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Effect of Volatile Organic Compounds of Entomopathogenic Fungi of the Genus Lecanicillium and Their Component, Acetic Acid, on Female Behavior in the Western Flower Thrips Frankliniella occidentalis (Pergande) (Thysanoptera, Thripidae)

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Abstract

The effect of VOC of six entomopathogenic fungal strains of the genus Lecanicillium on behavioral reactions of female western flower thrips Frankliniella occidentalis was studied on vegetating bean plants and in a Y-shaped olfactometer. Treatment with conidial suspensions of L. lecanii strains F2 and Vl 29 at a concentration of 1 × 107 spores/mL caused significant repellent reactions in female thrips and a 33–34% decrease in the number of offspring. VOC of L. muscarium strain Vl 21 and L. attenuatum strain Vit 71, showing repellency toward female thrips, also significantly reduced the thrips offspring. VOC of L. dimorphum strain ARSEF 2332 and L. longisporum strain Vl 13, isolated from aphids, had a tendency toward attractiveness. Testing in a Y-shaped olfactometer confirmed the repellency of L. lecanii strain F2 and the attractiveness of L. dimorphum strain ARSEF 2332, while the influence of the other studied strains on the thrips behavioral reactions was non-significant. Acetic acid, tested in the olfactometer at doses corresponding to its content in the fungal VOC above the growing mycelium, caused different reactions in female thrips depending on concentration: attractive at 0.17 ppm, neutral at 0.34 ppm, and weakly repellent at 0.85 ppm. These data indicate that acetic acid contained in the fungal VOC does affect the behavioral reactions of thrips. The repellent effect of Lecanicillium spores on female thrips and their negative impact on the pest offspring increase the effectiveness of entomopathogenic fungi.

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REFERENCES

  1. Baran, B., Krzyżowski, M., Cup, M., Janiec, J., Grabowski, M., and Francikowski, J., Repellent effect of volatile fatty acids on lesser mealworm (Alphitobius diaperinus), Insects, 2018, vol. 9, no. 1, p. 35. https://doi.org/10.3390/insects9010035

  2. 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 

  3. Bilbo, T.R., Kennedy, G.G., and Walgenbach, J.F., Western flower thrips (Frankliniella occidentalis) field resistance to spinetoram in North Carolina, Crop Prot., 2023, vol. 165, p. 106. https://doi.org/10.1016/j.cropro.2022.106168

  4. Bojke, A., Tkaczuk, C., Stepnowski, P., and Gołębiowski, M., Comparison of volatile compounds released by entomopathogenic fungi, Microbiol. Res., 2018, vol. 214, p. 129. https://doi.org/10.1016/j.micres.2018.06.011

    Article  CAS  PubMed  Google Scholar 

  5. Butt, T.M., Coates, C.J., Dubovskiy, I.M., and Ratcliffe, N.A., Entomopathogenic fungi: new insights into host–pathogen interactions, Adv. Genet., 2016, vol. 94, p. 307. https://doi.org/10.1016/bs.adgen.2016.01.006

    Article  CAS  PubMed  Google Scholar 

  6. Cao, Y., Zhi, J.R., Li, C., Zhang, R.Z., Wang, C., Shang, B.Z., and Gao, Y.L., Behavioral responses of Frankliniella occidentalis to floral volatiles combined with different background visual cues, Arthropod-Plant Interact., 2018, vol. 12, p. 31. https://doi.org/10.1007/s11829-017-9549-x

  7. González-Mas, N., Gutiérrez-Sánchez, F., Sánchez-Ortiz, A., Grandi, L., Turlings, T.C.J., Manuel Muñoz-Redondo, J., Moreno-Rojas, J.M., and Quesada-Moraga, E., Endophytic colonization by the entomopathogenic fungus Beauveria bassiana affects plant volatile emissions in the presence or absence of chewing and sap-sucking insects, Front. Plant Sci., 2021, vol. 12: 660460. https://doi.org/10.3389/fpls.2021.660460

  8. Hummadi, E.H., Dearden, A., Generalovic, T., Clunie, B., Harrott, A., Cetin, Y., Demirbek, M., Khoja, S., Eastwood, D., Dudley, E., Hazir, S., Touray, M., Ulug, D., Gulsen, S.H., Cimen, H., and Butt, T., Volatile organic compounds of Metarhizium brunneum influence the efficacy of entomopathogenic nematodes in insect control, Biol. Control, 2021, vol. 155: 104527. https://doi.org/10.1016/j.biocontrol.2020.104527

  9. Justin, G., Robbins, P.S., Rocco, T.A., Lukasz, L.S., and Lapointe, S.L., Formic and acetic acids in degradation products of plant volatiles elicit olfactory and behavioral responses from an insect vector, Chem. Senses, 2016, vol. 41, no. 4, p. 325. https://doi.org/10.1093/chemse/bjw005

    Article  CAS  Google Scholar 

  10. Kepler, R.M., Luangsa-Ard, 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 

  11. Kivett, J.M., Cloyd, R.A., and Bello, N.M., Evaluation of entomopathogenic fungi against the western flower thrips (Thysanoptera: Thripidae) under laboratory conditions, J. Entomol. Sci., 2016, vol. 51, no. 4, p. 274. https://doi.org/10.18474/JES16-07.1

    Article  Google Scholar 

  12. Kuzmin, A.G., Titov, Yu.A., Mitina, G.V., and Choglokova, A.A., Mass spectrometric studies of the composition of volatile organic compounds released by various fungal species of genus Lecanicillium, Nauch. Priborostr., 2021, vol. 31, no. 4, p. 71. https://doi.org/10.18358/np-31-4-i7178

  13. Lee, S.J., Kim, S., Kim, J.C., Lee, M.R., Hossain, M.S., Shin, T.S., Kim, T.H., and Kim, J.S., Entomopathogenic Beauveria bassiana granules to control soil-dwelling stage of western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae), BioControl, 2017, vol. 62, no. 5, p. 639. https://doi.org/10.1007/s10526-017-981

  14. Lozano-Soria, A., Picciotti, U., Lopez-Moya, F., LopezCepero, 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

  15. Mainali, B.P. and Lim, U.T., Behavioral response of western flower thrips to visual and olfactory cues, J. Insect Behav., 2011, vol. 24, p. 436. https://doi.org/10.1007/s10905-011-9267-7

    Article  Google Scholar 

  16. 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

  17. 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

  18. Mitina, G.V., Stepanycheva, E.A., Choglokova, A.A., and Cherepanova, M.A., 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, Entomol. Rev., 2021, vol. 101, no. 8, p. 1015. https://doi.org/10.1134/S0013873821080017

    Article  Google Scholar 

  19. Mitina, G.V., Stepanycheva, E.A., and Choglokova, A.A., New approaches to evaluating the effectiveness of entomopathogenic fungi in microbiological plant protection from the western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), Tr. Russ. Entomol. Ob-va, 2022a, vol. 93, p. 132. https://doi.org/10.47640/1605-7678_2022_93_132

  20. Mitina, G.V., Stepanycheva, E.A., Choglokova, A.A., and Cherepanova, M.A., The effects of volatile organic compounds of entomopathogenic Lecanicillium fungi on the behavior of female western flower thrips Frankliniella occidentalis (Pergande), in Sbornik statei XVII Mezhdunarodnoi nauchnoprakticheskoi konferentsii “Agropromyshlennyi kompleks: sostoyanie, problemy, perspektivy” (The Agroindustrial Complex: Its Present State, Problems, and Prospects. Proc. of the 17th Int. Conf.), Penza, 2022b, p. 210.

  21. 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 

  22. Mouden, S., Sarmiento, K.F., Klinkhamer, P.G., and Leiss, K., Integrated pest management in western flower thrips: past, present and future, Pest Manage. Sci., 2017, vol. 73, no. 5, p. 813. https://doi.org/10.1002/ps.4531

    Article  CAS  Google Scholar 

  23. Ormond, E.L., Thomas, A.P.M., Pell, J.K., Freeman, S.N., and Roy, H.E., Avoidance of a generalist entomopathogenic fungus by the ladybird, Coccinella septempunctata, FEMS Microbiol. Ecol., 2011, vol. 77, p. 229. https://doi.org/10.1111/j.1574-6941.2011.01100.x

  24. 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 

  25. Ponce, M.A., Kim, T.N., and Morrison, W.R. III, A systematic review of the behavioral responses by stored-product arthropods to individual or blends of microbially produced volatile cues, Insects, 2021, vol. 12, p. 391. https://doi.org/10.3390/insects12050391

    Article  PubMed  PubMed Central  Google Scholar 

  26. Reitz, S.R., Gao, Y.L., Kirk, W.D.J., Hoddle, M.S., Leiss, K.A., and Funderburk, J.E., Invasion biology, ecology, and management of the western flower thrips, Annu. Rev. Entomol., 2020, vol. 65, p. 17. https://doi.org/10.1146/annurev-ento-011019-024947

    Article  CAS  PubMed  Google Scholar 

  27. Rimal, S., Sang, J., Poudel, S., Thakur, D., Montell, C., and Lee, Y., Mechanism of acetic acid gustatory repulsion in Drosophila, Cell Rep., 2019, vol. 26, no. 6, p. 1432. https://doi.org/10.1016/j.celrep.2019.01.042

  28. Rondot, Y. and Reineke, A., Association of Beauveria bassiana with grapevine plants deters adult black vine weevils, Otiorhynchus sulcatus, Biocontrol Sci. Technol., 2017, vol. 27, p. 811. https://doi.org/10.1080/09583157.2017.1347604

  29. Skinner, M., Gouli, S., Frank, C.E., Parker, B.L., and Kim, J.S., Management of Frankliniella occidentalis (Thysanoptera: Thripidae) with granular formulations of entomopathogenic fungi, Biol. Control, 2012, vol. 63, p. 246. https://doi.org/10.1016/j.biocontrol.2012.08.004

  30. Weisskopf, L., Schulz, S., and Garbeva, P., Microbial volatile organic compounds in intra-kingdom and inter-kingdom interactions, Nature Rev. Microbiol., 2021, vol. 19, p. 391. https://doi.org/10.1038/s41579-020-00508-1

    Article  CAS  Google Scholar 

  31. Wu, S., Tang, L., Fang, F., Li, D., Yuan, X., Lei, Z., and Gao, Y., Screening, efficacy and mechanisms of microbial control agents against sucking pest insects as thrips, Crop Prot., 2018, vol. 55, p. 199. https://doi.org/10.1016/bs.aiip.2018.07.005

    Article  Google Scholar 

  32. Zanardi, O.Z., Volpe, H.X.L., Luvizotto, R.A.G., Magnani, R.F., Gonzalez, F., Carolina, C., Oehlschlager, C.A., Lehan, B.J., Esperança, V., Delfno, J.Y., Freitas, R., de Carvalho, R.I., Mulinari, T.A., Miranda, M.P., Bento, J.M.S., and Leal, W.S., Laboratory and field evaluation of acetic acid-based lures for male Asian citrus psyllid, Diaphorina citri, Sci. Rep., 2019, vol. 9: 12920. https://doi.org/10.1038/s41598-019-49469-3

  33. Zhang, T., Reitz, S.R., Wang, H., and Lei, Z., Sublethal effects of Beauveria bassiana (Ascomycota: Hypocreales) on life table parameters of Frankliniella occidentalis (Thysanoptera: Thripidae), J. Econ. Entomol., 2015, vol. 108, no. 3, p. 975. https://doi.org/10.1093/jee/tov091

  34. Zhou, Y.M., Zou, X., Zhi, J.R., Xie, J.Q., and Jiang, T., Fast recognition of Lecanicillium spp., and its virulence against Frankliniella occidentalis, Front. Microbiol., 2020, vol. 11: 561381. https://doi.org/10.3389/fmicb.2020.56138

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Funding

This work was supported by the Russian Science Foundation and Saint Petersburg Science Foundation (project 23-26-10052).

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  1. All-Russian Institute of Plant Protection, Pushkin, 196608, 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. Effect of Volatile Organic Compounds of Entomopathogenic Fungi of the Genus Lecanicillium and Their Component, Acetic Acid, on Female Behavior in the Western Flower Thrips Frankliniella occidentalis (Pergande) (Thysanoptera, Thripidae). Entmol. Rev. 103, 144–151 (2023). https://doi.org/10.1134/S0013873823020033

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