[en] Abstract
Entomopathogenic fungi (EPF) are insecticide alternatives for pest control. Their ability to easily adhere and quickly penetrate the insect cuticle is a key factor for their selection, which has received too little consideration so far. Here, we evaluated the impact of five EPF on the survival and fecundity of Drosophila suzukii, a worldwide invasive pest of soft-skinned fruits. We assessed the exposure time needed to achieve fly mortality as well as the mortality of two non-target insects: Orius laevigatus and Bombus terrestris, commonly encountered in greenhouses where D. suzukii is the most damaging.
Drosophila suzukii were exposed for 3 hours to a fungal culture from each EPF and survival rates were assessed daily. Beauvaria bassiana was the most efficient EPF, killing over 95% of the flies within 10 days. Additional flies were then exposed to this fungus culture for 10 seconds, 1 minute, 10 minutes and 1 hour. The exposure time impacted the mortality rates: 50% of the flies died within 4 days after a 3-hours exposure to B. bassiana, whereas 6 days were needed to reach the same result with 10 seconds of exposure. Whatever the exposure time, this EPF always needed ten days to be lethal for more than 95% of individuals. Beauvaria bassiana was not lethal for the non-target species.
Thus, B. bassiana is an option to control D. suzukii without harming beneficial insects. Further studies are now needed under real cultivation conditions to assess whether B. bassiana can be included in biocontrol strategies against D. suzukii.
Disciplines :
Entomology & pest control
Author, co-author :
Galland, Chloé
Lalaymia, Ismahen; Université catholique de Louvain
Declerck, Stéphane; Université catholique de Louvain
Verheggen, François ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs
Language :
English
Title :
Efficacy of entomopathogenic fungi against the fruit fly Drosophila suzukii and their side effects on predator and pollinator insects
Asplen, M. K., Anfora, G., Biondi, A., Choi, D.-S., Chu, D., Daane, K. M., … Desneux, N. (2015). Invasion biology of Spotted Wing Drosophila (Drosophila suzukii): A global perspective and future priorities. Journal of Pest Science, 88(3), 469–494. https://doi.org/10.1007/s10340-015-0681-z
Bellamy, D. E., Sisterson, M. S., & Walse, S. S. (2013). Quantifying host potentials: Indexing postharvest fresh fruits for spotted wing Drosophila, Drosophila suzukii. PLoS One, 8(4), e61227. https://doi.org/10.1371/journal.pone.0061227
Besard, L., Mommaerts, V., Abdu-Alla, G., & Smagghe, G. (2011). Lethal and sublethal side-effect assessment supports a more benign profile of spinetoram compared with spinosad in the bumblebee Bombus terrestris. Pest Management Science, 67(5), 541–547. https://doi.org/10.1002/ps.2093
Boughdad, A., Haddi, K., El Bouazzati, A., Nassiri, A., Tahiri, A., El Anbri, C., … Biondi, A. (2021). First record of the invasive Spotted Wing Drosophila infesting berry crops in Africa. Journal of Pest Science, 94(2), 261–271. Retrieved from https://doi.org/10.1007/s10340-020-01280-0
Cahenzli, F., Strack, T., & Daniel, C. (2018). Screening of 25 different natural crop protection products against Drosophila suzukii. Journal of Applied Entomology, 142(6), 563–577. https://doi. org/10.1111/jen.12510
Canassa, F., Tall, S., Moral, R. A., de Lara, I. A., Delalibera, I., Jr., & Meyling, N. V. (2019). Effects of bean seed treatment by the entomopathogenic fungi Metarhizium robertsii and Beauveria bassiana on plant growth, spider mite populations and behavior of predatory mites. Biological Control, 132, 199–208. https://doi.org/10.1016/j.biocontrol.2019.02.003
Cini, A., Ioriatti, C., & Anfora, G. (2012). A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bulletin of Insectology, 65(1), 149–160.
Cossentine, J., Robertson, J. G. M., & Buitenhuis, R. (2016). Impact of acquired entomopathogenic fungi on adult Drosophila suzukii survival and fecundity. Biological Control, 103, 129–137. https://doi.org/10.1016/j.biocontrol.2016.09.002
Cuthbertson, A. G. S., & Audsley, N. (2016). Further screening of entomopathogenic fungi and nematodes as control agents for Drosophila suzukii. Insects, 7(2), 24. https://doi.org/10.3390/insects7020024
Cuthbertson, A. G. S., Blackburn, L. F., & Audsley, N. (2014). Efficacy of commercially available invertebrate predators against Drosophila suzukii. Insects, 5(4), 952–960. https://doi. org/10.3390/insects5040952
Daǧlı, F., & Bahşi, Ş. Ü. (2009). Topical and residual toxicity of six pesticides to Orius majusculus. Phytoparasitica, 37(5), 399– 405. https://doi.org/10.1007/s12600-009-0054-3
Furuie, J. L., Stuart, A. K. da C., Baja, F., Voidaleski, M. F., Zawadneak, M. A. C., & Pimentel, I. C. (2022). Pathogenicity of Beauveria bassiana strains against Drosophila suzukii (Diptera: Drosophilidae). Research. Social Development, 11(2), e41611225730–e41611225730. https://doi.org/10.33448/rsd-v11i2.25730
Galland, C. D. (2022). Would you harm a fly? An introduction to Drosophila suzukii and alternative methods for controlling this invasive pest. Bulletin de la Société Royale des Sciences de Liège, 91(1), 134–167. https://doi.org/10.25518/0037-9565.11012
Galland, C. D., Glesner, V., & Verheggen, F. (2020). Laboratory and field evaluation of a combination of attractants and repellents to control Drosophila suzukii. Entomologia Generalis, 40(3), 263–272. https://doi.org/10.1127/entomologia/2020/1035
Gebremariam, A., Chekol, Y., & Assefa, F. (2022). Extracellular enzyme activity of entomopathogenic fungi, Beauveria bassiana and Metarhizium anisopliae and their pathogenicity potential as a bio-control agent against whitefly pests, Bemisia tabaci and Trialeurodes vaporiorum. (Hemiptera: Aleyrodidae). BMC Research Notes, 15(1), 117. https://doi.org/10.1186/s13104-022-06004-4
Jaber, L. R. (2018). Seed inoculation with endophytic fungal entomopathogens promotes plant growth and reduces crown and root rot (CRR) caused by Fusarium culmorum in wheat. Planta, 248(6), 1525–1535. https://doi.org/10.1007/s00425-018-2991-x
Kenis, M., Tonina, L., Eschen, R., van der Sluis, B., Sancassani, M., Mori, N., … Helsen, H. H. M. (2016). Non-crop plants used as hosts by Drosophila suzukii in Europe. Journal of Pest Science, 89(3), 735–748. https://doi.org/10.1007/s10340-016-0755-6
Larson, N. R., Strickland, J., Shields, V. D. C., & Zhang, A. (2020). Controlled-release dispenser and dry trap developments for Drosophila suzukii detection. Frontiers in Ecology and Evolution, 8, 45. https://doi.org/10.3389/fevo.2020.00045
Larson, N. R., Strickland, J., Shields, V. D., Rodriguez-Saona, C. R., Cloonan, K. R., Short, B. D., … Zhang, A. (2021). Field evaluation of different attractants for detecting and monitoring Drosophila suzukii. Frontiers in Ecology and Evolution, 9, 620445. https://doi.org/10.3389/fevo.2021.620445
Lasa, R., Aguas-Lanzagorta, S., & Williams, T. (2020). Agricultural-grade apple cider vinegar is remarkably attractive to Drosophila suzukii (Diptera: Drosophiliadae) in Mexico. Insects, 11(7), 448. https://doi.org/10.3390/insects11070448
Leach, H. L., Van Timmeren, S., & Isaacs, R. E. (2016). Exclusion netting delays and reduces Drosophila suzukii (Diptera: Drosophilidae) infestation in raspberries. Journal of Economic Entomology, 109(5), 2151–2158. https://doi.org/10.1093/jee/tow157
Lee, J. C., Wang, X. G., Daane, K. M., Hoelmer, K. A., Isaacs, R. E., Sial, A. A., & Walton, V. M. (2019). Biological control of Spotted-Wing Drosophila (Diptera: Drosophilidae): current and pending tactics. Journal of Integrated Pest Management, 10(1), 13. https://doi.org/10.1093/jipm/pmz012
Litwin, A., Nowak, M., & Różalska, S. (2020). Entomopathogenic fungi: unconventional applications. Reviews in Environmental Science and Bio/Technology, 19(1), 23–42. https://doi.org/10.1007/s11157-020-09525-1
Meyerson, L. A., & Mooney, H. A. (2007). Invasive alien species in an era of globalization. Frontiers in Ecology and the Environment, 5(4), 199–208. https://doi.org/10.1890/1540-9295(2007)5[199:IASIAE]2.0.CO;2
Mommaerts, V., Sterk, G., Hoffmann, L., & Smagghe, G. (2009). A laboratory evaluation to determine the compatibility of microbiological control agents with the pollinator Bombus terrestris. Pest Management Science, 65(9), 949–955. https://doi. org/10.1002/ps.1778
Naranjo-Lázaro, J. M., Mellín-Rosas, M. A., González-Padilla, V. D., Sánchez-González, J. A., Moreno-Carrillo, G., & Arredondo-Bernal, H. C. (2014). Susceptibility of Drosophila suzukii Matsumura (Diptera: Drosophilidae) to entomophato-genic fungi. The Southwestern Entomologist, 39(1), 201–203. https://doi.org/10.3958/059.039.0119
Pavlova, A. K., Dahlmann, M., Hauck, M., & Reineke, A. (2017). Laboratory bioassays with three different substrates to test the efficacy of insecticides against various stages of Drosophila suzukii (Diptera: Drosophilidae). Journal of Insect Science, 17(1), 8. https://doi.org/10.1093/jisesa/iew100
Pedrini, N. (2022). The entomopathogenic fungus Beauveria bassiana shows its toxic side within insects: Expression of genes encoding secondary metabolites during pathogenesis. Journal of Fungi (Basel, Switzerland), 8(5), 488. https://doi.org/10.3390/jof8050488
Portilla, M., Luttrell, R., Snodgrass, G., Zhu, Y. C., & Riddick, E. (2017). Lethality of the entomogenous fungus Beauveria bassiana strain NI8 on Lygus lineolaris (Hemiptera: Miridae) and its possible impact on beneficial arthropods. Journal of Entomological Science, 52(4), 352–369. https://doi.org/10.18474/JES17-15.1
Pyšek, P., & Richardson, D. M. (2010). Invasive species, environmental change and management, and health. Annual Review of Environment and Resources, 35(1), 25–55. https://doi.org/10.1146/annurev-environ-033009-095548
Rafaluk, C., Yang, W., Mitschke, A., Rosenstiel, P., Schulenburg, H., & Joop, G. (2017). Highly potent host external immunity acts as a strong selective force enhancing rapid parasite virulence evolution. Environmental Microbiology, 19(5), 2090– 2100. https://doi.org/10.1111/1462-2920.13736
Ramanaidu, K., & Cutler, G. C. (2013). Different toxic and hormetic responses of Bombus impatiens to Beauveria bassiana, Bacillus subtilis and spirotetramat. Pest Management Science, 69(8), 949–954. https://doi.org/10.1002/ps.3456
Rhodes, E. M., Avery, P. B., & Liburd, O. E. (2018). Efficacy of entomopathogenic fungal products for biological control of Spotted Wing Drosophila (Diptera: Drosophilidae) under laboratory conditions. The Florida Entomologist, 101(3), 526–528. https://doi.org/10.1653/024.101.0329
Sharma, A., Srivastava, A., Shukla, A. K., Srivastava, K., Srivastava, A. K., & Saxena, A. K. (2020). Entomopathogenic fungi: a potential source for biological control of insect pests. Phytobiomes: Current Insights and Future Vistas, 225–250. https://doi.org/10.1007/978-981-15-3151-4_9
Sharma, R., & Sharma, P. (2021). Fungal entomopathogens: A systematic review. Egyptian Journal of Biological Pest Control, 31(1), 1–13. https://doi.org/10.1186/s41938-021-00404-7
Toledo-Hernández, R. A., Lasa, R., Montoya, P., Liedo, P., Rodríguez, D., Sánchez, A., & Toledo, J. (2021). Efficacy of food-based attractants for monitoring Drosophila suzukii (Diptera: Drosophilidae) in berry crops. Crop Protection (Guildford, Surrey), 150, 105797. https://doi.org/10.1016/j. cropro.2021.105797
Walsh, D. B., Bolda, M. P., Goodhue, R. E., Dreves, A. J., Lee, J. C., Bruck, D. J., … Zalom, F. G. (2011). Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. Journal of Integrated Pest Management, 2(1), G1–G7. https://doi. org/10.1603/IPM10010
Wang, B., Kang, Q., Lu, Y., Bai, L., & Wang, C. (2012). Unveiling the biosynthetic puzzle of destruxins in Metarhizium species. Proceedings of the National Academy of Sciences of the United States of America, 109(4), 1287–1292. https://doi.org/10.1073/pnas.1115983109
Wang, P., Li, M. J., Bai, Q. R., Ali, A., Desneux, N., Dai, H. J., & Zang, L. S. (2021a). Performance of Trichogramma japonicum as a vector of Beauveria bassiana for parasitizing eggs of rice striped stem borer, Chilo suppressalis. Entomologia Generalis, 41(2), 147–155. https://doi.org/10.1127/entomologia/2021/1068
Wang, H., Peng, H., Li, W., Cheng, P., & Gong, M. (2021b). The toxins of Beauveria bassiana and the strategies to improve their virulence to insects. Frontiers in Microbiology, 12, 705343. https://doi.org/10.3389/fmicb.2021.705343
Wang, X., Lee, J. C., Daane, K. M., Buffington, M. L., & Hoelmer, K. A. (2020). Biological control of Drosophila suzukii. Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources, 15(054), PAVSNNR202015054. https://doi. org/10.1079/PAVSNNR202015054
Weng, Q., Zhang, X., Chen, W., & Hu, Q. (2019). Secondary metabolites and the risks of Isaria fumosorosea and Isaria farinosa. Molecules (Basel, Switzerland), 24(4), 664. https://doi. org/10.3390/molecules24040664
Williams, T., Valle, J., & Viñuela, E. (2003). Is the naturally derived insecticide Spinosad® compatible with insect natural enemies? Biocontrol Science and Technology, 13(5), 459–475. https://doi. org/10.1080/0958315031000140956
Woltz, J. M., Donahue, K. M., Bruck, D. J., & Lee, J. C. (2015). Efficacy of commercially available predators, nematodes and fungal entomopathogens for augmentative control of Drosophila suzukii. Journal of Applied Entomology, 139(10), 759–770. https://doi.org/10.1111/jen.12200
Yasin, M., Wakil, W., Ghazanfar, M. U., Qayyum, M. A., Tahir, M., & Bedford, G. O. (2019). Virulence of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae against red palm weevil, Rhynchophorus ferrugineus (Olivier). Entomological Research, 49(1), 3–12. https://doi.org/10.1111/1748-5967.12260
Yeo, H., Pell, J. K., Alderson, P. G., Clark, S. J., & Pye, B. J. (2003). Laboratory evaluation of temperature effects on the germination and growth of entomopathogenic fungi and on their pathogenicity to two aphid species. Pest Management Science, 59(2), 156–165. https://doi.org/10.1002/ps.622
Yousef, M., Aranda-Valera, E., & Quesada-Moraga, E. (2018). Lure-and-infect and lure-and-kill devices based on Metarhizium brunneum for Spotted Wing Drosophila control. Journal of Pest Science, 91(1), 227–235. https://doi.org/10.1007/s10340-017-0874-8
