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Research Articles

Sublethal effects of a Beauveria bassiana-based mycopesticide on Dutch and Serbian populations of Encarsia formosa (Hymenoptera: Aphelinidae)

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Pages 991-1008 | Received 24 Dec 2018, Accepted 12 Jun 2019, Published online: 25 Jun 2019

References

  • Albajes, R., Lodovica Gullino, M., van Lenteren, J. C., & Elad, Y. (Eds.). (1999). Integrated pest and disease management in greenhouse crops. Dordrecht: Kluwer Academic Publisher.
  • Askary, H., & Brodeur, J. (1999). Susceptibility of larval stages of the aphid parasitoid Aphidius nigripes to the entomopathogenic fungus Verticillium lecanii. Journal of Invertebrate Pathology, 73, 129–132. doi: 10.1006/jipa.1998.4824
  • Avery, P. B., Faull, J., & Simmonds, M. S. J. (2008). Effects of Paecilomyces fumosoroseus and Encarsia formosa on the control of the greenhouse whitefly: Preliminary assessment of a compatibility study. Biocontrol, 53, 303–316. doi: 10.1007/s10526-007-9073-5
  • Chandler, D., Bailey, A. S., Tatchell, G. M., Davidson, G., Greaves, J., & Grant, W. P. (2011). The development, regulation and use of biopesticides for integrated pest management. Philosophical Transactions of the Royal Society B: Biological Sciences, 366, 1987–1998. doi: 10.1098/rstb.2010.0390
  • Copping, L. G., & Menn, J. J. (2000). Biopesticides: A review of their action, applications and efficacy. Pest Management Science, 56, 651–676. doi:10.1002/1526-4998(200008)56:8<651::AID-PS201>3.0.CO;2-U
  • Daniel, C. (2014). Rhagoletis cerasi: Oviposition reduction effects of oil products. Insects, 5, 319–331. doi: 10.3390/insects5020319
  • Desneux, N., Decourtye, A., & Delpuech, J. M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52, 81–106. doi: 10.1146/annurev.ento.52.110405.091440
  • Desneux, N., Denoyelle, R., & Kaiser, L. (2006). A multi-step bioassay to assess the effect of the deltamethrin on the parasitic wasp Aphidius ervi. Chemosphere, 65, 1697–1706. doi: 10.1016/j.chemosphere.2006.04.082
  • Drobnjaković, T., Marčić, D., Prijović, M., Perić, P., Milenković, S., & Bošković, J. (2016). Life history traits and population growth of Encarsia formosa Gahan (Hymenoptera: Aphelinidae) local population from Serbia. Entomologia Generalis, 35, 281–295. doi: 10.1127/entomologia/2016/0183
  • Drobnjaković, T., Marčić, D., Prijović, M., Perić, P., Milenković, S., & Bošković, J. (2018). Sublethal effects of NeemAzal- T/S botanical insecticide on Dutch and Serbian populations of Encarsia formosa (Hymenoptera: Aphelinidae). Biocontrol Science and Technology, 28, 1–19. doi: 10.1080/09583157.2017.1409336
  • Enkegaard, A., & Brødsgaard, H. F. (2006). Biocontrol in protected crops: Is lack of biodiversity a limiting factor? In J. Eilenberg & H. M. T. Hokkanen (Eds.), An ecological and society approach to biological control (pp. 91–122). New York, NY: Springer.
  • EU. (2016). EU pesticides database. Retrieved from http://ec.europa.eu/food/plant/pesticides/eu-pesticides-database/public/?event=activesubstance.selection&language=PL
  • Europian Plant Protection Organisation (EPPO). (2004). Side effects on Encarsia formosa. EPPO, Paris, PP1/142(2).
  • Faria, M. R., & Wraight, S. P. (2007). Mycoinsecticides and mycoacaricides; a comprehensive list with worldwide coverage and international classification of formulation types. Biological Control, 43, 237–256. doi: 10.1016/j.biocontrol.2007.08.001
  • Feldhege, M., & Schmutterer, H. (1993). Investigations on side effects of Margosan-O on Encarsia formosa Gah. (Hym., Aphelenidae) parasitoid of greenhouse whitefly Trialeurodes vaporariorum Westw. (Hom., Aleyrodidae). Journal of Applied Entomology, 115, 37–42. doi: 10.1111/j.1439-0418.1993.tb00361.x
  • Fransen, J. J., & van Lenteren, J. C. (1993). Host selection and survival of the parasitoid Encarsia formosa on greenhouse whitefly, Trialeurodes vaporariorum, in the presence of hosts infected with the fungus Aschersonia aleyrodis. Entomologia Experimentalis et Applicata, 69, 239–249. doi: 10.1111/j.1570-7458.1993.tb01747.x
  • Fransen, J. J., & van Lenteren, J. C. (1994). Survival of the parasitoid Encarsia formosa after treatment of parasitized greenhouse whitefly larvae with fungal spores of Aschersonia aleyrodis. Entomologia Experimentalis et Applicata, 71, 235–243. doi: 10.1111/j.1570-7458.1994.tb01790.x
  • Furlong, M. J. (2004). Infection of the immature stages of Diadegma semiclausum, an endolarval parasitoid of the diamondback moth, by Beauveria bassiana. Journal of Invertebrate Pathology, 86, 52–55. doi: 10.1016/j.jip.2004.03.006
  • Hamdi, F., Fargues, J., Ridray, G., Jeannequin, B., & Bonato, O. (2011). Compatibility among entomopathogenic hyphocreales and two beneficial insects used to control Trialeurodes vaporariorum (Hemiptera: Aleurodidae) in Mediterranean greenhouses. Journal of Invertebrate Pathology, 108, 22–29. doi: 10.1016/j.jip.2011.05.018
  • Hidayat, Y., Heather, N., & Hassan, E. (2013). Repellency and oviposition deterrence effects of plant essential and vegetable oils against female Queensland fruit fry Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Australian Journal of Entomology, 52, 379–386. doi: 10.1111/aen.12040
  • Hoddle, M. S., Van Driesche, R. G., & Sanderson, J. P. (1998). Biology and use of the whitefly parasitoid Encarsia formosa. Annual Review of Entomology, 43, 645–669. doi: 10.1146/annurev.ento.43.1.645
  • James, R. R., Buckner, J. S., & Freeman, T. P. (2003). Cuticular lipids and silverleaf whitefly stage affect conidial germination of Beauveria bassiana and Paecilomyces fumosoroseus. Journal of Invertebrate Pathology, 84, 67–74. doi: 10.1016/j.jip.2003.08.006
  • Jazzar, C., & Hammad, E. A. F. (2004). Efficacy of multiple biocontrol agents against the sweet potato whitefly Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) on tomato. Journal of Applied Entomology, 128, 188–194. doi: 10.1111/j.1439-0418.2004.00833.x
  • Jones, W. A., & Poprawski, T. J. (1996). Bemisia argentifolii parasitized by Eretmocerus sp. is immune to infection by Beauveria bassiana. In T. C. Henneberry, N. C. Toscano, & R. M. Faust (Eds.), Silverleaf whitefly, supplement to the five-year national research and action plan (pp. 118). USDA, ARS 1996-01.
  • Labbé, R. (2005). Intraguild interactions of the greenhouse whitefly natural enemies, predator Dicyphus hesperus, pathogen Beauveria bassiana and parasitoid E. formosa (M.Sc.Thesis). Université Laval. Faculté des Siences de I’Agriculture et de I’Alimentation, Québec.
  • Labbé, R. M., Gillespie, D. R., Cloutier, C., & Brodeur, J. (2009). Compatibility of an entomopathogenic fungus with a predator and a parasitoid in the biological control of greenhouse whitefly. Biocontrol Science and Technology, 19, 429–446. doi: 10.1080/09583150902803229
  • Lacey, L. A., Mesquita, A. L. M., Mercadier, G., Debire, R., Kazmer, D. J., & Leclant, F. (1997). Acute and sublethal activity of the entomopathogenic fungus Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) on adult Aphelinus asychis (Hymenoptera: Aphelinidae). Environmental Entomology, 26, 1452–1460. doi: 10.1093/ee/26.6.1452
  • Mesquita, A. L. M., Lacey, L. A., & Leclant, F. (1997). Individual and combined effects of the fungus, Pacilomyces fumoroseus and a parasitoid, Aphelinus asychis Walker (Hym. Aphelinidae) on confined populations of the Russian wheat aphid, Diura phisnoxia (Mordvilko) (Hom., Aphididae) under field conditions. Journal of Applied Entomology, 121, 155–163. doi: 10.1111/j.1439-0418.1997.tb01386.x
  • Oreste, M., Bubici, G., Poliseno, M., & Tarasco, E. (2015). Effect of Beauveria bassiana and Metarhizium anisopliae on the Trialeurodes vaporariorum - Encarsia formosa system. Journal of Pesticide Science, 89, 153–160. doi: 10.1007/s10340-015-0660-4
  • Oreste, M., Bubici, G., Poliseno, M., & Tarasco, E. (2016). Effects of entomopathogenic fungi on Encarsia formosa Gahan.(Hymenoptera: Aphelinidae) activity and behavior. Biological Control, 100, 46–53. doi: 10.1016/j.biocontrol.2016.05.011
  • Oreste, M., Poliseno, M., & Tarasco, E. (2013). Effect of entomopathogic fungi against Trialeurodes vaporariorum and its parasitoid Encarsia formosa: Preliminary laboratory assays. IOBC/WPRS Bulletin, 90, 91.
  • Perić, P., Marčić, D., & Stamenković, S. (2009). Natural enemies of whitefly (Trialeurodes vaporariorum Westwood) in Serbia. Acta Horticulturae, 830, 539–544. doi: 10.17660/ActaHortic.2009.830.77
  • Polaszek, A., Evans, G. A., & Bernett, E. D. (1992). Encarsia parasitoids of Bemisia tabaci (Hymenoptera: Aphelinidae, Homoptera: Aleyrodidae): A preliminary guide to identification. Bulletin of Entomological Research, 82, 375–392. doi: 10.1017/S0007485300041171
  • Prijović, M., Škaljac, M., Drobnjaković, T., Žanić, K., Perić, P., Marčić, D., & Puizina, J. (2014). Genetic variation of the greenhouse whitefly, Trialeurodes vaporariorum (Hemiptera: Aleyrodidae), among populations from Serbia and neighbouring countries, as inferred from COI sequence variability. Bulletin of Entomological Research, 104, 357–366. doi: 10.1017/S0007485314000169
  • Rashki, M., Kharazi-Pakdel, A., Allahyari, H., & van Alphen, J. J. M. (2009). Interactions among the entomopathogenic fungus, Beauveria bassiana (Ascomycota: Hypocreales), the parasitoid, Aphidius matricariae (Hymenoptera: Braconidae), and its host, Myzus persicae (Homoptera: Aphididae). Biological Control, 50, 324–328. doi: 10.1016/j.biocontrol.2009.04.016
  • Robertson, J. L., Russell, R. M., Preisler, H. K., & Savin, N. E. (2007). Bioassays with arthropods (2nd ed.). Boca Raton, FL: CRC Press, Taylor & Francis Group.
  • Rombach, M. C., & Gillespie, A. T. (1988). Entomogenous hyphomycetes for insect and mite control on greenhouse crops. Biocontrol News and Information, 9, 7–18.
  • Schoonover, J. R., & Larson, L. L. (1995). Laboratory activity of spinosad on non-target beneficial arthropods, 1994. Arthropod Management Tests, 20, 357–357. doi: 10.1093/amt/20.1.357
  • Shi, W. B., Feng, M. G., & Liu, S. S. (2008). Sprays of emulsifiable Beauveria bassiana formulation are ovicidal towards Tetranychus urticae (Acari: Tetranychidae) at various regimes of temperature and humidity. Experimental and Applied Acarology, 46, 247–257. doi: 10.1007/s10493-008-9172-8
  • Simmonds, M. S. J., Manlove, J. D., Blaney, W. M., & Khambay, B. P. S. (2002). Effects of selected botanical insecticides on the behaviour and mortality of the glasshouse whitefly Trialeurodes vaporarium and the parasitoid Encarsia formosa. Entomologia Experimentalis et Applicata, 102, 39–47. doi: 10.1046/j.1570-7458.2002.00923.x
  • Stansly, P. A., & Liu, T. X. (1997). Selectivity of insecticides to Encarsia pergandiella, an endoparasitoid of Bemisia argentifolii. Bulletin of Entomological Research, 87, 525–531. doi: 10.1017/S0007485300041390
  • Stark, J. D., & Banken, J. A. O. (1999). Importance of population structure at the time of toxicant exposure. Ecotoxicology and Environmental Safety, 42, 282–287. doi: 10.1006/eesa.1998.1760
  • Stark, J. D., & Banks, J. E. (2003). Population-level effects of pesticides and other toxicants on arthropods. Annual Review of Entomology, 48, 505–519. doi: 10.1146/annurev.ento.48.091801.112621
  • Stark, J. D., Tanigoshi, L., Bounfour, M., & Antonelli, A. (1997). Reproductive potential: Its influence on the susceptibility of a species to pesticides. Ecotoxicology and Environmental Safety, 37, 273–279. doi: 10.1006/eesa.1997.1552
  • Stouthamer, R., & Mak, F. (2002). Influence of antibiotics on the offspring production of the Wolbachia-infected parthenogenetic parasitoid Encarsia formosa. Journal of Invertebrate Pathology, 80, 41–45. doi: 10.1016/S0022-2011(02)00034-4
  • Tsolakis, H., & Ragusa, S. (2008). Effects of a mixture of vegetable and essential oils and fatty acid potassium salts on Tetranychus urticae and Phytoseiulus persimilis. Ecotoxicology and Environmental Safety, 70, 276–282. doi: 10.1016/j.ecoenv.2007.10.001
  • van Lenteren, J. C., & Martin, G. (1999). Biological control of whiteflies. In R. Albajes, M. L. Gullino, J. C. van Lenteren, & Y. Elad (Eds.), Integrated pest and disease management in greenhouse crops (pp. 202–215). Dordrecht: Kluwer.
  • Villaverde, J. J., Sevilla-Morán, B., Sandín-España, P., López-Goti, C., & Alonso-Prados, J. L. (2014). Biopesticides in the framework of the European pesticide regulation (EC) no. 1107/2009. Pest Management Science, 70, 2–5. doi: 10.1002/ps.3663
  • Walthall, W. K., & Stark, J. D. (1997). Comparison of two population-level ecotoxicological endpoints: The intrinsic (rm) and instantaneous (ri) rates of increase. Environmental Toxicology and Chemistry, 16, 1068–1073. doi: 10.1016/S0147-6513(03)00033-2
  • Whalon, M. E., Mota-Sanchez, D., Hollingworth, R. M., & Duynslager, L. (2018). Arthropod pesticide resistance database. Retrieved from https://-www.pesticideresistance.com
  • Wraight, S. P., Jackson, M. A., & De Kock, S. L. (2001). Production, stabilization and formulation of fungal biocontrol agents. In T. M. Butt, C. Jackson, & N. Magan (Eds.), Fungi as biocontrol agents (pp. 253–287). Wallingford: CAB International.
  • Yang, N. W., Li, A. L., Wan, F. H., Liu, W. X., & Johnson, D. (2010). Effects of plant essential oils on immature and adult sweetpotato whitefly, Bemisia tabaci biotype B. Crop Protection, 29, 1200–1207. doi: 10.1016/j.cropro.2010.05.006
  • Zchori-Fein, E., Roush, R. T., & Sanderson, J. P. (1994). Potential for integration of biological and chemical control of greenhouse whitefly (Homoptera: Aleyrodidae) using Encarsia formosa (Hymenoptera: Aphelinidae) and abamectin. Environmental Entomology, 23, 1277–1282. doi: 10.1093/ee/23.5.1277

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