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Combined action of the entomopathogenic fungus Metarhizium robertsii and avermectins on the larvae of the colorado potato beetle Leptinotarsa decemlineata (Say) (Coleoptera, Chrysomelidae)

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Abstract

Synergy between the entomopathogenic fungus Metarhizium robertsii J.F. Bisch., S.A. Rehner et Humber and a complex of natural avermectins was observed after combined treatment of the Leptinotarsa decemlineata (Say) larvae. This effect was also recorded at the larval stage most resistant to fungi (5 days after molting to the IV instar). Intoxication with avermectins led to a 2.7-fold decrease in food consumption and arrest of larval development. Synergy between the fungus and avermectins was revealed in field experiments conducted in the steppe zone of Western Siberia under strong fluctuations of temperature and humidity. In particular, the median lethal time (LT50) decreased 2.8-fold after combined treatment as compared to treatment with M. robertsii alone. The mechanisms of synergy and the prospects of using the combined treatment for Colorado potato beetle control are discussed.

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References

  1. Anderson, T.E., Hajek, A.E., Roberts, D.W., Preisler, H.K., and Robertson, J.L., “Colorado Potato Beetle (Coleoptera: Chrysomelidae): Effects of Combinations of Beauveria bassiana with Insecticides,” Journal of Economic Entomology 82 (1), 83–89 (1989).

    Article  CAS  Google Scholar 

  2. Asi, M.R., Bioefficacy of Entomopathogenic Fungi and Their Combinations with Selective Insecticides against Spodoptera litura F. (Lepidoptera: Noctuidae) on Cotton. PhD Thesis (University of Agriculture, Faisalabad, 2012).

    Google Scholar 

  3. Barcic, J.I., Bazok, R., Bezjak, S., Culjak, T.G., and Barcic, J., “Combinations of Several Insecticides Used for Integrated Control of Colorado Potato Beetle (Leptinotarsa decemlineata Say, Coleoptera: Chrysomelidae),” Journal of Pest Science 79 (4), 223–232 (2006).

    Article  Google Scholar 

  4. Bloomquist, J.R., “Ion Channels as Targets for Insecticides,” Annual Review of Entomology 41, 63–190 (1996).

    Article  Google Scholar 

  5. Boomsma, J.J., Jensen, A.B., Meyling, N.V., and Eilenberg, J., “Evolutionary Interaction Networks of Insect Pathogenic Fungi,” Annual Review of Entomology 59, 467–485 (2014).

    Article  CAS  PubMed  Google Scholar 

  6. Burg, R.W., Miller, B.M., Baker, E.E., Birnbaum, J., Currie, S.A., Hartman, R., Kong, Y.L., Monaghan, R.L., Olson, G., Putter, I., Tunac, J.B., Wallick, H., Stapley, E.O., Oiwa, R., and Omura, S., “Avermectins, New Family of Potent Anthelmintic Agents: Producing Organism and Fermentation,” Antimicrobial Agents and Chemotherapy 15 (3), 361–367 (1979).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Butt, T.M., Coates, C.J., Dubovskiy, I.M., and Ratcliffe, N.A., “Entomopathogenic Fungi: New Insights into Host–Pathogen Interactions,” Advances in Genetics 94, 307–364 (2016).

    CAS  PubMed  Google Scholar 

  8. Charnley, A.K. and Collins, S.A., “Entomopathogenic Fungi and Their Role in Pest Control,” in Environmental and Microbial Relationships. The Mycota. Vol. 4, Ed. by C.P. Kubicek and I.S. Druzhinina (Springer, Berlin, 2007), pp. 159–187.

    Google Scholar 

  9. Charnley, A.K., “Fungal Pathogens of Insects: Cuticle Degrading Enzymes and Toxins,” Advances in Botanical Research 40, 241–321 (2003).

    Article  CAS  Google Scholar 

  10. De Block, M. and Stoks, R., “Short-Term Larval Food Stress and Associated Compensatory Growth Reduce Adult Immune Function in a Damselfly,” Ecological Entomology 33 (6), 796–801 (2008).

    Google Scholar 

  11. Drinyaev, V.A., Kruglyak, E.B., Mosin, V.A., Ter-Simonyan, V.G., Novik, T.S., Rusakov, S.V., Berezina, N.S., Berezkina, N.E., and Sterlina, T.S., “Aversectin C: Its Physiochemical and Biological Properties,” Prikladnaya Biokhimiya i Mikrobiologiya 35 (2), 199–205 (1999).

    CAS  Google Scholar 

  12. Dubovskiy, I.M., Kryukov, V.Yu., Benkovskaya, G.V., Yaroslavtseva, O.N., Surina, E.V., and Glupov, V.V., “Activity of Detoxificative Enzyme System and Encapsulation Rate in Colorado Potato Beetle Leptinotarsa decemlineata Larvae under Organophosphorus Insecticide Treatment and Entomopathogenic Fungus Metarhizium anisopliae Infection,” Euroasian Entomological Journal 4, 577–582 (2010).

    Google Scholar 

  13. Etter, A., Cully, D.F., Liu, K.K., Reiss, B., Vassilatis, D.K., Schaeffer, J.M., and Arena, J.P., “Picrotoxin Blockade of Invertebrate Glutamate-Gated Chloride Channels: Subunit Dependence and Evidence for Binding within the Pore,” Journal of Neurochemistry 72 (1), 318–326 (1999).

    CAS  PubMed  Google Scholar 

  14. Forrester, S.G., Hamdan, F.F., Prichard, R.K., and Beech, R.N., “Cloning, Sequencing, and Developmental Expression Levels of a Novel Glutamate-Gated Chloride Channel Homologue in the Parasitic Nematode, Haemonchus contortus,” Biochemical and Biophysical Research Communications 254 (3), 529–534 (1999).

    Article  CAS  PubMed  Google Scholar 

  15. Furlong, M.J. and Groden, E., “Evaluation of Synergistic Interactions between the Colorado Potato Beetle (Coleoptera: Chrysomelidae) Pathogen Beauveria bassiana and the Insecticides Imidacloprid and Cyromazine,” Journal of Economic Entomology 94 (2), 344–356 (2001).

    Article  CAS  PubMed  Google Scholar 

  16. Furlong, M.J. and Groden, E., “Starvation Induced Stress and the Susceptibility of the Colorado Potato Beetle, Leptinotarsa decemlineata, to Infection by Beauveria bassiana,” Journal of Invertebrate Pathology 83 (2), 127–138 (2003).

    Article  PubMed  Google Scholar 

  17. James, R.R. and Xu, J., “Mechanisms by Which Pesticides Affect Insect Immunity,” Journal of Invertebrate Pathology 109 (2), 175–182 (2012).

    Article  CAS  PubMed  Google Scholar 

  18. Kokoz, Yu.M., Tsyganova, V.G., Korystova, A.F., Grichenko, A.S., Zenchenko, K.I., Drinyaev, V.A., Mosin, V.A., Kruglyak, E.B., Sterlina, T.S., and Victorov, A.V., “Selective Cytostatic and Neurotoxic Effects of Avermectins and Activation of the GABAalpha Receptors,” Bioscience Reports 19 (6), 535–546 (1999).

    Article  CAS  PubMed  Google Scholar 

  19. Kryukov, V.Yu., Doctoral Dissertation in Biology (Novosibirsk, 2015).

  20. Kryukov, V.Yu., Khodyrev, V.P., Yaroslavtseva, O.N., Kamenova, A.S., Duisembekov, B.A., and Glupov, V.V. “Synergistic Action of Entomopathogenic Hyphomycetes and the Bacteria Bacillus thuringiensis ssp. morrisoni in the Infection of Colorado Potato Beetle Leptinotarsa decemlineata,” Applied Biochemistry and Microbiology 45 (5), 511–516 (2009).

    Article  CAS  Google Scholar 

  21. Kryukov, V.Yu., Luzina, O.A., Yaroslavtseva, O.N., Polovinka, M.P., Salakhutdinov, N.F., and Glupov, V.V., “Screening of Usnic Acid Modificates as Potential Synergists of the Entomopathogenic Fungus Beauveria bassiana, for the Colorado Potato Beetle Control,” Agrokhimiya, No. 2, 59–66 (2012).

    Google Scholar 

  22. Kryukov, V.Yu., Martemyanov, V.V., Polovinka, M.P., Luzina, O.A., Dubovskiy, I.M., Serebrov, V.V., Khodyrev, V.P., Malyarchuk, A.A., Gerber, O.N., Yaroslavtseva, O.N., Boyarishcheva, E.A., Levchenko, M.V., Glupov, V.V., Salakhutdinov, N.F., and Tolstikov, G.A., “Usnic Acid: Promising Synergist for Biopesticide Containing Entomopathogenic Microorganisms,” Doklady Biological Sciences 423 (2), 279–282 (2008).

    Google Scholar 

  23. Kryukov, V.Yu., Yaroslavtseva, O.N., Dubovskiy, I.M., Tyurin, M.V., Kryukova, N.A., and Glupov, V.V., “Insecticidal and Immunosuppressive Effect of Ascomycete Cordyceps militaris on the Larvae of the Colorado Potato Beetle Leptinotarsa decemlineata,” Biology Bulletin 41 (3), 276–283 (2014).

    Article  CAS  Google Scholar 

  24. Kryukov, V.Yu., Yaroslavtseva, O.N., Elisaphenko, E.A., Mitkovets, P.V., Lednev, G.R., Duisembekov, B.A., Zakian, S.M., and Glupov, V.V., “Change in the Temperature Preferences of Beauveria bassiana sensu lato Isolates in the Latitude Gradient of Siberia and Kazakhstan,” Microbiology 81 (4), 453–459 (2012).

    Article  CAS  Google Scholar 

  25. Lacey, L.A., Grzywacz, D., Shapiro-Ilan, D.I., Frutos, R., Brownbridge, M., and Goettel, M.S., “Insect Pathogens as Biological Control Agents: Back to the Future,” Journal of Invertebrate Pathology 132, 1–41 (2015).

    Article  CAS  PubMed  Google Scholar 

  26. Lee, K.P., Cory, J.S., Wilson, K., Raubenheimer, D., and Simpson, S.J., “Flexible Diet Choice Offsets Protein Costs of Pathogen Resistance in a Caterpillar,” Proceedings of the Royal Society B, Biological Sciences 273, 823–829 (2006).

    Article  CAS  PubMed  Google Scholar 

  27. Mosin, V.A., Kruglyak, E.B., Sterlina, T.S., Korystov, Yu.N., Shaposhnikova, V.V., Narimanov, A.A., Kublik, L.N., Levitman, M.Kh., Victorov, A.V., and Drinyaev, V.A., “Cytostatic and Cytotoxic Action of Avermectins on Tumor Cells in vitro,” Antibiotiki i Khimioterapii, No. 10, 10–14 (2000).

    Google Scholar 

  28. Polovinka, M.P., Salakhutdinov, N.F., Luzina, O.A., Kryukov, V.Yu., Yaroslavtseva, O.N., Khodyrev, V.P., and Glupov, V.V., A Synergist Increasing the Efficacy of Biopreparations for the Colorado Potato Beetle Control. Application 2010152851/04. Priority 23.12.2010. Patent RU2448464. Bulletin No. 12, 27.04.2012 (2012).

  29. Putter, I., MacConnell, J.G., Preiser, F.A., Haidri, A.A., Ristich, S.S., and Dybas, R.A., “Avermectins: Novel Insecticides, Acaricides and Nematocides from a Soil Microorganism,” Experientia 37, 963–964 (1981).

    Article  CAS  Google Scholar 

  30. Quintela, E.D. and McCoy, C.W., “Synergistic Effect of Imadacloprid and Two Entomopathogenic Fungi on the Behavior and Survival of Larvae of Diaprepes abbreviatus (Coleoptera: Curculionidae) in Soil,” Journal of Economic Entomology 91, 110–122 (1998).

    Article  CAS  Google Scholar 

  31. Roditakis, E., Couzin, I.D., Balrow, N.R., Franks, N.R., and Charnley, A.K., “Improving Secondary Pick Up of Insect Fungal Pathogen Conidia by Manipulating Host Behavior,” Annals of Applied Biology 137, 329–335 (2000).

    Article  Google Scholar 

  32. Shternshis, M. and Tsvetkova, V., “Comparison of Some Preparations for the Control of Siberian Population of Colorado Beetle,” Information Bulletin of the EPRS IOBC 37, 21–24 (2007).

    Google Scholar 

  33. Tomilova, O.G., Kryukov, V.Yu., Duisembekov, B.A., Yaroslavtseva, O.N., Tyurin, M.V., Kryukova, N.A., Skorokhodov, V., Dubovskiy, I.M., and Glupov, V.V., “Immune-Physiological Aspects of Synergy between Avermectins and the Entomopathogenic Fungus Metarhizium robertsii in Colorado Potato Beetle Larvae,” Journal of Invertebrate Pathology 140, 8–15 (2016).

    Article  CAS  PubMed  Google Scholar 

  34. Tounou, A.-K., Kooyman, C., Douro-Kpindou, O.-K., and Poehling, H.M., “Interaction between Paranosema locustae and Metarhizium anisopliae var. acridum, Two Pathogens of the Desert Locust, Schistocerca gregaria under Laboratory Conditions,” Journal of Invertebrate Pathology 97 (3), 203–210 (2008).

    Article  PubMed  Google Scholar 

  35. Wraight, S.P. and Ramos, M.E., “Synergistic Interaction between Beauveria bassiana- and Bacillus thuringiensis tenebrionis-Based Biopesticides Applied against Field Populations of Colorado Potato Beetle Larvae,” Journal of Invertebrate Pathology 90 (3), 139–150 (2005).

    Article  CAS  PubMed  Google Scholar 

  36. Wraight, S.P., Inglis, G.D., and Goettel, M.S., “Fungi,” in Field Manual of Techniques in Invertebrate Pathology: Application and Evaluation of Pathogens for Control of Insects and Other Invertebrate Pests, Ed. by L.A. Lacey and H.K. Kaya (Springer, Dordrecht, 2007a), pp. 223–248.

    Chapter  Google Scholar 

  37. Wraight, S.P., Sporleder, M., Poprawski, T.J., and Lacey, A.L., “Application and Evaluation of Entomopathogens in Potato,” in Field Manual of Techniques in Invertebrate Pathology: Application and Evaluation of Pathogens for Control of Insects and Other Invertebrate Pests, Ed. by L.A. Lacey and H.K. Kaya (Springer, Dordrecht, 2007b), pp. 329–359.

    Chapter  Google Scholar 

  38. Xu, G. and Long, G.E., “Feeding and Performance of Colorado Potato Beetle, Leptinotarsa decemlineata Reared on Nightshade and Potato,” Journal of the Entomological Society of British Columbia 92, 73–79 (1995).

    Google Scholar 

  39. Yaroslavtseva, O.N., Dubovskiy, I.M., Khodyrev, V.P., Duisembekov, B.A., Kryukov, V.Yu., and Glupov, V.V., “Immunological Mechanisms of Synergy between Fungus Metarhizium robertsii and Bacteria Bacillus thuringiensis ssp. morrisoni on Colorado Potato Beetle Larvae,” Journal of Insect Physiology 96, 14–20 (2017).

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Yu. B. Akhanaev.

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Original Russian Text © Yu.B. Akhanaev, O.G. Tomilova, O.N. Yaroslavtseva, B.A. Duisembekov, V.Yu. Kryukov, V.V. Glupov, 2016, published in Entomologicheskoe Obozrenie, 2017, Vol. 96, No. 1, pp. 25–35.

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Akhanaev, Y.B., Tomilova, O.G., Yaroslavtseva, O.N. et al. Combined action of the entomopathogenic fungus Metarhizium robertsii and avermectins on the larvae of the colorado potato beetle Leptinotarsa decemlineata (Say) (Coleoptera, Chrysomelidae). Entmol. Rev. 97, 158–165 (2017). https://doi.org/10.1134/S0013873817020026

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