a fish’s eye view. Ecol Appl 10:350–366

    Article  Google Scholar 

  15. De Smet H, Blust R (2001) Stress responses and changes in protein metabolism in carp Cyprinus carpio during cadmium exposure. Ecotox Environ Safe 48:255–262

    Article  Google Scholar 

  16. Diaz RJ (2001) Overview of hypoxia around the world. J Environ Qual 30:275–281

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  Google Scholar 

  20. 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 40:391–407

    Article  CAS  Google Scholar 

  21. Elliott JM (1976) The energetics of feeding, metabolism and growth of brown trout (Salmo trutta L.) in relation to body weight, water temperature and ration size. J Anim Ecol 45:923–948

    Article  Google Scholar 

  22. Encina L, Granado-Lorencio C (1997) Seasonal variations in the physiological status and energy content of somatic and reproductive tissues of chub. J Fish Biol 50:511–522

    Article  Google Scholar 

  23. Erk M, Ivanković D, Raspor B, Pavičić J (2002) Evaluation of different purification procedures for the electrochemical quantification of mussel metallothioneins. Talanta 57:1211–1218

    Article  CAS  Google Scholar 

  24. Falchuk KH, Czupryn M (1991) Isolation of metallothioneins under metal-free conditions. In: Riordan JF, Vallee BL (eds) Methods in Enzymology, vol 205, Metallobiochemistry Part B. Metallothionein and Related Molecules. Academic Press Inc, San Diego, pp 47–53

    Google Scholar 

  25. Fattal B, Dotan A, Parpari L, Techorsh Y, Cabelli VJ (1993) Microbiological purification of fish grown in fecally contaminated commercial fish pond. Water Sci Technol 27:303–311

    Google Scholar 

  26. Filipović Marijić V, Raspor B (2006) Age and tissue dependent metallothionein and cytosolic metal distribution in a native Mediterranean fish, Mullus barbatus, from the Eastern Adriatic Sea. Comp Biochem Phys C 143:382–387

    Article  Google Scholar 

  27. Filipović Marijić V, Raspor B (2007) Metal exposure assessment in native fish, Mullus barbatus L., from the Eastern Adriatic Sea. Toxicol Lett 168:292–301

    Article  Google Scholar 

  28. 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. Fresen Environ Bull 17:705–712

    Google Scholar 

  29. 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 Phys C 152:133–138

    Google Scholar 

  30. Friesen CN, Aubin-Horth N, Chapman LJ (2012) The effect of hypoxia on sex hormones in an African cichlid Pseudocrenilabrus multicolorvictoriae. Comp Biochem Phys A 162:22–30

    Article  CAS  Google Scholar 

  31. Galli RJ, Mariniello L, Crosa G, Ortis M, Mcchipinti Ambrogi A, D’Amelio S (1998) Populations of Acanthocephalus anguillae and Pomphorhynchus laevis in rivers with different pollution levels. J Helminthol 72:331–335

    Article  Google Scholar 

  32. Galli P, Crosa G, Mariniello L, Ortis M, D’Amelio D (2001) Water quality as a determinant of the composition of fish parasite communities. Hydrobiologia 452:173–179

    Article  Google Scholar 

  33. Gelnar M, Koubkova B, Plankova H, Jurajda P (1996) Report on metazoan parasites of fishes of the River Morava with remarks on the effects of water pollution. Helminthologia 31:47–56

    Google Scholar 

  34. 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 61:1702–1716

    Article  Google Scholar 

  35. Goldberg ED (1995) Emerging problems in the coastal zone for the twenty-first century. Mar Pollut Bull 31:152–158

    Article  CAS  Google Scholar 

  36. Graham JB (2006) Aquatic and aerial respiration. In: Evans DH, Claiborne JB (eds) The Physiology of Fishes. Taylor and Francis, Boca Raton, pp 85–117

    Google Scholar 

  37. Hattink J, De Boeck G, Blust R (2005) The toxicokinetics of cadmium in carp under normoxic and hypoxic conditions. Aquat Toxicol 75:1–15

    Article  CAS  Google Scholar 

  38. Hogstrand C, Lithner G, Haux C (1991) The importance of metallothionein for the accumulation of copper, zinc and cadmium in environmentally exposed perch, Perca fluviatilis. Pharmacol Toxicol 68:492–501

    Article  CAS  Google Scholar 

  39. HRN EN 14011 (2005) Fish sampling by electric power

  40. 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 46:51–55

    Article  CAS  Google Scholar 

  41. Kägi JHR, Schäffer A (1988) Biochemistry of metallothionein. Biochemistry 27:8509–8515

    Article  Google Scholar 

  42. Kapetanović D, Kurtović B, Teskeredžić E (2005) Differences in bacterial population in rainbow trout (Oncorhynchus mykiss Walbum) fry after transfer from incubator to pools. Food Technol Biotech 43:189–193

    Google Scholar 

  43. Kennedy CR (2006) Ecology of the Acanthocephala. Cambridge University Press, Cambridge, UK

    Book  Google Scholar 

  44. Khan RA, Barker DE, Ryan K, Murphy B, Hooper RG (1996) Abnormalities in winter flounder (Pleuronectes americanus) living near a paper mill in the Humber Arm, Newfoundland. In: Servos MR, Munkittrick KR, Carey JH, Van Der Kraak GJ (eds) Environmental Fate and Effects of Pulp and Paper Mill Effluents, St. Lucie Press, Del Ray Beach, pp 511–523

  45. Kramer DL (1987) Dissolved oxygen and fish behavior. Environ Biol Fish 18:81–92

    Article  Google Scholar 

  46. Lafferty KD (1997) Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitol Today 13:251–255

    Article  CAS  Google Scholar 

  47. Landry CA, Steele SL, Manning S, Cheek AO (2007) Long term hypoxia suppresses reproductive capacity in the estuarine fish, Fundulus grandis. Comp Biochem Physiol A 148:317–323

    Article  CAS  Google Scholar 

  48. 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 

  49. Maage A, Waagbo R, Olsson P-E, Julshamn K, Sandnes K (1990) Ascorbate-2-sulfate as a dietary vitamin C source for Atlantic salmon (Salmo salar): 2. Effects of dietary levels and immunization on the metabolism of trace elements. Fish Physiol Biochem 8:429–436

    Article  CAS  Google Scholar 

  50. Mills CA, Eloranta A (1985) Reproductive strategies in the stone loach, Noemacheilus barbatulus. Oikos 44:341–349

    Article  Google Scholar 

  51. Moravec F (2004) Class Acanthocephala Rudolphi, 1808.In: Metazoan parasites of salmonid fishes of Europe, 1st edn. Nakladatelstvi Academie ved Ceske Republiky, Academia Praha, pp 380–412

    Google Scholar 

  52. Movahedinia A, Abtahi B, Bahmani M (2012) Gill histopathological lesions of the sturgeons. Asian J Anim Vet Adv 7:710–717

    Article  Google Scholar 

  53. Ognev SI, Fink N (1956) The biology of vertebrae (In Croatian). Grafički zavod Hrvatske, Zagreb

    Google Scholar 

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

    Article  CAS  Google Scholar 

  55. Olsson P-E, Zafarullah M, Foster R, Hamor T, Gedamu L (1990) Developmental regulation of metallothionein mRNA, zinc and copper levels in rainbow trout, Salmo gairdneri. Eur J Biochem 193:229–235

    Article  CAS  Google Scholar 

  56. Öztaş H (1989) A study on the reproduction biology of the chub (Leuciscus cephalus L. 1758) in the Müceldi Stream in East Anatolia. Turk J Vet Anim Sci 13:171–179

    Google Scholar 

  57. Pathak SP, Gopal K (2005) Occurrence of antibiotic and metal resistance in bacteria from organs of river fish. Environ Res 98:100–103

    Article  CAS  Google Scholar 

  58. Pihl L, Baden SP, Diaz RJ (1991) Effects of periodic hypoxia on distribution of demersal fish and crustaceans. Mar Biol 108:349–360

    Article  Google Scholar 

  59. 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.). Environ Monit Assess 157:1–10

    Article  CAS  Google Scholar 

  60. 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 75:843–849

    Article  CAS  Google Scholar 

  61. Pollock MS, Clarke LMJ, Dubé MG (2007) The effects of hypoxia on fishes: from ecological relevance to physiological effects. Environ Rev 15:1–14

    Article  CAS  Google Scholar 

  62. Pulliainen E, Korhonen K (1990) Seasonal changes in condition indices in adult mature and non-maturing burbot, Lota lota (L.), in the north-eastern Bothnian Bay, northern Finland. J Fish Biol 36:251–259

    Article  Google Scholar 

  63. Randall DJ (1970) Gas exchange in fish. In: Hoar WS, Randall DJ (eds) Fish Physiology. Academic Press, London, pp 253–292

    Google Scholar 

  64. Randall D (1982) The control of respiration and circulation in fish during exercise and hypoxia. J Exp Biol 100:275–288

    Google Scholar 

  65. Randall D, Daxboeck C (1984) Oxygen and carbon dioxide transfer across fish gills. Fish Physiol 10:263–314

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  67. Rätz H-J, Lloret J (2003) Variation in fish condition between Atlantic cod (Gadus morhua) stocks, the effect on their productivity and management implications. Fish Res 60:369–380

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  69. Şaşi H (2004) The reproduction biology of chub (Leuciscus cephalus L. 1758) in Topçam Dam Lake (Aydın, Turkey). Turk J Vet Anim Sci 28:693–699

    Google Scholar 

  70. Sepúlveda MS, Gallagher EP, Gross TS (2004) Physiological changes in largemouth bass exposed to paper mill effluents under laboratory and field conditions. Ecotoxicology 13:291–301

    Article  Google Scholar 

  71. Sepúlveda MS, Johnson WE, Higman JC, Denslow ND, Schoeb TR, Gross TS (2002) An evaluation of biomarkers of reproductive function and potential contaminant effects in Florida largemouth bass (Micropterus salmoides floridanus) sampled from the St. Johns River. Sci Total Environ 289:133–144

    Article  Google Scholar 

  72. Shang EHH (2006) Hypoxia affects sex differentiation and development, leading to a male-dominated population in zebrafish (Danio rerio). Environ Sci Technol 40:3118–3122

    Article  CAS  Google Scholar 

  73. Soimasuo MR, Aaltonen T, Nikinmaa M, Pellinen J, Ristola T, Oikari A (1995) Physiological toxicity of low-chlorine bleached pulp and paper mill effluent on whitefish (Coregonus lavaretus L. s.1): a laboratory exposure simulating lake pollution. Ecotox Safe 31:228–237

    Article  CAS  Google Scholar 

  74. Sures B, Siddall R, Taraschewski H (1999) Parasites as accumulation indicators of heavy metal pollution. Parasitol Today 15:16–21

    Article  CAS  Google Scholar 

  75. Teskeredžić E, Teskeredžić Z, Tomec M, Kurtović B, Raspor B, Kapetanović D, Dragun Z, Vardić I, Valić D, Strižak Ž, Španović B, Šoštarić Vulić Z, Roman Z (2009) Programme for the monitoring of the freshwater fishery status in the year 2009 - Group D - Fishing area Sava; River Sutla. [In Croatian: Program praćenja stanja slatkovodnog ribarstva u 2009. godini - Grupa D - ribolovno područje Sava; rijeka Sutla]. Ruđer Bošković Institute, Zagreb

  76. Timmerman CM, Chapman LJ (2004) Hypoxia and interdemic variation in Poecilia latipinna. J Fish Biol 65:635–650

    Article  Google Scholar 

  77. Treer T, Safner R, Aničić I, Lovrinov M (1995) Fishery (In Croatian). Globus, Zagreb

    Google Scholar 

  78. Ünver B (1998) An investigation on the reproduction properties of chub (Leuciscus cephalus L., 1758) in Lake Tödürge (Zara/Sivas). Turk J Zool 22:141–147

    Google Scholar 

  79. van Cleef KA, Kaplan LAE, Crivello JF (2000) The relationship between reproductive status and metallothionein mRNA expression in the common killifish, Fundulus heteroclitus. Environ Biol Fishes 57:97–105

    Article  Google Scholar 

  80. van Dyk JC, Cochrane MJ, Wagenaar GM (2012) Liver histopathology of the sharptooth catfish Clarias gariepinus as a biomarker of aquatic pollution. Chemosphere 87:301–311

    Article  Google Scholar 

  81. Vašák M (2005) Advances in metallothionein structure and functions. J Trace Elem Med Biol 19:13–17

    Article  Google Scholar 

  82. Viarengo A, Burlando B, Dondero F, Marro A, Fabbri R (1999) Metallothionein as a tool in biomonitoring programmes. Biomarkers 4:455–466

    Article  CAS  Google Scholar 

  83. Weltzien F, Doving KB, Carr WES (1999) Avoidance reaction of yolk-sac larvae of the inland silverside Menidia beryllina (Atherinidae) to hypoxia. J Exp Biol 202:2869–2876

    Google Scholar 

  84. Woo NYS, Wu RSS (1984) Changes in biochemical composition in the red grouper, Epinephelus akaara (Temminck and Schlegel), and the Black Sea bream, Mylio macrocephalus (Basilewsky), during hypoxic exposure. Comp Biochem Physiol A Physiol 77:475–482

    Article  Google Scholar 

  85. Zorita I, Ortiz-Zarragoitia M, Apraiz I, Cancio I, Orbea A, Soto M, Marigómez I, Cajaraville MP (2008) Assessment of biological effects of environmental pollution along the NW Mediterranean Sea using red mullets as sentinel organisms. Environ Pollut 153:157–168

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The financial support by the Ministry of Science, Education and Sport of the Republic of Croatia (project nos. 098-0982934-2721 and 098-0982934-2752) is acknowledged. This study was carried out as a part of the Monitoring of freshwater fishery in 2009 - Group D - Fishing area Sava River - Sutla River, funded by Ministry of Agriculture, Fisheries and Rural Development of the Republic of Croatia. The authors are especially thankful to Dr. Nevenka Mikac for the opportunity to use HR ICP-MS and to Branko Španović for the help in the field work.

Author information

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, Vlatka Filipović Marijić, Nesrete Krasnići, Željka Strižak & Biserka Raspor

  2. Division for Marine and Environmental Research, Laboratory for Aquaculture and Pathology of Aquatic Organisms, Ruđer Bošković Institute, P.O. Box 180, 10002, Zagreb, Croatia

    Damir Kapetanović, Damir Valić, Irena Vardić Smrzlić, Božidar Kurtović & Emin Teskeredžić

Authors
  1. Zrinka Dragun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vlatka Filipović Marijić
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Damir Kapetanović
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Damir Valić
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Irena Vardić Smrzlić
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nesrete Krasnići
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Željka Strižak
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Božidar Kurtović
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Emin Teskeredžić
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Biserka Raspor
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zrinka Dragun.

Additional information

Responsible editor: Henner Hollert

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dragun, Z., Filipović Marijić, V., Kapetanović, D. et al. Assessment of general condition of fish inhabiting a moderately contaminated aquatic environment. Environ Sci Pollut Res 20, 4954–4968 (2013). https://doi.org/10.1007/s11356-013-1463-x

Download citation

Keywords

  • Bacteria
  • European chub
  • Intestinal parasites
  • Metallothioneins
  • Sutla River
  • Stress