Skip to main content
SpringerLink
Log in

Effects of the Entomopathogenic Fungi, Beauveria bassiana and Metarhizium robertsii, on the Physiological and Behavioral Traits of the Northern Red-Backed Vole (Myodes rutilus, Rodentia, Cricetidae) under Stressful Conditions

  • Published:
Biology Bulletin Aims and scope Submit manuscript

Abstract

An experiment aimed at revealing the consequences of adding two species of entomopathogenic Ascomycetes, Beauveria bassiana and Metarhizium robertsii, to grain fodder showed that northern red-backed voles that received M. robertsii conidia in their food for 15 days had higher levels of triglycerides, glucose, and peroxidase in the blood; differed from other animals in social behavior patterns; and demonstrated significantly less emotionality in an open field test than control animals. The voles fed fungal conidia showed a trend towards reduced survival in captivity compared to controls. These data indicate the significant impact of entomopathogenic fungi on the metabolism, behavior, and lifespan of nontarget mammals.

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

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

REFERENCES

  1. Andreeva, V.A., Ferment peroksidaza (Enzyme Peroxidase), Moscow: Nauka, 1988.

  2. Baas, J. and Kooijman, S.A., Sensitivity of animals to chemical compounds links to metabolic rate, Ecotoxicology, 2015, vol. 24, no. 3, pp. 657–663.

    Article  CAS  Google Scholar 

  3. Bamisile, B.S., Dash, C.K., Akutse, K.S., Keppanan, R., Afolabi, O.G., Hussain, M., et al., Prospects of endophytic fungal entomopathogens as biocontrol and plant growth promoting agents: an insight on how artificial inoculation methods affect endophytic colonization of host plants, Microbiol. Res., 2018, vol. 217, pp. 34–50. https://doi.org/10.1016/j.micres.2018.08.016

    Article  Google Scholar 

  4. Bezel’, V.S., Bol’shakov, V.N., and Vorobeichik, E.L., Populyatsionnaya ekotoksikologiya (Population Ecotoxicology), Moscow: Nauka, 1994.

  5. Birke, L., Some behavioral changes associated with guinea pig oestrus cycle, Zeitschrift Tierpsychologie, 1981, vol. 55, pp. 79–89.

    Article  CAS  Google Scholar 

  6. Brunner-Mendoza, C., Reyes-Montes, M.D.R., Moonjely, S., Bidochka, M.J., and Toriello, C., A review on the genus Metarhizium as an entomopathogenic microbial biocontrol agent with emphasis on its use and utility in Mexico, Biocontrol Sci. Technol., 2019, vol. 29, no. 1, pp. 83–102.

    Article  Google Scholar 

  7. Calow, P., Proximate and ultimate responses to stress in biological systems, Biol. J. Linn. Soc., 1989, vol. 37, nos. 1–2, pp. 173–181. https://doi.org/10.1111/j.1095-8312.1989.tb02101.x

    Article  Google Scholar 

  8. Chigrinskii, E.A., Gerunova, L.K., Konvai, V.D., and Gerunov, T.V., Biochemical markers of cypermethrin toxicity for forest voles Myodes, in Problemy i monitoring prirodnykh ekosistem (Problems and Monitoring of Natural Ecosystems), 2018, pp. 155–159.

    Google Scholar 

  9. Clifton, E.H., Jaronski, S.T., Hodgson, E.W., and Gassmann, A.J., Abundance of soil-borne entomopathogenic fungi in organic and conventional fields in the midwestern USA with an emphasis on the effect of herbicides and fungicides on fungal persistence, PLoS One, 2015, vol. 10, no. 7, art. ID e0133613. https://doi.org/10.1371

  10. Colborn, T., Pesticides-how research has succeeded and failed to translate science into policy: endocrinological effects on wildlife, Environ. Health Perspect., 1995, vol. 103, suppl. 6, pp. 81–85.

    Google Scholar 

  11. Drugan, R.C., Basile, A.S., Ha, J.H., Healy, D., and Ferland, R.J., Analysis of the importance of controllable versus uncontrollable stress on subsequent behavioral and physiological functioning, Brain Res. Protoc., 1997, vol. 2, pp. 69–74.

    Article  CAS  Google Scholar 

  12. De Faria, M.R. and Wraight, F.R., Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types, Biol. Control, 2007, vol. 43, pp. 237–256. https://doi.org/10.1016/j.biocontrol.2007.08.001

    Article  CAS  Google Scholar 

  13. García-Herranz, V., Valdehita, A., Navas, J.M., and Fernandez-Cruz, M.L., Cytotoxicity against fish and mammalian cell lines and endocrine activity of the mycotoxins beauvericin, deoxynivalenol and ochratoxin-A, Food Chem. Toxicol., 2019, vol. 127, pp. 288–297.

    Article  Google Scholar 

  14. Golo, P.S., Gardner, D.R., Grilley, M.M., Takemoto, J.Y., Krasnoff, S.B., Pires, M.S., et al., Production of destruxins from Metarhizium spp. fungi in artificial medium and in endophytically colonized cowpea plants, PLoS One, 2014, vol. 9, no. 8. https://doi.org/10.1371/journal.pone.0104946

  15. Gosudarstvennyi katalog pestitsidov i agrokhimikatov, razreshennykh k primeneniyu na territorii Rossiiskoi Federatsii na 8 fevralya 2021. Ch. I. Pestitsidy (State Catalog of Pesticides and Agrochemicals Permitted for Use on the Territory of the Russian Federation as of February 8, 2021. Part I. Pesticides), Moscow: Minsel’khoz Rossii, 2021.

  16. Hall, C.S., Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality, J. Comp. Psychol., 1934, vol. 18, pp. 385–403.

    Article  Google Scholar 

  17. Hall, CS., The relationship between emotionality and ambulatory activity, J. Comp. Psychol., 1936, vol. 22, pp. 345–452.

    Article  Google Scholar 

  18. Ignoffo, C.M., Effects of entomopathogens on vertebrates, Ann. N.Y. Acad. Sci., 1973, vol. 217, no. 1, pp. 141–164.

    Article  CAS  Google Scholar 

  19. Jaronski, S.T., Ecological factors in the inundative use of fungal entomopathogens, BioControl, 2010, vol. 55, pp. 159–185. https://doi.org/10.1007/s10526-009-9248-3

    Article  Google Scholar 

  20. Kershaw, M.J., Moorhouse, E.R., Bateman, R., Reynolds, S.E., and Charnley, A.K., The role of destruxins in the pathogenicity of Metarhizium anisopliae for three species of insect, J. Invertebr. Pathol., 1999, vol. 74, no. 3, pp. 213–223.

    Article  CAS  Google Scholar 

  21. Mancebo, A., González, F., Aldana, L., González, Y., Lugo, S., González, B., et al., Pathogenicity of the entomopathogenic fungus Beauveria bassiana 9205 in rats using different routes of exposition, Toxicol. Environ. Chem., 2009, vol. 91, no. 1, pp. 99–108.

    Article  CAS  Google Scholar 

  22. Mikhailenko, V.G., Ambiguous resistance of organisms, Usp. Sovrem. Biol., 2002, vol. 122, no. 4, pp. 334–341.

    Google Scholar 

  23. Moonjely, S., Barelli, L., and Bidochka, M.J., Insect pathogenic fungi as endophytes, Adv. Genet., 2016, vol. 94, pp. 107–135. doi.org/https://doi.org/10.1016/bs.adgen.2015.12.004

    Article  CAS  Google Scholar 

  24. Novikov, E.A., Kondratuk, E.Yu., and Polikarpov, I.A., Age-related differences in physiology and survival of northern red-backed voles (Myodes rutilus) in captivity, Biogerontology, 2019. https://doi.org/10.1007/s10522-019-09847-w

  25. Novikov, E.A., Population dynamics and spatial distribution of red-backed voles in the Teletskaya taiga, Ekologiya, 1995, no. 3, pp. 40–46.

  26. Novikov, E.A., Panov, V.V., and Moshkin, M.P., Density-dependent mechanisms of regulation of northern red-backed vole (Myodes rutilus) populations in optimal and suboptimal habitats in the south of Western Siberia, Zh. Obshch. Biol., 2012, vol. 73, no. 1, pp. 63–72.

    Google Scholar 

  27. Olenev, G.V., Alternative types of ontogeny in cyclomorphic rodents and their role in population dynamics: an ecological analysis, Russ. J. Ecol., 2002, vol. 33, no. 5, pp. 321–330.

    Article  Google Scholar 

  28. Panov, V.V., Winter period in the life of small mammals in the Ob pine forests of the northern forest-steppe of Western Siberia, Sib. Ekol. Zh., 2001, vol. 8, no. 6, pp. 777–784.

    Google Scholar 

  29. Polikarpov, I.A., Kondratyuk, E.Yu., Petrovskii, D.V., and Novikov, E.A., Interpopulation variability of the endocrine-metabolic response to cold stress in the northern red-backed vole (Myodes rutilus), Zh. Obshch. Biol., 2016, vol. 77, no. 4, pp. 284–292.

    CAS  Google Scholar 

  30. Prut, L. and Belzung, C., The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review, Eur. J. Pharmacol., 2003, vol. 4, no. 63, pp. 3–33.

    Article  Google Scholar 

  31. Ríos-Moreno, A., Garrido-Jurado, I., Raya-Ortega, M.C., and Quesada-Moraga, E., Qantification of fungal growth and destruxin a during infection of Galleria mellonella larvae by Metarhizium brunneum, J. Invertebr. Pathol., 2017, vol. 149, pp. 29–35.

    Article  Google Scholar 

  32. Royce, J.R., Pauley, W., and Iedall, L.T., Genetic-behavioral analysis of emotionality in mice. Factor analysis, in Aktual’nye problemy genetiki povedeniya (Actual Problems of Genetics of Behavior), Leningrad: Nauka, Leningr. Otd., 1975.

  33. Saunders, B., Peroxidases and catalases, in Neorganicheskaya biokhimiya (Inorganic Biochemistry), Moscow: Mir, 1978, vol. 2, pp. 434–470.

  34. Scheepmaker, J.W.A. and Butt, T.M., Natural and released inoculum levels of entomopathogenic fungal biocontrol agents in soil in relation to risk assessment and in accordance with eu regulations, Biocontrol Sci. Technol., 2010, vol. 20, no. 5, pp. 503–552. https://doi.org/10.1080/09583150903545035

    Article  Google Scholar 

  35. Senthilraja, G., Anand, T., Kennedy, J.S., Raguchander, T., and Samiyappan, R., Plant growth promoting rhizobacteria (PGPR) and entomopathogenic fungus bioformulation enhance the expression of defense enzymes and pathogenesis-related proteins in groundnut plants against leafminer insect and collar rot pathogen, Physiol. Mol. Plant Pathol., 2013, vol. 82, pp. 10–19.

    Article  CAS  Google Scholar 

  36. Shilov, I.A., Praktikum po ekologii nazemnykh pozvonochnykh zhivotnykh (A Practical Course in the Ecology of Terrestrial Vertebrates), Moscow: Vysshaya Shkola, 1961.

  37. Shilova, S.A., Populyatsionnaya ekologiya kak osnova kontrolya chislennosti melkikh mlekopitayushchikh (Population Ecology as a Basis for the Control of the Number of Small Mammals), Moscow: Nauka, 1993.

  38. Skrobek, A., Shah, F.A., and Butt, T.M., Destruxin production by the entomogenous fungus Metarhizium anisopliae in insects and factors influencing their degradation, BioControl, 2008, vol. 53, no. 2, pp. 361–373.

    Article  CAS  Google Scholar 

  39. Van Straalen, N.M., Ecotoxicology becomes stress ecology, Environ. Sci. Technol., 2003, pp. 324A–330A. https://doi.org/10.1021/es0325720

  40. Strasser, H., Vey, A., and Butt, T.M., Are there any risks in using entomopathogenic fungi for pest control, with particular reference to the bioactive metabolites of Metarhizium, Tolypocladium and Beauveria species?, Biocontrol Sci. Technol., 2000, vol. 10, pp. 717–735.

    Article  Google Scholar 

  41. Tarakhtii, E.A. and Mukhacheva, S.V., Response of the blood system of forest voles to stress against the background of chronic chemical pollution of the environment, Usp. Sovrem. Biol., 2011, vol. 131, no. 6, pp. 613–621.

    CAS  Google Scholar 

  42. Tête, N., Afonso, E., Bouguerra, G., and Scheifler, R., Blood parameters as biomarkers of cadmium and lead exposure and effects in wild wood mice (Apodemus sylvaticus) living along a pollution gradient, Chemosphere, 2015, vol. 138, pp. 940–946.

    Article  Google Scholar 

  43. Tomilova, O.G., Yaroslavtseva, O.N., Ganina, M.D., Tyurin, M.V., Chernyak, E.I., Senderskiy, I.V., et al., Changes in antifungal defence systems during the intermoult period in the Colorado potato beetle, J. Insect Physiol., 2019, vol. 116, pp. 106–117. https://doi.org/10.1016/j.jinsphys.2019.05.003

    Article  CAS  Google Scholar 

  44. Tomilova, O.G., Shaldyaeva, E.M., Kryukova, N.A., Pilipova, Y.V., Schmidt, N.S., Danilov, V.P., Krukov, V.Y., and Glupov, V.V., Entomopathogenic fungi decrease Rhizoctonia disease in potato in field conditions, PeerJ, 2020, vol. 8, art. ID e9895. https://doi.org/10.7717/peerj.9895

    Article  Google Scholar 

  45. Vega, F.E., The use of fungal entomopathogens as endophytes in biological control: a review, Mycologia, 2018, vol. 110, no. 1, pp. 4–30. https://doi.org/10.1080/00275514.2017.1418578

    Article  Google Scholar 

  46. Vey, A., Hoagland, R.E., and Butt, T.M., Toxic metabolites of fungal biocontrol agents, Fungi as Biocontrol Agents, 2001, pp. 311–346.

    Book  Google Scholar 

  47. Vos, J.G. and Moore, J.A., Immune suppression as related to toxicology, CRC Crit. Rev. Toxicol., 1977, vol. 5, no. 1, pp. 67–101.

    Article  CAS  Google Scholar 

  48. Wei, G., Lai, Y., Wang, G., Chen, H., Li, F., and Wang, S., Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality, Proc. Natl. Acad. Sci. U. S. A., 2017, vol. 114, no. 23, pp. 5994–5999. https://doi.org/10.1073/pnas.1703546114

  49. Xiao, G., Ying, S.H., Zheng, P., Wang, Z.L., Zhang, S., Xie, X.Q., et al., Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana, Sci. Rep., 2012, vol. 2, p. 483. https://doi.org/10.1038/srep00483

    Article  CAS  Google Scholar 

  50. Zhivotovskii, L.A., Populyatsionnaya biometriya (Population Biometrics), Moscow: Nauka, 1991.

  51. Zimmermann, G., Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii, Biocontrol Sci. Technol., 2007, vol. 17, no. 6, pp. 553–596. https://doi.org/10.1080/09583150701309006

    Article  Google Scholar 

  52. Zimmermann, G., Review on safety of the entomopathogenic fungus Metarhizium anisopliae, Biocontrol Sci. Technol., 2007a, vol. 17, no. 9, pp. 879–920. https://doi.org/10.1080/09583150701593963

    Article  Google Scholar 

  53. Zollitsch, W., Raffaseder, C., Bohm, J., Wagner, E., and Leitgeb, R., Impact of the mycotoxins moniliformin and beauvericin on growth and carcass traits of broilers, Wiener Tierarztliche Monatsschrift, 2003, no. 9, pp. 238–243.

Download references

ACKNOWLEDGMENTS

We thank I.A. Polikarpov and A.A. Khalin for help in measuring the basal metabolic rate and M.V. Tyurin and T.M. Marchenko for help in fungal cultivation.

Funding

This work was carried out within the framework of the Federal Program for Fundamental Scientific Research for 2013–2020, project VI.51.1.8. State registration number АААА-А16-116121410118-7 with partial financial support from the Russian Foundation for Basic Research (project no. 19-04-00929).

Author information

Authors and Affiliations

  1. Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences, 630091, Novosibirsk, Russia

    E. A. Novikov, P. A. Zadubrovskiy, E. Yu. Kondratyuk, V. Yu. Kryukov, E. V. Novikova & V. V. Glupov

  2. Novosibirsk State Agrarian University, 630036, Novosibirsk, Russia

    E. A. Novikov

Authors
  1. E. A. Novikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. A. Zadubrovskiy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. Yu. Kondratyuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. V. Yu. Kryukov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. V. Novikova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. V. Glupov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. A. Novikov.

Ethics declarations

Conflict of interest. The authors declare that they have no conflicts of interest.

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Novikov, E.A., Zadubrovskiy, P.A., Kondratyuk, E.Y. et al. Effects of the Entomopathogenic Fungi, Beauveria bassiana and Metarhizium robertsii, on the Physiological and Behavioral Traits of the Northern Red-Backed Vole (Myodes rutilus, Rodentia, Cricetidae) under Stressful Conditions. Biol Bull Russ Acad Sci 49, 924–932 (2022). https://doi.org/10.1134/S1062359022070123

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062359022070123

Keywords:

Search

Navigation