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Features of Behavioral Reactions of the Peach Aphid Myzus persicae (Sulzer, 1776) (Hemiptera, Aphididae) to Volatile Organic Compounds of Entomopathogenic Fungi of the Genus Lecanicillium

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Abstract

In evaluating the effectiveness of entomopathogenic fungi for control of the green peach aphid Myzus persicae (Sulzer, 1776), a dangerous pest and a virus vector, it is necessary to consider the effects of fungal spores and mycelium on the behavior of aphids related to host plant selection. In laboratory experiments, 5 out of 13 strains of different species of the genus Lecanicillium caused the repellency response in aphid females, with the index of aggregation varying from −22.7 to −39.7 and the number of nymphs in the daughter generation decreasing by 1.6–4.2 times. The species of fungi varied significantly in their ability to infect aphid nymphs: Lecanicillium longisporum was the most virulent against the green peach aphid, causing 89% nymphal mortality at a concentration of 1 × 107 spores / mL, while Lecanicillium psalliotae was practically non-pathogenic to aphids. All the strains showing significant repellency also possessed pronounced pathogenicity, while the opposite was not always true.

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REFERENCES

  1. Baverstock, J., Roy, H.E., and Pell, J.K., Entomopathogenic fungi and insect behaviour: from unsuspecting hosts to targeted vectors, BioControl, 2010, vol. 55, no. 1, p. 89. https://doi.org/10.1007/s10526-009-9238-5

    Article  Google Scholar 

  2. Blackman, R.L. and Eastop, V.F., Aphids on the World’s Crops: an Identification and Information Guide. Second Edition, New York: John Wiley et Sons 2000.

  3. Bwye, A.M., Proudlove, W., Berlandier, F.A., and Jones, R.A., Effects of applying insecticides to control aphid vectors and cucumber mosaic virus in narrow-leafed lupins (Lupinus angustifolius), Aust. J. Exp. Agric., 1997, vol. 37, p. 93. https://doi.org/10.1071/EA96041

  4. Campos, V.P., De Pinho, S.C.R., and Freire, E.S., Volatiles produced by interacting microorganisms potentially useful for the control of plant pathogens, Ciênc. Agrotecnol., 2010, vol. 34, no. 3, p. 525. https://doi.org/10.1590/S1413-70542010000300001

    Article  CAS  Google Scholar 

  5. Crespo, R., Pedrini, N., Juárez, M.P., and Bello, G.M.D., Volatile organic compounds released by the entomopathogenic fungus Beauveria bassiana, Microbiol. Res., 2008, vol. 163, no. 2, p. 148. https://doi.org/10.1016/j.micres.2006.03.013

  6. Dewar, A.M., Chemical control, in Aphids as Crop Pests, van Emden, H.F. and Harrington, R., Eds., Wallingford: CAB International, 2007, p. 391. https://doi.org/10.1079/9780851998190.0000

  7. Dromph, K.M. and Vestergaard, S., Pathogenicity and attractiveness of entomopathogenic hyphomycete fungi to collembolans, Appl. Soil Ecol., 2002, vol. 21, no. 3, p. 197. https://doi.org/10.1016/S0929-1393(02)00092-6

    Article  Google Scholar 

  8. Eskandari, F., Sylvester, E.S., and Richardson, J., Evidence for lack of propagation of potato leaf roll virus in its aphid vector, Myzus persicae, Phytopathology, 1979, vol. 69, p. 45.

  9. Faria, M.R. and Wraight, S.P., Mycoinsecticides and mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types, Biol. Control, 2007, vol. 43, no. 3, p. 237. https://doi.org/10.1016/j.biocontrol.2007.08.001

    Article  CAS  Google Scholar 

  10. Foster, S.P., Denholm, I., and Thompson, R., Variation in response to neonicotinoid insecticide in peach-potato aphids, Myzus persicae (Hemiptera: Aphididae), Pest Manage. Sci., 2003, vol. 59, no. 2, p. 166. https://doi.org/10.1002/ps.570

  11. Goettel, M.S., Koike, M., Kim, J.J., Aiuchi, D., Shinya, R., and Brodeur, J., Potential of Lecanicillium spp. for management of insects, nematodes and plant diseases, J. Invertebr. Pathol., 2008, vol. 98, no. 3, p. 256. https://doi.org/10.1016/j.jip.2008.01.009

  12. Gurulingappa, P., McGee, P.A., and Sword, G., Endophytic Lecanicillium lecanii and Beauveria bassiana reduce the survival and fecundity of Aphis gossypii following contact with conidia and secondary metabolites, Crop Prot., 2011, vol. 30, no. 3, p. 349. https://doi.org/10.1016/j.cropro.2010.11.017

  13. Holighaus, G. and Rohlfs, M., Volatile and non-volatile fungal oxylipins in fungus-invertebrate interactions, Fungal Ecol., 2019, vol. 38, p. 28. https://doi.org/10.1016/J.FUNECO.2018.09.005

    Article  Google Scholar 

  14. Hussain, A.I., Anwar, F., Shahid, M., Ashraf, M., and Przybylski, R., Chemical composition, antioxidant and antimicrobial activities of essential oil of spearmint (Mentha spicata L.) from Pakistan, J. Essent. Oil Res., 2010, vol. 22, p. 78. https://doi.org/10.1080/10412905.2010.9700269

  15. Kakareka, N.N., Tolkach, V.F., Sapotsky, M.V., Volkov, Yu.G., and Shchelkanov, M.Yu., Insect vectors of viral diseases of potatoes in the Russian Far East, in Chteniya pamyati Alekseya Ivanovicha Kurentsova (A.I. Kurentsov’s Annual Memorial Meetings), Issue 30, 2019, p. 191. https://doi.org/10.25221/kurentzov.30.18

  16. Kepler, R.M., Luangsaard, J.J., Hywel-Jones, N.L., Quandt, C., Gi-Ho Sung, Rehner, S.A., Aime, M.C., Henkel, T.W., Sanjuan, T., Zare, R., Chen, M., Zhengzhi, L., Rossman, A.Y., Spatafora, J.W., and Shrestha, B., A phylogenetically-based nomenclature for Cordycipitaceae (Hypocreales), IMA Fungus, 2017, vol. 8, no. 2, p. 335. https://doi.org/10.5598/imafungus.2017.08.02.08

    Article  PubMed  PubMed Central  Google Scholar 

  17. Khoja, S., Eltayef, K.M., Baxter, I., Myrta, A., Bull, J.C., and Butt, T.M., Volatiles of the entomopathogenic fungus, Metarhizium brunneum, attract and kill plant parasitic nematodes, Biol. Control, 2021, vol. 152, art. 104472. https://doi.org/10.1016/j.biocontrol.2020.104472

  18. Kramer, R. and Abraham, W.R., Volatile sesquiterpenes from fungi: What are they good for? Phytochem. Rev., 2012, vol. 11, p. 15. https://doi.org/10.1007/s11101-011-9216-2

    Article  CAS  Google Scholar 

  19. Lednev, G.R., Levchenko, M.V., and Kazartsev, I.A., Entomopathogenic fungi in the bark beetle populations of Karelia: their species composition and virulence, in Materialy Vtoroi Vserossiiskoi konferentsii s mezhdunarodnym uchastiem “Monitoring i biologicheskie metody kontrolya vreditelei i patogenov drevesnykh rastenii: ot teorii k praktike” (Monitoring and Biological Control Methods against Pests and Pathogens of Woody Plants: from Theory to Practice. Proc. of the 2nd All-Russian Conf.), Krasnoyarsk: Inst. Lesa, 2019, p. 107.

  20. Lord, J.C., Desiccant dusts synergize the effect of Beauveria bassiana (Hyphomycetes: Moniliales) on stored-grain beetles, J. Econ. Entomol., 2001, vol. 94, no. 2, p. 367. https://doi.org/10.1603/0022-0493-94.2.367

  21. Lozano-Soria, A., Picciotti, U., Lopez-Moya, F., Lopez-Cepero, J., Porcelli, F., and Lopez-Llorca, L.V., Volatile organic compounds from entomopathogenic and nematophagous fungi, repel banana black weevil (Cosmopolites sordidus), Insects, 2020, vol. 11, no. 8, p. 509. https://doi.org/10.3390/insects11080509

  22. Manoussopoulos, Y., Mantzoukas, S., Lagogiannis, I., Goudoudaki, S., and Kambouris, M., Effects of three strawberry entomopathogenic fungi on the prefeeding behavior of the aphid Myzus persicae, J. Insect Behav., 2019, vol. 32, p. 99. https://doi.org/10.1007/s10905-019-09709-w

  23. Maslyakov, V.Yu. and Izhevsky, S.S., Invazii rastitel’noyadnykh nasekomykh v evropeiskuyu chast’ Rossii (Invasions of Herbivorous Insects in European Russia), Moscow: Inst. Geogr., 2011.

  24. Mburu, D.M., Ndung’u, M.W., Maniania, N.K., and Hassanali, A., Comparison of volatile blends and gene sequences of two isolates of Metarhizium anisopliae of different virulence and repellency toward the termite Macrotermes michaelseni, J. Exp. Biol., 2011, vol. 214, p. 956. https://doi.org/10.1242/jeb.050419

  25. Mburu, D.M., Maniania, N.K., and Hassanali, A., Comparison of volatile blends and nucleotide sequences of two Beauveria bassiana isolates of different virulence and repellency towards the termite Macrotermes michaelseni, J. Chem. Ecol., 2013, vol. 39, p. 101. https://doi.org/10.1007/s10886-012-0207-6

  26. Mitina, G., Kazartsev, I., Vasileva, A., and Yli-Mattila, T., Multilocus genotyping based species identification of entomopathogenic fungi of the genus Lecanicillium (= Verticillium lecanii s. l.), J. Basic Microbiol., 2017, vol. 57, no. 11, p. 950. https://doi.org/10.1002/jobm.201700092

  27. Mitina, G.V., Stepanycheva, E.A., and Petrova, M.O., The effects of volatile compounds of mycelium and extracts of entomopathogenic fungi on the behavioral response and viability of the western flower thrips Frankliniella occidentalis (Pergande), Parazitologiya, 2019, vol. 53, no. 3, p. 230. https://doi.org/10.1134/S0031184719030050

  28. Mitina, G.V., Selitskaya, O.G., and Schenikova, A.V., Effect of volatile compounds of the entomopathogenic fungi Beauveria bassiana (Bals.-Criv.) Vuill. and Lecanicillium muscarium R. Zare et W. Gams on the behavior of Sitophilus granarius (L.) (Coleoptera, Dryophthoridae) and evaluation of the virulence of different strains of these fungi, Entomol. Rev., 2020, vol. 100, no. 4, p. 456. https://doi.org/10.1134/S001387382004003X

  29. Morath, S.U., Hung, R., and Bennett, J.W., Fungal volatile organic compounds: A review with emphasis on their biotechnological potential, Fungal Biol. Rev., 2012, vol. 26, p. 73. https://doi.org/10.1016/j.fbr.2012.07.001

    Article  Google Scholar 

  30. Müller, A., Faubert, P., Hagen, M., Castell, W., Polle, A., Schnitzler, J.P., and Rosenkranz, M., Volatile profiles of fungi—chemotyping of species and ecological functions, Fungal Gen. Biol., 2013, vol. 54, p. 25. https://doi.org/10.1016/j.fgb.2013.02.005

    Article  CAS  Google Scholar 

  31. Namba, R. and Sylvester, E.S., Transmission of cauliflower mosaic virus by the green peach, turnip, cabbage, and pea aphids, J. Econ. Entomol., 1981, vol. 74, no. 5, p. 546. https://doi.org/10.1093/jee/74.5.546

    Article  Google Scholar 

  32. Ortiz-Urquiza, A. and Keyhani, N.O., Action on the surface: entomopathogenic fungi versus the insect cuticle, Insects, 2013, vol. 4, no. 3, p. 357. https://doi.org/10.3390/insects4030357

    Article  PubMed  PubMed Central  Google Scholar 

  33. Pascual-Villalobos, M.J. and Robledo, A., Screening for antiinsect activity in Mediterranean plants, Ind. Crops Prod., 1998, vol. 8, no. 3, p. 183. https://doi.org/10.1016/S0926-6690(98)00002-8

    Article  CAS  Google Scholar 

  34. Pazyuk, I.M., Fominykh, T.S., and Medvedeva, K.D., Evaluation of the possibility of potato virus Y transmission by the predatory bug Orius majusculus Reuter (Hemiptera, Anthocoridae) and the greenbug Schizaphis graminum Rondani (Homoptera: Aphididae), Vestn. Zashch. Rast., 2017, vol. 91, no. 1, p. 26.

  35. Popov, N.A. and Belousov, Yu.V., A technique of mass rearing of predatory midges on cereal aphids, in Primenenie biologicheskikh metodov zashchity rastenii v sel’skokhozyaistvennom proizvodstve (Biological Methods of Plant Protection in Agriculture), Kishinev, 1988, p. 3.

  36. Rohlfs, M., Obmann, B.R., and Petersen, R., Competition with filamentous fungi and its implication for a gregarious lifestyle in insects living on ephemeral resources, Ecol. Entomol., 2005, vol. 30, p. 556. https://doi.org/10.1111/j.0307-6946.2005.00722.x

    Article  Google Scholar 

  37. Roy, H.E., Steinkraus, D.C., Eilenberg, J., Hajek, A.E., and Pell, J.K., Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts, Annu. Rev. Entomol., 2006, vol. 51, p. 331. https://doi.org/10.1146/annurev.ento.51.110104.150941

    Article  CAS  PubMed  Google Scholar 

  38. Samson, R.A., Evans, H.C., and Latgé, J.-P., Atlas of Entomopathogenic Fungi, Berlin: Springer, 1988.

  39. Sinha, K.K., Choudhary, A.K., and Kumari, P., Entomopathogenic fungi, in Ecofriendly Pest Management for Food Security, San Diego: Academic Press, 2016, p. 475.

  40. Splivallo, R., Bossi, S., Maffei, M., and Bonfante, P., Discrimination of truffle fruiting body versus mycelial aromas by stir bar sorptive extraction, Phytochemistry, 2007, vol. 68, p. 2584. https://doi.org/10.1016/j.phytochem.2007.03.030

    Article  CAS  PubMed  Google Scholar 

  41. Steinkraus, D.C., Factors affecting transmission of fungal pathogens of aphids, J. Invertebr. Pathol., 2006, vol. 92, no. 3, p. 125. https://doi.org/10.1016/j.jip.2006.03.009

    Article  PubMed  Google Scholar 

  42. Stevens, M. and Lacomme, C., Transmission of plant viruses, in Aphids as Crop Pests, Second Edition, van Emden, H.F. and Harrington, R., Eds., UK: CAB International, 2017, p. 323. https://doi.org/10.1079/9781780647098.0000

  43. Vasiliev, V.P. and Livshits, I.Z., Vrediteli plodovykh kul’tur (Pests of Fruit Crops), Moscow: Kolos, 1984.

  44. Weikl, F., Ghirardo, A., Schnitzler, J.P., and Pritsch, K., Sesquiterpene emissions from Alternaria alternata and Fusarium oxysporum: effects of age, nutrient availability, and co-cultivation, Sci. Rep., 2016, vol. 6, no. 1, art. 22152. https://doi.org/10.1038/srep22152

  45. Zeyruk, V.N., Belyakova, N.A., Belov, G.L., Vasilyeva, S.V., Derevyagina, M.K., and Mitina, G.V., Biological protection of nuclear seed potato from pests – vectors of viruses in greenhouses, Zashchita Kartofelya, 2017, no. 4, p. 3. http://www.kartofel.org/zakart/zk4_2017.pdf

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This work was supported by the Russian Foundation for Basic Research (project 20-016-00241).

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  1. All-Russian Institute of Plant Protection, Pushkin, 188608, St. Petersburg, Russia

    G. V. Mitina, E. A. Stepanycheva, A. A. Choglokova & M. A. Cherepanova

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Mitina, G.V., Stepanycheva, E.A., Choglokova, A.A. et al. Features of Behavioral Reactions of the Peach Aphid Myzus persicae (Sulzer, 1776) (Hemiptera, Aphididae) to Volatile Organic Compounds of Entomopathogenic Fungi of the Genus Lecanicillium. Entmol. Rev. 101, 1015–1023 (2021). https://doi.org/10.1134/S0013873821080017

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