Environmental Science and Pollution Research

, Volume 21, Issue 22, pp 13095–13102 | Cite as

Nickel exposure promotes osmoregulatory disturbances in Oreochromis niloticus gills: histopathological and energy dispersive spectrometry analysis

  • A. C. C. Marcato
  • A. T. Yabuki
  • C. S. Fontanetti
Research Article


Water is an essential factor for maintaining the vital functions of living beings. Nickel is the 24th most abundant element on Earth; it is a heavy metal that is genotoxic and mutagenic in its chloride form. Due to industrial use, its concentration in surface sediments increased considerably. Fish develop characteristics that make them excellent experimental models for studying aquatic toxicology. They are particularly useful because they can alert of the potential danger of chemical substances or environmental pollution. Due to water quality impairment and because there are few published studies that relate nickel to tissue alteration, this study aimed to examine the consequences of nickel in an aquatic environment. For this analysis, individuals of Oreochromis niloticus were exposed for 96 h to three different concentrations of nickel dissolved in water according to the standard established by Brazilian law and compared them to a control group. After exposure, the gills were analyzed using X-ray microanalysis, ultramorphology, and histological and histochemical analysis. The results demonstrated that all the concentrations used in the experiment altered the histophysiology of the individuals exposed. In conclusion, the nickel presents a toxic potential to fish, even at the lowest concentration tested, which is equivalent to half of the concentration allowed by law. The CONAMA resolution should be revised for this parameter because of the interference of this metal in the histophysiology of the tested organism.


Histopathology Mucous cells Water pollution Heavy metals Bioindicator Freshwater fish 



This research was supported by CNPq (National Council for Scientific and Technological Development) and FAPESP (São Paulo Research Foundation) process n. 2011/14881-3. The authors would like to thank Prof. Dr. José Carlos Marconato for contributing to the dilution calculations of the nickel used and the researchers Annelise Francisco, Jorge E. Correia, Júlia F. U. Marinho, and Larissa R. Nogarol for their help during the collections.


  1. Alves-Costa JRM (2001) Biomarcadores de contaminação em peixes de água doce, por contaminação em chumbo (II): ensaios laboratoriais com Hoplias malabaricus e Oreochromis niloticus. Dissertação, Universidade Federal do Paraná, (in Portuguese)Google Scholar
  2. Arellano JM, Storch V, Sarasquete C (1999) Histological changes and copper accumulation in liver and gills of the Senegales Sole, Solea senegalensis. Ecotoxicol Environ Safety 44:62–72CrossRefGoogle Scholar
  3. Ateeq B, Abul Farah M, Niamat A, Wassem A (2002) Induction of micronuclei and erythrocyte alterations in the catfish Clarias batrachus by 2,4-dichlorophenoxyacetic acid and butachlor. Mutat Res 518:135–144CrossRefGoogle Scholar
  4. Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34CrossRefGoogle Scholar
  5. Biagini FR, David JAO, Fontanetti CS (2009) The use of histological, histochemical and ultramorphological techniques to detect gill alterations in Oreochromis niloticus reared in treated polluted waters. Micron 40:839–844CrossRefGoogle Scholar
  6. Brix KV, Keithly J, Deforest DK, Laughlin J (2004) Acute and chronic toxicity of nickel to rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 23:2221–2228CrossRefGoogle Scholar
  7. Cerqueira CCC, Fernandes MN (2002) Gill tissue recovery after copper exposure and blood parameter responses in the tropical fish Prochilodus scrofa. Ecotoxicol Environ Saf 52:83–91CrossRefGoogle Scholar
  8. Chowdhury MJ, Bucking C, Wood CM (2008) Pre-exposure to waterborne nickel downregulates gastrointestinal nickel uptake in rainbow trout: indirect evidence for nickel essentiality. Environ Sci Technol 42:1359–1364CrossRefGoogle Scholar
  9. David JAO, Salaroli RB, Fontanetti CS (2008) The significance of changes in Mytella falcata (Orbigny, 1842) gill filaments chronically exposed to polluted environments. Micron 39:1293–1299CrossRefGoogle Scholar
  10. Evans DH (1987) The fish gill: site of action and model for toxic effects of environmental pollutants. Environ Health Perspect 71:47–58CrossRefGoogle Scholar
  11. Exley C, Chappell JS, Birchall JD (1991) A mechanism for acute aluminium toxicity in fish. J Theor Biol 151:417–28CrossRefGoogle Scholar
  12. Fanta E, Rios FS, Romão S, Vianna ACC, Freiberger S (2002) Histopathology of the fish Corydoras paleatus contaminated with sublethal levels of organophosphorus in water and food. Ecotoxicol Environ Safety 54:119–130CrossRefGoogle Scholar
  13. Fontanetti CS, Souza TS, Christofoletti CA (2012) The role of biomonitoring in the quality assessment of water resources. In: Bilibio C, Hensel O, Selbach J (eds) Sustainable water management in the tropics and subtropics—and cases study in Brazil. UNIPAMPA/UNIKASSEL, Brasil/Alemanha, pp 975–1005Google Scholar
  14. Ikem A, Egiebor NO, Nyavor K (2003) Trace elements in water, fish and sediment from Tuskegee Lake, south-eastern USA. Water Air Soil Pollut 149:51–75CrossRefGoogle Scholar
  15. Junqueira LCU, Junqueira MMS (1983) Técnicas básicas de citologia e histologia. Livraria Editora Santos, São Paulo, (in Portuguese)Google Scholar
  16. Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative at high osmolarity for use in electron microscopy. J Cell Biol 11:137–140Google Scholar
  17. Kasprzak KS (1987) Nickel. Adv Mod Environ Toxicol 11:145–183Google Scholar
  18. Kikuchi M, Wakabayashi M, Kojima H, Yoshida (1978) Uptake, distribution and elimination of sodium linear alkylbenzene sulfonate and sodium alkyl sulfate in carp. Ecotoxicol Environ Safety 2:115–127CrossRefGoogle Scholar
  19. Koca S, Koca YB, Yildiz S, Gurcu B (2008) Genotoxic and histopathological effects of water pollution on two fish species, Barbus capito pectoralis and Chondrostoma nasus in the Büyük Menderes River, Turkey. Biol Trace Elem Res 122:276–291CrossRefGoogle Scholar
  20. Laurent P, Perry SF (1991) Environmental effects on fish gill morphology. Physiol Zool 64:4–25Google Scholar
  21. Mallat J (1985) Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can J Fish Aquat Sci 42:630–648CrossRefGoogle Scholar
  22. Mansouri B, Ebrahimpour M, Babaei H (2012) Bioaccumulation and elimination of nickel in the organs of black fish (Capoeta fusca). Toxicol Ind Health 28:361–8CrossRefGoogle Scholar
  23. Martinez CBR, Nagae MY, Zaia CTBV, Zaia DAM (2004) Acute morphological and physiological effects of lead in the neotropical fish Prochilodus lineatus. Braz J Biol 64:797–807CrossRefGoogle Scholar
  24. Mckim JM, Erickson RJ (1991) Environmental impacts on the physiological mechanisms controlling xenobiotic transfer across fish gills. Physiol Zool 64:39–67Google Scholar
  25. Mishra V, Lal H, Chawla G, Viswanatan PN (1985) Pathomorphological changes in the gills of fish fingerlings (Cirrhina mingala) by lineal alkylbenzene sulfonate. Ecotoxicol Environ Safety 10:302–308CrossRefGoogle Scholar
  26. Otitoloju AA, Elegba OK, Osibona AO (2009) Biological responses in edible crab, Callinectes amnicola that could serve as markers of heavy metals pollution. Environmentalist 29:37–46CrossRefGoogle Scholar
  27. Pane EF, Mcdonald MD, Curry HN, Blanchard J, Wood CM, Grosell M (2006) Hydromineral balance in the marine gulf toadfish (Opsanus beta) exposed to waterborne or infused nickel. Aquat Toxicol 80:70–81CrossRefGoogle Scholar
  28. Perry SF, Laurent P (1993) Environmental effects on fish gill structure and function. In: Rankin JC, Jensen FB (eds) Fish ecophysiology. Chapman & Hall, London, pp 231–264CrossRefGoogle Scholar
  29. Powers DA (1989) Fish as model systems. Science 246:352–358CrossRefGoogle Scholar
  30. Randi AS, Monserrat JM, Rodriguez EM, Romano LA (1996) Histopathological effects of cadmium on the gills of the freshwater fish, Macropsobrycon uruguayanae Eigenmann (Pisces, Atherinidae). J Fish Dis 19:311–322CrossRefGoogle Scholar
  31. Rankin JC, Atagg RM, Bolis L (1982) Effects of pollutants on gills. In: Huolihan DF, Rankin JC, Shuttleworth TJ (eds) Gills. Cambridge University Press, New York, pp 207–220Google Scholar
  32. Romeoa M, Siaub Y, Sidoumou Z, Gnassia-barelli M (1999) Heavy metal distribution in different fish species from the Mauritania coast. Sci Total Environ 232:169–175CrossRefGoogle Scholar
  33. Sze PWC, Lee SY (1995) The potential role of mucus in the depuration of copper from the mussels Perna viridis (L.) and Septifer virgatus (Wiegmann). Mar Pollut Bull 31:390–393CrossRefGoogle Scholar
  34. Takashima F, Hibiya T (1995) An atlas of fish histology: normal and pathological features. Kodanska/Stuttgart. Fischer Verlag, TokyoGoogle Scholar
  35. Tjälve H, Borg-Neczak K (1994) Effects of lipophilic complex formation on the disposition of nickel in experimental animals. Sci Total Environ 148:217–242CrossRefGoogle Scholar
  36. Vijayan MM, Morgan JD, Sakamoto T, Grau EG, Iwana GK (1996) Food deprivation effects seawater acclimation in tilápia: hormonal and metabolic changes. J Exp Biol 199:2467–2475Google Scholar
  37. Wendelaar Bonga SE, Lock RAC (1991) Toxicants and osmoregulation in fish. Neth J Zool 42:478–493CrossRefGoogle Scholar
  38. Wong CK, Wong M (2000) Morphological and biochemical changes in the gills of tilapia (Oreochromis mossambicus) to ambient cadmium exposure. Aquat Toxicol 48:517–527CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • A. C. C. Marcato
    • 1
  • A. T. Yabuki
    • 1
  • C. S. Fontanetti
    • 1
  1. 1.UNESPSão Paulo State UniversityRio ClaroBrazil

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