Skip to main content
SpringerLink
Log in

Assessment of the joint effect of thermal stress, pollution, and parasitic infestation on the activity of antioxidative enzymes in pulmonate mollusk Lymnaea stagnalis

  • Published:
Contemporary Problems of Ecology Aims and scope

Abstract

This study makes a multifactor analysis of the joint effect of reservoir contamination, parasitic infestation, and experimental hyperthermia on the activity of antioxidative enzymes (peroxidase, catalase, and glutathione S-transferase) in the pulmonate mollusk Lymnaea stagnalis from the clean Naroch Lake and contaminated Chizhovsky Reservoir in the Republic of Belarus. The activity of peroxidase is ascertained to be affected most strongly by the simultaneous effect of parasitic infestation and reservoir contamination and parasitic infestation coupled with experimental hyperthermia. The joint effect of parasitic infestation and reservoir pollution is found to influence the activity of catalase. Meanwhile, no correlation is found between the studied factors and the activity of glutathione S-transferase. It is shown that there is no mutual influence of the three studied factors on the activity of the investigated enzymes.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abele, D., Tesch, C., Wencke, P., et al., How does oxidative stress relate to thermal tolerance in the Antarctic bivalve Yoldia eightsi? Antarct. Sci., 2001, vol. 13, no. 2, pp. 111–118.

    Article  Google Scholar 

  • Adema, C.M., Sapp, K.K., Hertel, L.A., and Loker, E.S., Immunobiology of the relationships of the echinostomes with snail intermediate hosts, in Echinostomes as Experimental Models for Biological Research, Dordrecht: Kluwer, 2000, pp. 149–173.

    Chapter  Google Scholar 

  • Aebi, H., Catalase in vitro, Methods Enzymol., 1984, vol. 105, pp. 121–126.

    Article  CAS  PubMed  Google Scholar 

  • Ataev, G.L. and Coustau, C., Cellular response to Echinostoma caproni infection in Biomphalaria glabrata strains selected for susceptibility resistance, Dev. Comp. Immunol., 1999, vol. 23, pp. 187–198.

    Article  CAS  PubMed  Google Scholar 

  • Ataev, G.L. and Molevshchikov, A.V., Protective reactions of gastropod molluscs. 1. Cell reactions, Parazitologiya, 2004, no. 4, pp. 342–351.

    Google Scholar 

  • Axenov-Gribanov, D.V., Vereshchagina, K.P., Lubyaga, Yu.A., Gurkov, A.N., Bedulina, D.S., Shatilina, Zh.M., Khomich, A.S., Golubev, A.P., and Timofeyev, M.A., Stress response at the cellular and biochemical levels indicates the limitation of the environmental temperature range for Eastern Siberia populations of the common gastropod Lymnaea stagnalis, Malacologia, 2015, vol. 59, no. 1, pp. 33–34.

    Article  Google Scholar 

  • Bechtold, D.A., Rush, S.J., and Brown, I.R., Localization of the heat-sock protein HSP70 to the synapse following hypertermic stress in the brain, J. Neurochem., 2000, vol. 74, pp. 641–646.

    Article  CAS  PubMed  Google Scholar 

  • Bondarevich, N.V., Kozlovskii, I.S., and Novik, G.I., microbiological plankton of the Svisloch’ River with the channel in Minsk, Mater. 7oi Vseross. nauchnoprakt. konf. s mezhdunar. uchastiem “Ekologicheskie problemy promyshlennykh gorodov,” Saratov, 8–10 aprelya 2015 g., Tezisy dokladov (Proc. 7th All-Russ. Sci.- Pract. Conf. with Int. Participation “Ecological Problems of Industrial Cities,” Saratov, April 8–10, 2015, Abstracts of Papers), Saratov, 2015, pp. 24–26.

    Google Scholar 

  • Borovikov, V.P., Iskusstvo analiza dannykh na komp’yutere (The Art of Computer Data Analysis), St. Petersburg: Statistica. 2003.

    Google Scholar 

  • Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, vol. 72, nos. 1–2, pp. 248–254.

    Article  CAS  PubMed  Google Scholar 

  • Camargo, J.A. and Alonso, Á., Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment, Environ. Int., 2006, vol. 32, no. 6, pp. 831–849.

    Article  CAS  PubMed  Google Scholar 

  • Chapple, J.P., Smerdon, G.R., and Hawkirs, A.J.S., Stress-70 protein induction in Mitilis edulis: tissuespecific responses to elevated temperature reflect relative vulnerability and physiological function, J. Exp. Mar. Biol. Ecol., 1997, vol. 217, pp. 225–235.

    Article  CAS  Google Scholar 

  • Chuiko, G.M., Tillitt, D.E., and Zajicek, J.L., Chemical contamination of the Rybinsk reservoir, northwest Russia: relationship between liver polychlorinated biphenyls (PCB) content and health indicators in bream (Abramis brama), Chemosphere, 2007, vol. 67, no. 3, pp. 527–536.

    Article  CAS  PubMed  Google Scholar 

  • Connors, V.A., Lodes, M.J., and Yoshin, T.P., Identification of Schistosoma mansoni sporocyst excretory secretory antioxidant molecule and its effect on superoxide production by Biomphalaria glabrata hemocytes, J. Invertebr. Pathol., 1991, vol. 58, pp. 387–395

    Article  CAS  PubMed  Google Scholar 

  • Dorozhenkova, T.E. and Bekish, O.Ya.L., Sposob opredeleniya vidovoi prinadlezhnosti tserkariev ptich’ikh trematod semeistva Schistosomatidae v bryukhonogikh legochnykh mollyuskakh. Instruktsiya po primeneniyu (Determination of Species Affiliation of Cercariae of the Bird Trematodes of Family Schistosomatidae in Pulmonary Gastropods: Instruction for Implementation), Minsk: Minist. Zdravookhr. Resp. Belarus, 2007.

    Google Scholar 

  • Drotar, A., Phelps, P., and Fall, R., Evidence for glutathione peroxidase activities in cultured plant cells., Plant Sci., 1985, vol. 42, pp. 35–40.

    Article  CAS  Google Scholar 

  • Habig, W.H., Pabst, M.J., and Jakoby, W.B., Glutathione S-transferases: the first enzymatic step in mercapturic acid formation, J. Biol. Chem., 1974, vol. 249, pp. 7130–7139.

    CAS  PubMed  Google Scholar 

  • Gladyshev, M.B., Gribovskaya, I.V., and Ivanova, E.A., Metal concentrations in the ecosystem and around recreational and fish-breeding pond Bugach, Water Resour., 2001, vol. 28, no. 3, pp. 288–296.

    Article  CAS  Google Scholar 

  • Gnatishina, L.L., Fal’fushinskaya, G.I., Golubev, A.P., Dallinger, R., and Stoliar, O.B., Role of metallothioneins in adaptation of Lymnaea stagnalis (Mollusca: Pulmonata) to environment pollution, Hydrobiol. J., 2011, vol. 47, no. 5, pp. 56–66.

    Article  Google Scholar 

  • Golubev, A.P., Thermoresistance and radioresistance of the population of Lymnaea stagnalis (Gastropoda, Pulmonata) from water bodies with different types of anthropogenic pressure, Dokl. Biol. Sci., 1995, vol. 342, no. 2, pp. 280–283.

    CAS  Google Scholar 

  • Golubev, A.P., Samooplodotvorenie u presnovodnykh legochnykh mollyuskov. Kolichetvennaya otsenka i adaptivnoe znachenie (Autogamy of Freshwater Pulmonata Mollusks: Quantitative Evaluation and Adaptive Value), Minsk: Pravo i Ekonomika, 2014.

    Google Scholar 

  • Golubev, A., Afonin, V., Maksimova, S., and Androsov, V., The current state of pond snail Lymnaea stagnalis (Gastropoda, Pulmonata) populations from water reservoirs of the Chernobyl nuclear accident zone, Radioprotection, 2005, vol. 40, no. 1, pp. 511–517.

    Article  Google Scholar 

  • Grosell, M., Gerdes, R.M., and Brix, K.V., Chronic toxicity of lead to three freshwater invertebrates—Brachionus calyciflorus, Chironomus tentans, and Lymnaea stagnalis, Environ. Toxicol. Chem., 2006, vol. 25, no. 1, pp. 97–104.

    Article  CAS  PubMed  Google Scholar 

  • Haas, W., Parasitic worms: strategies of host finding, recognition and invasion, Zoology, 2003, vol. 106, pp. 349–364.

    Article  PubMed  Google Scholar 

  • Hellou, J. and Law, R.J., Stress on stress response of wild mussels, Mytilus edulis and Mytilus trossulus, as an indicator of ecosystem health, Environ. Pollut., 2003, vol. 126, no. 3, pp. 407–416.

    CAS  PubMed  Google Scholar 

  • Hochachka, P.W. and Somero, G.N., Biochemical Adaptation: Mechanism and Process in Physiological Evolution, New York: Oxford Univ. Press, 2016.

    Google Scholar 

  • Kamlyuk, L.V., Semenyuk, G.A., and Eremova, N.G., Dominant complex and seasonal dynamics of development of zooplankton in urban reservoirs, Vestn. Belarus. Gos. Univ., 2002, pp. 40–45.

    Google Scholar 

  • Kryukova, N.A., Yurlova, N.I., Rastyagenko, N.M., Antonova, E.V., and Glupov, V.V., The influence of Plagiorchis mutationis larval infection on the cellular immune response of the snail host Lymnaea stagnalis, J. Parasitol., 2014, vol. 100, no. 3, pp. 284–287.

    Article  PubMed  Google Scholar 

  • Lushchak, V.I., Environmentally induced oxidative stress in aquatic animals, Aquat. Toxicol., 2011, no. 10, pp. 13–30.

    Article  Google Scholar 

  • Lushchak, V.I., Bagnyukova, T.V., Husak, V.V., et al., Hyperoxia results in transient oxidative stress and an adaptive response by antioxidant enzymes in goldfish tissues, Int. J. Biochem. Cell Biol., 2005, vol. 37, pp. 1670–1680.

    Article  CAS  PubMed  Google Scholar 

  • Ostapenya, A.P., Zhukova, T.V., Mikheeva, T.M., Kovalevskaya, R.Z., Makarevich, T.A., Zhukova, A.A., Luk’yanova, E.V., Nikitina, L.V., Makarevich, O.A., Dubko, N.V., Karabanovich, V.S., Savich, I.V., and Veres, Yu.K., Benthification of the lake ecosystems: reasons, mechanisms, possible consequences, and prospective studies, Tr. Belarus. Gos. Univ., 2012, no. 7, pp. 135–148.

    Google Scholar 

  • Sidorov, A.V., Influence of temperature on respiration, defensive behavior, and locomotion of freshwater snail Lymnaea stagnalis, Zh. Vyssh. Nervn. Deyat. im. I.P. Pavlova, 2003, no. 4, pp. 513–517.

    Google Scholar 

  • Soldánová, M., Selbach, C., Sures, B., Kostadinova, A., and Pérez-del-Olmo, A., Larval trematode communities in Radix auricularia and Lymnaea stagnalis in a reservoir system of the Ruhr River, Parasites Vectors, 2010, vol. 3, no. 1, p.56.

    Article  PubMed  PubMed Central  Google Scholar 

  • Spees, J.L., Chang, S.A., Mykles, D.L., et al., Molt cycledependent molecular chaperone and polyubiquitin gene expression in lobster, Cell Stress Chaperones, 2003, vol. 8, no. 3, pp. 258–264.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teskey, M.L., Lukowiak, K.S., Riaz, H., Dalesman, S., and Lukowiak, K., What’s hot: the enhancing effects of thermal stress on long-term memory formation in Lymnaea stagnalis, J. Exp. Biol., 2012, vol. 215, no. 24, pp. 4322–4329.

    Article  PubMed  Google Scholar 

  • Troschinski, S., Di Lellis, M.A., Sereda, S., Hauffe, T., Wilke, T., Triebskorn, R., and Kohler, H.R., Intraspecific variation in cellular and biochemical heat response strategies of Mediterranean Xeropicta derbentina (Pulmonata, Hygromiidae), PLoS One, 2014, vol. 9, no. 1, p. e86613.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tunholi-Alves, V.M., Tunholi, V.M., Castro, R.N., Sant’Ana, L.D.O., Santos-Amaral, L., de Oliveira, A.P.M., and Maldonado, A., Activation of anaerobic metabolism in Biomphalaria glabrata (Mollusca: Gastropoda) experimentally infected by Angiostrongylus cantonensis (Nematoda, Metastrongylidae) by high-performance liquid chromatography, Parasitol. Int., 2014, vol. 63, no. 1, pp. 64–68.

    Article  CAS  PubMed  Google Scholar 

  • Van der Schalie, H. and Berry, E.G., Effects of Temperature on Growth and Reproduction of Aquatic Snails, Washington: US Environ. Protect. Agency, 1973.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. International Sakharov Environmental Institute of Belarusian State University, Minsk, 220070, Republic of Belarus

    A. S. Khomich, O. A. Bodilovskaya & A. P. Golubev

  2. Research Institute of Biology, Irkutsk State University, Irkutsk, 664003, Russia

    D. V. Axenov-Gribanov, Y. A. Shirokova, E. P. Shchapova, Y. A. Lubyaga, Z. M. Shatilina & V. A. Emshanova

  3. Baikalian Research Centre, Irkutsk, 664003, Russia

    D. V. Axenov-Gribanov & Z. M. Shatilina

Authors
  1. A. S. Khomich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. V. Axenov-Gribanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. O. A. Bodilovskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Y. A. Shirokova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. P. Shchapova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Y. A. Lubyaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Z. M. Shatilina
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. V. A. Emshanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. A. P. Golubev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. S. Khomich.

Additional information

Original Russian Text © A.S. Khomich, D.V. Axenov-Gribanov, O.A. Bodilovskaya, Y.A. Shirokova, E.P. Shchapova, Y.A. Lubyaga, Z.M. Shatilina, V.A. Emshanova, A.P. Golubev, 2017, published in Sibirskii Ekologicheskii Zhurnal, 2017, No. 2, pp. 184–192.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khomich, A.S., Axenov-Gribanov, D.V., Bodilovskaya, O.A. et al. Assessment of the joint effect of thermal stress, pollution, and parasitic infestation on the activity of antioxidative enzymes in pulmonate mollusk Lymnaea stagnalis . Contemp. Probl. Ecol. 10, 157–163 (2017). https://doi.org/10.1134/S1995425517020068

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1995425517020068

Keywords

Search

Navigation