Central European Journal of Biology

, Volume 8, Issue 10, pp 975–985 | Cite as

Histopathological indicators: a useful fish health monitoring tool in common carp (Cyprinus carpio Linnaeus, 1758) culture

  • Božidar Rašković
  • Ivan Jarić
  • Vesna Koko
  • Milan Spasić
  • Zorka Dulić
  • Zoran Marković
  • Vesna Poleksić
Research Article


In order to evaluate the relationship between water quality in ponds and indices of histopathological changes occurring in the vital organs of the common carp (Cyprinus carpio L., 1758), two six-month field experiments were carried out using two different water supplies: from the nearby stream and a tube well. The fish were fed supplemental feed: raw cereals, pelleted and extruded compound feed. Histopathological analysis, alteration frequencies, and semi-quantitative scoring of the changes were used to assess the health status of the fish. Ponds supplied by stream water were characterized by higher water hardness, dissolved oxygen and pH values, while those supplied by the tube well had higher electroconductivity, total ammonium and orthophosphates content. Fish survival rate and habitat suitability index were lower in ponds supplied by stream water, while the weight gain did not differ between the two water supplies. The use of stream water resulted in a higher level of histopathological changes in gills and liver. Among the water quality parameters, pH level had the strongest influence on fish. Differences in water supply produced greater influence on the level of histopathological changes than the type of feed applied. Gills were the most sensitive organ, while the kidney was the least responsive.


Histopathology Semi-quantitative scoring Water quality Pond Common carp 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. [1]
    Hinton D.E., Lauren D.J., Integrative histopathological approaches to detecting effects of environmental stressors on fishes, In: Adams R., Lloyd R. (Eds.), Biological indicators of stress in fish, American Fisheries Society, Bethesda, Maryland, 1990Google Scholar
  2. [2]
    van der Oost R., Beyer J., Vermeulen N.P.E., Fish bioaccumulation and biomarkers in environmental risk assessment: a review, Environ. Toxicol. Pharmacol., 2003, 13, 57–149PubMedCrossRefGoogle Scholar
  3. [3]
    Schwaiger J., Wanke R., Adam S., Pawert M., Honnen W., Triebskorn R., The use of histopathological indicators to evaluate contaminant-related stress in fish, J. Aquat. Ecosyst. Stress Recovery, 1997, 6, 75–86CrossRefGoogle Scholar
  4. [4]
    Teh S.J., Adams S.M., Hinton D.E., Histopathologic biomarkers in feral freshwater fish populations exposed to different types of contaminant stress, Aquat. Toxicol., 1997, 37, 51–70CrossRefGoogle Scholar
  5. [5]
    Bernet D., Schmidt-Posthaus H., Wahli T., Burkhardt-Holm P., Evaluation of two monitoring approaches to assess effects of waste water disposal on histological alterations in fish, Hydrobiologia, 2004, 524, 53–66CrossRefGoogle Scholar
  6. [6]
    Camargo M.M.P., Martinez C.B.R., Histopathology of gills, kidney and liver of a Neotropical fish caged in an urban stream, Neotrop. Ichthyol., 2007, 5, 327–336CrossRefGoogle Scholar
  7. [7]
    Carbis C.R., Rawlin G.T., Grant P., Mitchell G.F., Anderson J.W., McCauley I., A study of feral carp, Cyprinus carpio L., exposed to Microcystis aeruginosa at Lake Mokoan, Australia, and possible implications for fish health, J. Fish Dis., 1997, 20, 81–91CrossRefGoogle Scholar
  8. [8]
    Dulić Z., Poleksić V., Rašković B., Lakić N., Marković Z., Živić I., et al., Assessment of the water quality of aquatic resources using biological methods, Desalin. Water Treat., 2009, 11, 264–274CrossRefGoogle Scholar
  9. [9]
    Madureira T.V., Rocha M.J., Cruzeiro C., Rodrigues I., Monteiro R.A.F., Rocha E., The toxicity potential of pharmaceuticals found in the Douro River estuary (Portugal): Evaluation of impacts on fish liver, by histopathology, stereology, vitellogenin and CYP1A immunohistochemistry, after sub-acute exposures of the zebrafish model, Environ. Toxicol. Pharmacol., 2012, 34, 34–45PubMedCrossRefGoogle Scholar
  10. [10]
    Bernet D., Schmidt H., Meier W., Burkhardt-Holm P., Wahli T., Histopathology in fish: proposal for a protocol to assess aquatic pollution, J. Fish Dis., 1999, 22, 25–34CrossRefGoogle Scholar
  11. [11]
    Ashley P.J., Fish welfare: Current issues in aquaculture, Appl. Anim. Behav. Sci., 2007, 104, 199–235CrossRefGoogle Scholar
  12. [12]
    Segner H., Sundh H., Buchmann K., Douxfils J., Sundell K.S., Mathieu C., et al., Health of farmed fish: its relation to fish welfare and its utility as welfare indicator, Fish Physiol. Biochem., 2012, 38, 85–105PubMedCrossRefGoogle Scholar
  13. [13]
    Rašković B., Poleksić V., Živić I., Spasić M., Histology of carp (Cyprinus carpio, L.) gills and pond water quality in semiintensive production, Bulg. J. Agric. Sci., 2010, 16, 253–262Google Scholar
  14. [14]
    Skorić S., Rašković B., Poleksić V., Gačić Z., Lenhardt M., Scoring of the extent and intensity of carp (Cyprinus carpio) skin changes made by cormorants (Phalacrocorax carbo sinensis): relationship between morphometric and histological indices, Aquac. Int., 2012, 20, 525–535CrossRefGoogle Scholar
  15. [15]
    Poleksić V., Vlahović M., Mitrović-Tutundžić V., Marković Z., Effects of environmental conditions on gill morphology of carp from the ‘Dubica’ farm during the 1998 rearing season, Acta Biol. Iugosl. (E Ichthyol.), 1999, 31, 43–52Google Scholar
  16. [16]
    Poleksić V., Dulić-Stojanović Z., Marković Z., Gill structure of carp fingerlings from Baranda fish farm, Acta Biol. Iugosl. (E Ichthyol.), 2002, 34, 11–22Google Scholar
  17. [17]
    Mommsen T., Vijayan M., Moon T., Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation, Rev. Fish Biol. Fish., 1999, 9, 211–268CrossRefGoogle Scholar
  18. [18]
    Harper C., Wolf J.C., Morphologic effects of the stress response in fish, ILAR J., 2009, 50, 387–396PubMedCrossRefGoogle Scholar
  19. [19]
    Svobodová Z., Lloyd R., Máchová J., Vykusová B., Water quality and fish health, Food and Agriculture Organization of the United Nations, Rome, 1993Google Scholar
  20. [20]
    Edwards E.A., Twomey K., Habitat suitability index models: common carp, U.S. Fish and Wildlife Service, Washington, DC, 1982Google Scholar
  21. [21]
    Humason G.L., Animal tissue techniques, 3rd, W. H. Freeman, San Francisco, 1979Google Scholar
  22. [22]
    Bechara J.A., Roux J.P., Ruiz Díaz F.J., Flores Quintana C.I., atLongoni de Meabe C.A., The effect of dietary protein level on pond water quality and feed utilization efficiency of pacú Piaractus mesopotamicus (Holmberg, 1887), Aquac. Res., 2005, 36, 546–553CrossRefGoogle Scholar
  23. [23]
    Gross A., Boyd C.E., Wood C.W., Nitrogen transformations and balance in channel catfish ponds, Aquac. Eng., 2000, 24, 1–14CrossRefGoogle Scholar
  24. [24]
    Kaushik S.J., Nutrient requirements, supply and utilization in the context of carp culture, Aquaculture, 1995, 129, 225–241CrossRefGoogle Scholar
  25. [25]
    Driver P.D., Closs G.P., Koen T., The effects of size and density of carp (Cyprinus carpio L.) on water quality in an experimental pond, Arch. Hydrobiol., 2005, 163, 117–131CrossRefGoogle Scholar
  26. [26]
    Lougheed V.L., Crosbie B., Chow-Fraser P., Predictions on the effect of common carp (Cyprinus carpio) exclusion on water quality, zooplankton, and submergent macrophytes in a Great Lakes wetland, Can. J. Fish. Aquat. Sci., 1998, 55, 1189–1197CrossRefGoogle Scholar
  27. [27]
    Marković Z., Common carp: rearing in fish ponds and cages [Šaran: gajenje u ribnjacima i kaveznim sistemima], Prof. dr Zoran Marković, Belgrade, 2010, (in Serbian)Google Scholar
  28. [28]
    Korwin-Kossakowski M., Growth and survival of carp (Cyprinus carpio L.) larvae in alkaline water, J. Fish Biol., 1992, 40, 981–982CrossRefGoogle Scholar
  29. [29]
    Boyd C.E., Water quality management of pond fish culture, Elsevier, Amsterdam, The Netherlands, 1982Google Scholar
  30. [30]
    Garg S.K., Bhatnagar A., Effect of varying closes of organic and inorganic fertilizers on plankton production and fish biomass in brackish water fish ponds, Aquac. Res., 1996, 27, 157–166CrossRefGoogle Scholar
  31. [31]
    Chughtai M.I., Mahmood K., Semi-intensive carp culture in saline water-logged area: A multi-location study in Shorkot (district Jhang), Pakistan, Pak. J. Zool., 2012, 44, 1065–1072Google Scholar
  32. [32]
    Boeck G., Nilsson G., Vlaeminck A., Blust R., Central monoaminergic responses to salinity and temperature rises in common carp, J. Exp. Biol., 1996, 199, 1605–1611PubMedGoogle Scholar
  33. [33]
    Altinok I., Grizzle J.M., Effects of low salinities on Flavobacterium columnare infection of euryhaline and freshwater stenohaline fish, J. Fish Dis., 2001, 24, 361–367CrossRefGoogle Scholar
  34. [34]
    Zhou B.S., Wu R.S.S., Randall D.J., Lam P.K.S., Ip Y.K., Chew S.F., Metabolic adjustments in the common carp during prolonged hypoxia, J. Fish Biol., 2000, 57, 1160–1171CrossRefGoogle Scholar
  35. [35]
    Vega M., Pardo R., Barrado E., Debán L., Assessment of seasonal and polluting effects on the quality of river water by exploratory data analysis, Water Res., 1998, 32, 3581–3592CrossRefGoogle Scholar
  36. [36]
    Holmstrup M., Bindesbøl A.-M., Oostingh G.J., Duschl A., Scheil V., Köhler H.-R., et al., Interactions between effects of environmental chemicals and natural stressors: A review, Sci. Total Environ., 2010, 408, 3746–3762PubMedCrossRefGoogle Scholar
  37. [37]
    Howe G.E., Marking L.L., Bills T.D., Rach J.J., Mayer F.L., Effects of water temperature and pH on toxicity of terbufos, trichlorfon, 4-nitrophenol and 2,4-dinitrophenol to the amphipod Gammarus pseudolimnaeus and rainbow trout (Oncorhynchus mykiss), Environ. Toxicol. Chem., 1994, 13, 51–66Google Scholar
  38. [38]
    Randall D.J., Tsui T.K.N., Ammonia toxicity in fish, Mar. Pollut. Bull., 2002, 45, 17–23PubMedCrossRefGoogle Scholar
  39. [39]
    Frances J., Nowak B.F., Allan G.L., Effects of ammonia on juvenile silver perch (Bidyanus bidyanus), Aquaculture, 2000, 183, 95–103CrossRefGoogle Scholar
  40. [40]
    Lease H.M., Hansen J.A., Bergman H.L., Meyer J.S., Structural changes in gills of Lost River suckers exposed to elevated pH and ammonia concentrations, Comp. Biochem. Phys. C, 2003, 134, 491–500Google Scholar
  41. [41]
    Benli A.Ç.K., Köksal G., Özkul A., Sublethal ammonia exposure of Nile tilapia (Oreochromis niloticus L.): Effects on gill, liver and kidney histology, Chemosphere, 2008, 72, 1355–1358PubMedCrossRefGoogle Scholar
  42. [42]
    Wilkie M.P., Wood C.M., Recovery from high pH exposure in the rainbow trout: white muscle ammonia storage, ammonia washout, and the restoration of blood chemistry, Physiol. Zool., 1995, 379–401Google Scholar
  43. [43]
    Wilkie M.P., Wright P.A., Iwama G.K., Wood C.M., The physiological adaptations of the Lahontan cutthroat trout (Oncorhynchus clarki henshawi) following transfer from well water to the highly alkaline waters of Pyramid Lake, Nevada (pH 9.4), Physiol. Zool., 1994, 355–380Google Scholar
  44. [44]
    Wright P.A., Iwama G.K., Wood C.M., Ammonia and urea excretion in Lahontan cutthroat trout (Oncorhynchus clarki henshawi) adapted to the highly alkaline Pyramid Lake (pH 9.4), J. Exp. Biol., 1993, 175, 153–172Google Scholar
  45. [45]
    Wang Y.S., Gonzalez R.J., Patrick M.L., Grosell M., Zhang C., Feng Q., et al., Unusual physiology of scale-less carp, Gymnocypris przewalskii, in Lake Qinghai: a high altitude alkaline saline lake, Comp. Biochem. Phys. A, 2003, 134, 409–421CrossRefGoogle Scholar
  46. [46]
    Spencer P., Pollock R., Dubé M., Effects of unionized ammonia on histological, endocrine, and whole organism endpoints in slimy sculpin (Cottus cognatus), Aquat. Toxicol., 2008, 90, 300–309PubMedCrossRefGoogle Scholar
  47. [47]
    Sollid J., Nilsson G.E., Plasticity of respiratory structures — Adaptive remodeling of fish gills induced by ambient oxygen and temperature, Respir. Physiol. Neurobiol., 2006, 154, 241–251PubMedCrossRefGoogle Scholar
  48. [48]
    Karan V., Vitorović S., Tutundžić V., Poleksić V., Functional enzymes activity and gill histology of carp after copper sulfate exposure and recovery, Ecotoxicol. Environ. Saf., 1998, 40, 49–55PubMedCrossRefGoogle Scholar
  49. [49]
    Nilsson G.E., Gill remodeling in fish — a new fashion or an ancient secret?, J. Exp. Biol., 2007, 210, 2403–2409PubMedCrossRefGoogle Scholar
  50. [50]
    Poleksić V., Mitrović-Tutundžić V., Fish gills as a monitor of sublethal and chronic effects of pollution, In: Muller R., Lloyd R. (Eds.), Sublethal and chronic toxic effects of pollutants on freshwater fish, Blackwell Scientific Publications Ltd., Oxford, 1994Google Scholar
  51. [51]
    Fernandes M.N., Mazon A.F., Environmental pollution and fish gill morphology, In: Val L., Kapoor B.G. (Eds.), Fish Adaptations, Science Publishers, Enfield, 2003Google Scholar
  52. [52]
    Mallatt J., Fish gill structural changes induced by toxicants and other irritants: a statistical review, Can. J. Fish. Aquat. Sci., 1985, 42, 630–648CrossRefGoogle Scholar
  53. [53]
    Booth J.H., The effects of oxygen supply, epinephrine, and acetylcholine on the distribution of blood flow in trout gills, J. Exp. Biol., 1979, 83, 31–39Google Scholar
  54. [54]
    Schmidt H., Bernet D., Wahli T., Meier W., Burkhardt-Holm P., Active biomonitoring with brown trout and rainbow trout in diluted sewage plant effluents, J. Fish Biol., 1999, 54, 585–596CrossRefGoogle Scholar
  55. [55]
    Koponen K., Myers M.S., Ritola O., Huuskonen S.E., Lindström-Seppä P., Histopathology of feral fish from a PCB-contaminated freshwater lake, AMBIO, 2001, 30, 122–126PubMedGoogle Scholar
  56. [56]
    Reite O.B., Mast cells/eosinophilic granule cells of teleostean fish: a review focusing on staining properties and functional responses, Fish Shellfish Immunol., 1998, 8, 489–513CrossRefGoogle Scholar
  57. [57]
    Silva A.G., Martinez C.B.R., Morphological changes in the kidney of a fish living in an urban stream, Environ. Toxicol. Pharmacol., 2007, 23, 185–192PubMedCrossRefGoogle Scholar
  58. [58]
    Reimschuessel R., A fish model of renal regeneration and development, ILAR J., 2001, 42, 285–291PubMedCrossRefGoogle Scholar

Copyright information

© Versita Warsaw and Springer-Verlag Wien 2013

Authors and Affiliations

  • Božidar Rašković
    • 1
  • Ivan Jarić
    • 2
  • Vesna Koko
    • 3
  • Milan Spasić
    • 1
  • Zorka Dulić
    • 1
  • Zoran Marković
    • 1
  • Vesna Poleksić
    • 1
  1. 1.Faculty of Agriculture, ZemunUniversity of BelgradeBelgradeSerbia
  2. 2.Institute for Multidisciplinary ResearchUniversity of BelgradeBelgradeSerbia
  3. 3.Faculty of BiologyUniversity of BelgradeBelgradeSerbia

Personalised recommendations