Skip to main content
Log in

The Role of Trace Elements in the Adaptation of Fish Metabolism under Reduced Pollution: A Case Study of the Subarctic Lake Imandra

  • Published:
Geochemistry International Aims and scope Submit manuscript

Abstract

The mechanisms of fish adaptation to survival in the historically contaminated Lake Imandra were studied. The role of trace elements in the protective functions of the organism and their importance in the re-adaptation of organisms to improving the habitat was established. The lake whitefish (Coregonus lavaretus L.) unable to migrate for large distance was chosen as the object of research. The indices of red blood as an indicator of fish homeostasis, as well as the role of white blood cells in the activation of the immune system were examined. The causes of the occurrence of histopathologies of organs and tissues are explained. Data on the accumulation of trace elements in the body of fish from this lake are presented. The principal difference in the bioaccumulation of elements is the intense metabolism of Se. An elevated S to Se ratio indicates a high antioxidant status of fish from the historically contaminated part of the lake, while an increased accumulation of Fe, Cu, and Se can serve as a marker of liver pathologies, and Zn and Co, of kidney pathologies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. S. I. M. Abril, C. Dalmolin, P. G. Costa, and A. Bianchini, “Expression of genes related to metal metabolism in the freshwater fish Hyphessobrycon luetkenii living in a historically contaminated area associated with copper mining,” Environ. Toxicol. Pharmacol. 60, 146–156 (2018).

    Article  Google Scholar 

  2. E. Agamy, “Histopathological liver alterations in juvenile rabbit fish (Siganus canaliculatus) exposed to light Arabian crude oil, dispersed oil and dispersant,” Ecotoxicol. Environ. Saf. 75, 171–179 (2012).

    Article  Google Scholar 

  3. M. K. Ahmed, M. H. Al-Mamun, E. Parvin, M. S. Akter, and M. S. Khan, “Arsenic induced toxicity and histopathological changes in gill and liver tissue of freshwater fish, tilapia (Oreochromis mossambicus),” Exp. Tox. Pathol. 65 (6), 903–909 (2013).

    Article  Google Scholar 

  4. D. Bernet, H. Schmidt, W. Meier, P. Burkhardt-Holm, and T. Wahli, “Histopathology in fish: proposal for a protocol to assess aquatic pollution,” J. Fish Dis. 22, 25–34 (1999).

    Article  Google Scholar 

  5. M. Chadzinska, P. Baginski, E. Kolaczkowska, H. F  J. Savelkoul, and B. M. L. V. Kemenade, “Expression profiles of matrix metalloproteinase 9 in teleost fish provide evidence for its active role in initiation and resolution of inflammation,” Immunology 125, 601–610 (2008).

    Article  Google Scholar 

  6. N. J. Clark, B. J. Shaw, and R. D. Handy, “Low hazard of silver nanoparticles and silver nitrate to the haematopoietic system of rainbow trout,” Ecotoxicol. Environ. Saf. 152, 121–131 (2018).

    Article  Google Scholar 

  7. A. T. Correia, D. Rebelo, J. Marques, and B. Nunes, “Effects of the chronic exposure to cerium dioxide nanoparticles in Oncorhynchus mykiss: Assessment of oxidative stress, neurotoxicity and histological alterations,” Environ. Toxicol. Phar. 68, 27–36 (2019).

    Article  Google Scholar 

  8. A. T. Correia, S. Rodrigues, D. Ferreira-Martins, A. C. Nunes, M. I. Ribeiro, and S. C. Antunes, “Multi-biomarker approach to assess the acute effects of cerium dioxide nanoparticles in gills, liver and kidney of Oncorhynchus mykiss,” Comp. Biochem. Physiol. C: Pharmacol. Toxicol. 238, 108842 (2020).

    Google Scholar 

  9. P. M. Costa, M. S. Diniz, S. Caeiro, J. Lobo, M. Martins, A. M. Ferreira, M. Caetano, C. Vale, T. Á. DelValls, and M. H. Costa, “Histological biomarkers in liver and gills of juvenile Solea senegalensis exposed o contaminated estuarine sediments: a weighted indices approach,” Aquat. Toxicol. 92, 202–212 (2009).

    Article  Google Scholar 

  10. W. F. da Silva, M. I. Egami, A. A. Santos, M. A. Antoniazzi, M. Silva, R. C. Gutierre, and M. J. R. Paiva, “Cytochemical, immunocytochemical and ultrastructural observations on leukocytes and thrombocytes of fat snook (Centropomus parallelus),” Fish Shellfish Immunol. 31, 571–577 (2011).

    Article  Google Scholar 

  11. W. F. da Silva, M. J. Simões, R. C. Gutierre, M. I. Egami, A. A. Santos, M. M. Antoniazzi, G. R. Sasso, and M. J. T. Ranzani-Paiva, “Special dyeing, histochemistry, immunohistochemistry and ultrastructure: A study of mast cells/eosinophilic granules cells (MCs/EGC) from Centropomus parallelus intestine,” Fish Shellfish Immunol. 60, 502–508 (2017).

    Article  Google Scholar 

  12. K. B. Elahee and S. Bhagwant, “Hematological and gill histopathological parameters of three tropical fish species from a polluted lagoon on the west coast of Mauritius,” Ecotoxicol. Environ. Saf. 68, 361–371 (2007).

    Article  Google Scholar 

  13. V. V. Ermakov, “Biogeochemical provinces: concept, classification, and ecological assessment, Main Directions in Geochemistry. On 100 th Anniversary of Academician A.P. Vinogradov (Nauka, Moscow, 1995), pp. 183–196 [in Russian].

  14. Fish Physiology: Homeostasis and Toxicology of Essential Metals, Ed. by C. M. Wood, A. P. Farrell, and C. J. Brauner (Academic Press, London, 2012), Vol. 31A.

  15. J. Galindo-Villegas, E. Garcia-Garcia, and V. Mulero, “Role of histamine in the regulation of intestinal immunity in fish,” Dev. Comp. Immunol. 64, 178–186 (2016).

    Article  Google Scholar 

  16. N. A. Gashkina, “Essential elements in the organs and tissues of fish depending on the freshwater toxicity and physiological state,” Geochem. Int. 55 (10), 927–934 (2017).

    Article  Google Scholar 

  17. N. A. Gashkina and T. I. Moiseenko, “Adaptation of fish metabolism to thermal pollution of subarctic Lake Imandra,” Geochem. Int. 58 (10), 1110–1122 (2020).

    Article  Google Scholar 

  18. N. A. Gashkina and T. I. Moiseenko, “Influence of thermal pollution on the physiological conditions and bioaccumulation of metals, metalloids, and trace metals in whitefish (Coregonus lavaretus L.),” Int. J. Mol. Sci. 12, 4343 (2020).

    Article  Google Scholar 

  19. N. A. Gashkina, T. I. Moiseenko, and L. P. Kudryavtseva, “Fish response of metal bioaccumulation to reduced toxic load on long-term contaminated Lake Imandra,” Ecotoxicol. Environ. Saf. 191, 110205 (2020).

    Article  Google Scholar 

  20. M. B. Griffith, “Toxicological perspective on the osmoregulation and ionoregulation physiology of major ions by freshwater animals: teleost fish, crustacea, aquatic insects, and mollusca,” Environ. Toxicol. Chem. 36 (3), 576–600 (2017).

    Article  Google Scholar 

  21. Handbook on the Toxicology of Metals, 3th edition (Academic Press, Amsterdam–Boston, 2007).

  22. Hematology: Basic Principles and Practice, 7th Ed., Ed. by R. Hoffman, E. J. Benz, L. E. Silberstein, H. E. Heslop, J. I. Weitz, J. Anastasi, M. E. Salama, and S. A. Abutalib (Elsevier, Philadelphia, 2018).

    Google Scholar 

  23. A. Herrero, K. D. Thompson, A. Ashby, H. D. Rodger, and M. P. Dagleish, “Complex gill disease: an emerging syndrome in farmed Atlantic salmon (Salmo salar L.),” J. Comp. Path. 163, 23–28 (2018).

    Article  Google Scholar 

  24. D. E. Hinton, P. C. Baumann, G. C. Gardner, W. E. Hawkins, J. D. Hendricks, R. A. Murchelano, and M. S. Okihiro, “Histopathologic biomarkers,” In Biomarkers: Biochemical, Physiological and Histological Markers of Anthropogenic Stress, Ed. by R. J. Huggett, R. A. Kimerly, P. M. Mehrle, and H. L. Bergman (Boca Raton, CRC Press, London–New York, 2017), pp. 155–210.

  25. H. Kaya, F. Aydın, M. Gürkan, S. Yılmaz, M. Ates, V. Demir, and Z. Arslan, “A comparative toxicity study between small and large size zinc oxide nanoparticles in tilapia (Oreochromis niloticus): Organ pathologies, osmoregulatory responses and immunological parameters,” Chemosphere. 144, 571–582 (2016).

    Article  Google Scholar 

  26. A. Yu. Klishin, “Morphofunctional changes of lamellae and phylaments of pike gills (Esox lucius),” Community and Civilization in 21rst Century: Tendencies and Prospects of Evolution, (Nuachn-Issled. Publ., Voronezh, 2014), pp. 25–29 [in Russian].

    Google Scholar 

  27. V. V. Koval’skii, “Origin and evolution of biosphere,” Usp. Sovremen. Biol. 55 (1), 45–67 (1963).

    Google Scholar 

  28. V. V. Koval’skii, Geochemical Ecology (Nauka, Moscow, 1974) [in Russian].

    Google Scholar 

  29. O. N. Krylov, Textbook on Prophylactics and Diagnostics of Fish Poisoning by Toxicants (Moscow, 1980) [in Russian].

    Google Scholar 

  30. O. I. Kubrak, V. V. Husak, B. M. Rovenko, J. M. Storey, K. B. Storey, and V. I. Lushchak, “Cobalt-induced oxidative stress in brain, liver and kidney of goldfish Carassius auratus,” Chemosphere 85, 983–989 (2011).

    Article  Google Scholar 

  31. T. B. Lapirova and E. A. Zabotkina, “A comparative analysis of parameters of immunophysiological state of bream Abramis Brama (L.) from variably contaminated sites of the Rybinsk Reservoir,” Biol. Vnutren. Morei 3 (2), 86–91 (2010).

    Google Scholar 

  32. C. B. Martinez, M. Y. Nagae, C. T. B. Zaia, and D. M. A. Zaia, “Morphological and physiological acute effects of lead in the neotropical fish Prochilodus lineatus,” Brazil. J. Biol. 64, 797–807 (2004).

    Google Scholar 

  33. A. K. Mishra and B. Mohanty, “Acute toxicity impacts of hexavalent chromium on behavior and histopathology of gill, kidney and liver of the freshwater fish, Channa punctatus (Bloch),” Environ. Toxicol. Pharmacol. 26, 136–141 (2008).

    Article  Google Scholar 

  34. T. I. Moiseenko and L. P. Kudryavtseva, “Trace metals accumulation and fish pathologies in areas affected by mining and metallurgical enterprises in the Kola Region, Russia,” Environ. Pollut. 114 (2), 285–297 (2001).

    Article  Google Scholar 

  35. T. Moiseenko and A. Sharov, “Large Russian lakes Ladoga, Onega, and Imandra under strong pollution and in the period of revitalization: a review,” Geosci. 9 (12), 492 (2019).

    Article  Google Scholar 

  36. T. I. Moiseenko, N. A. Gashkina, A. N. Sharov, O. I. Vandysh, and L. P. Kudryavtseva, “Anthropogenic transformations of the Arctic ecosystem of Lake Imandra: tendencies for recovery after long period of pollution,” Water Res. 36 (3), 296–309 (2009).

    Article  Google Scholar 

  37. T. I. Moiseenko, B. A. Morgunov, N. A. Gashkina, V. V. Megorskiy, and A. A. Pesiakova, “Ecosystem and human health assessment in relation to aquatic environment pollution by heavy metals: case study of northwest of the Russian arctic, Kola peninsula,” Environ. Res. Lett. 13, 065005 (2018).

    Article  Google Scholar 

  38. T. I. Moiseenko, V. A. Dauvalter, A. A. Lukin, L. P. Kudryavtseva, B. P. Il’yashchuk, L. I. Il’yashchuk, S. S. Sandimirov, L. Ya. Kagan, O. I. Vandysh, A. N. Sharov, Yu. N. Sharova, and I. N. Koroleva, Anthropogenic Modifications of Ecosystem of Lake Imandra (Nauka, Moscow, 2002) [in Russian].

    Google Scholar 

  39. S. M. Monteiro, E. Rocha, A. Fontaínhas-Fernandes, and M. Sousa, “Quantitative histopathology of Oreochromis niloticus gills after copper exposure,” J. Fish Biol. 73, 1376–1392 (2008).

    Article  Google Scholar 

  40. S. M. Monteiro, J. M. Mancera, A. Fontaínhas-Fernandes, and M. Sousa, “Copper induced alterations of biochemical parameters in the gill and plasma of Oreochromis niloticus,” Comp. Biochem. Physiol. C: Pharmacol. Toxicol. 141, 375–383 (2005).

    Google Scholar 

  41. N. Nero, A. Farwell, A. Lister, G. van Der Kraak, L. E. J. Lee, T. van Meer, M. D. MacKinnon, and D. G. Dixon, “Gill and liver histopathological changes in yellow perch (Perca flavescens) and goldfish (Carassius auratus) exposed to oil sands process-affected water,” Ecotoxicol. Environ. Saf. 63, 365–377 (2006).

    Article  Google Scholar 

  42. A. Nogueira-Pedro G. G. dos Santos, D. C. Oliveira, A. A. Hastreiter, and R. A. Fock, “Erythropoiesis in vertebrates: from ontogeny to clinical relevance,” Front. Biosci., Elite. 8, 100–112 (2016).

    Google Scholar 

  43. J. B. Ortiz, M. L. G. De Canales, and C. Sarasquete, “Histopathological changes induced by lindane (γ-HCH) in various organs of fishes,” Sci. Mar. 67(1), 53–61 (2003).

    Article  Google Scholar 

  44. M. Palikova, I. Papezikova, Z. Markova, S. Navratil, J. Mares, L. Mares, L. Vojtek, P. Hyrsl, E. Jelinkova, and H. Schmidt-Posthaus, “Proliferative kidney disease in rainbow trout (Oncorhynchus mykiss) under intensive breeding conditions: pathogenesis and haematological and immune parameters,” Vet. Parasitol. 238, 5–16 (2017).

    Article  Google Scholar 

  45. L. Pijanowski, B. M. Verburg-van Kemenade, and M. Chadzinska, “Chemokine CXCb1 stimulates formation of NETs in trunk kidney neutrophils of common carp,” Dev. Comp. Immunol. 103, 103521 (2020).

    Article  Google Scholar 

  46. I. F. Pravdin, Guidebook on The Study of Fish (Pishchevaya Prom., Moscow, 1966) [in Russian].

    Google Scholar 

  47. A. Ratn, R. Prasad, Y. Awasthi, M. Kumar, A. Misra, and S. P. Trivedi, “Zn2+ induced molecular responses associated with oxidative stress, DNA damage and histopathological lesions in liver and kidney of the fish, Channa punctatus (Bloch, 1793),” Ecotoxicol. Environ. Saf. 151, 10–20 (2018).

    Article  Google Scholar 

  48. O. B. Reite and Ø. Evensen, “Inflammatory cells of teleostean fish: A review focusing on mast cells/eosinophilic granule cells and rodlet cells,” Fish Shellfish Immunol. 20, 192–208 (2006).

    Article  Google Scholar 

  49. M. Sakamoto, A. Yasutake, J. Domingo, H. M. Chan, M. Kubota, and K. Murata, “Relationships between trace elements concentration in chorionic tissue of placenta and umbilical cord tissue: Potential use as indicators for prenatal exposure,” Environ. Intern. 60, 106–111 (2013).

    Article  Google Scholar 

  50. Standards of Water Quality of Fishery Water Bodies, Including Standards of Maximum Permissible Concentrations of Toxic Matters in Waters of Fishery Water Bodies (VNIRO, Moscow, 2011) [in Russian].

  51. G. D. Stentiford, M. Longshaw, B. P. Lyons, G. Jones, M. Green, and S. W. Feist, “Histopathological biomarkers in estuarine fish species for the assessment of biological effects of contaminants,” Mar. Environ. Res. 55, 137–159 (2003).

    Article  Google Scholar 

  52. B. Talukdar, H. K. Kalita, S. Basumatary, D. J. Saikia, and D. Sarma, “Cytotoxic and genotoxic affects of acid mine drainage on fish Channa punctata (Bloch),” Ecotoxicol. Environ. Saf. 144, 72–78 (2017).

    Article  Google Scholar 

  53. R. van der Oost, J. Beyer, and N. P. E. Vermeulen, “Fish bioaccumulation and biomarkers in environmental risk assessment: a review,” Environ. Toxicol. Pharmacol. 13, 57–149 (2003).

    Article  Google Scholar 

  54. A. P. Vinogradov, “Biogeochemical provinces and their role in organic evolution,” Geokhimiya, No. 3, 199–242 (1963).

    Google Scholar 

  55. Y. Wang, J. Fang, S. S. Leonard, and K. M. Rao, “Cadmium inhibits the electron transfer chain and induces reactive oxygen species,” Free Radic. Biol. Med. 36, 1434–1443 (2004).

    Article  Google Scholar 

  56. A. K. Whitfield and M. Elliott, “Fish as indicators of environmental and ecological changes within estuaries: a review of progress and some suggestions for the future,” J. Fish Biol. 61, 229–250 (2002).

    Article  Google Scholar 

  57. S. K. Whyte, “The innate immune response of finfish – a review of current knowledge,” Fish Shellfish Immunol. 23, 1127–1151 (2007).

    Article  Google Scholar 

  58. C. M. Wood and J. Eom, “The osmorespiratory compromise in the fish gill,” Comp. Biochem. Physiol. A: Physiol. 254, 110895 (2021).

    Article  Google Scholar 

  59. X. Xia, X. Wang, W. Qin, J. Jiang, and L. Cheng, “Emerging regulatory mechanisms and functions of autophagy in fish,” Aquaculture 511, 734212 (2019).

    Article  Google Scholar 

  60. Yeom D.-H. and S. M. Adams, “Assessing effects of stress across levels of biological organization using an aquatic ecosystem health index,” Ecotoxicol. Environ. Saf. 67, 286–295 (2007).

    Article  Google Scholar 

  61. E. A. Zabotkina, “Influence of organic and inorganic toxicants on the structure of melano-macrofagal centers of bony fishes. A review,” Tr. IBVV RAS 77 (80), 20–32 (2017).

    Google Scholar 

  62. E. A. Zabotkina, T. B. Lapirova, and E. A. Nazarova, “Influence of cadmium ions on some morphofunctional and immune-physiological parameters of perch (Perca fluviatilis, Perciformes, Percidae) underyearlings,” J. Ichthyol. 49 (1), 111–1184 (2009).

    Article  Google Scholar 

Download references

ACKNOWLEDGMENTS

This study was supported by the State Task of the Vernadsky Institute of Geochemistry and Analytcial Chemistry (project no. 0137-2019-0008).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. A. Gashkina.

Ethics declarations

The authors declare that they have no conflicts of interest.

Additional information

Translated by M. Bogina

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gashkina, N.A., Moiseenko, T.I., Shuman, L.A. et al. The Role of Trace Elements in the Adaptation of Fish Metabolism under Reduced Pollution: A Case Study of the Subarctic Lake Imandra. Geochem. Int. 60, 154–169 (2022). https://doi.org/10.1134/S0016702922020057

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0016702922020057

Keywords:

Navigation