Virulence of the entomopathogenic fungus Lecanicillium longisporum against the greenhouse whitefly, Trialeurodes vaporariorum and its parasitoid Encarsia formosa

References

• Abbott W. 1925. A method of computing the effectiveness of an insecticide. J Econ Entomol. 18:265–267.
   Web of Science ®Google Scholar
• Aiuchi D, Saito Y, Tone J, Kanazawa M, Tani M, Koike M. 2012. The effect of entomopathogenic Lecanicillium spp. (Hypocreales: Cordycipitaceae) on the aphid parasitoid Aphidius colemani (Hymenoptera: Aphidiinae). Appl Entomol Zool. 47:351–357.
   Web of Science ®Google Scholar
• Aqueel MA, Leather SR. 2013. Virulence of Verticillium lecanii (Z.) against cereal aphids; does timing of infection affect the performance of parasitoids and predators? Pest Manag Sci. 69:493–498.
   PubMed Web of Science ®Google Scholar
• Askary H, Brodeur J. 1999. Susceptibility of larval stages of the aphid parasitoid Aphidius nigripesto the entomopathogenic fungus Verticillium lecanii. J Invertebr Pathol. 73:129–132.
   PubMed Web of Science ®Google Scholar
• Avilla J, Albajes R, Alomar O, Castañé C, Gabarra R. 2004. Biological control of whiteflies on vegetable crops. In: Heinz K.M., Van Driesche R.G. and Parrella M.P., editors. Biocontrol in protected culture. Batavia, IL: Ball Publishing; p. 171–184.
   Google Scholar
• Baverstock J, Alderson P, Pell J. 2005. Influence of the aphid pathogen Pandora neoaphidis on the foraging behaviour of the aphid parasitoid Aphidius ervi. Ecol Entomol. 30:665–672.
   Web of Science ®Google Scholar
• Baverstock J, Roy H, Clark S, Alderson P, Pell J. 2006. Effect of fungal infection on the reproductive potential of aphids and their progeny. J Invertebr Pathol. 91:136–139.
   PubMed Web of Science ®Google Scholar
• Bird AE, Hesketh H, Cross JV, Copland M. 2004. The common black ant, Lasius niger (Hymenoptera: Formicidae), as a vector of the entomopathogen Lecanicillium longisporum to rosy apple aphid, Dysaphis plantaginea (Homoptera: Aphididae). Biocontrol Sci Tech. 14:757–767.
   Web of Science ®Google Scholar
• Brodeur J, Rosenheim JA. 2000. Intraguild interactions in aphid parasitoids. Entomol Exp Appl. 97:93–108.
   Web of Science ®Google Scholar
• Brooks W.M. 1993. Host-parasitoid-pathogen interactions. In: Beckage N.E., Thompson S.N., and Federici B.A., editors. Parasites and Pathogens of Insects, Vol. 2: Pathogens. San Diego: Academic Press; p. 231–272.
   Google Scholar
• Chee Dhang C. 2013. Temephos resistance in field Aedes (Stegomyia) albopictus (Skuse) from Selangor, Malaysia. Trop Biomed. 30:220–230.
   Google Scholar
• Cortez-Madrigal H, Alatorre-Rosas R, Mora-Aguilera G, Bravo-Mojica H, Ortiz-Garcia C, Aceves-Navarro L. 2003. Characterization of multisporic and monosporic isolates of Lecanicillium (= Verticillium) lecanii for the management of Toxoptera aurantii in cocoa. BioControl 48:321–334.
   Web of Science ®Google Scholar
• Danfa A, Van der Valk H. 1999. Laboratory testing of Metarhizium spp. and Beauveria bassiana on Sahelian non-target arthropods. Biocontrol Sci Tech. 9:187–198.
   Web of Science ®Google Scholar
• de Faria MR, Wraight SP. 2007. Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256.
   Web of Science ®Google Scholar
• De la Rosa W, Segura H, Barrera J, Williams T. 2000. Laboratory evaluation of the impact of entomopathogenic fungi on Prorops nasuta (Hymenoptera: Bethylidae), a parasitoid of the coffee berry borer. Environ Entomol. 29:126–131.
   Web of Science ®Google Scholar
• Down RE, Cuthbertson AG, Mathers JJ, Walters KF. 2009. Dissemination of the entomopathogenic fungi, Lecanicillium longisporum and L. muscarium, by the predatory bug, Orius laevigatus, to provide concurrent control of Myzus persicae, Frankliniella occidentalis and Bemisia tabaci. Biol Control 50:172–178.
   Web of Science ®Google Scholar
• Drummond J, Heale J. 1988. Genetic studies on the inheritance of pathogenicity in Verticillium lecanii against Trialeurodes vaporariorum. J Invertebr Pathol. 52:57–65.
   Web of Science ®Google Scholar
• Drummond J, Heale J, Gillespie A. 1987. Germination and effect of reduced humidity on expression of pathogenicity in Verticillium lecanii against the glasshouse whitefly Trialeurodes vaporariorum. An Appl Biol. 111:193–201.
   Web of Science ®Google Scholar
• Fadayivata S, Moravvej G, Karimi J. 2014. Pathogenicity of the fungus Lecanicillium longisporum against Sipha maydis and Metopolophium dirhodum in laboratory conditions. J Plant Protect Res. 54:67–73.
   Google Scholar
• Finney DJ. 1971. Probit analysis. 3rd ed. New York: Cambridge University Press.
   Google Scholar
• Fransen JJ, Winkelman K, van Lenteren JC. 1987. The differential mortality at various life stages of the greenhouse whitefly, Trialeurodes vaporariorum (Homoptera: Aleyrodidae), by infection with the fungus Aschersonia aleyrodis (Deuteromycotina: Coelomycetes). J Invertebr Pathol. 50:158–165.
   Web of Science ®Google Scholar
• Furlong MJ. 2004. Infection of the immature stages of Diadegma semiclausum, an endolarval parasitoid of the diamondback moth, by Beauveria bassiana. J Invertebr Pathol. 86:52–55.
   PubMed Web of Science ®Google Scholar
• Furlong MJ, Pell JK. 2005. Interactions between entomopathogenic fungi and arthropod natural enemies. In: Vega F.E. and Blackwell M., editors. Insect-fungal associations: ecology and evolution. New York: Oxford University Press; p. 51–73.
   Google Scholar
• Geden C, Rutz D, Steinkraus D. 1995. Virulence of different isolates and formulations of Beauveria bassiana for house flies and the parasitoid Muscidifurax raptor. Biol Control 5:615–621.
   Web of Science ®Google Scholar
• Goettel M.S., Inglis D.G. 1997. Hyphomycetes, Chapter V-3. In: L.A. Lacey, editor. Manual of Techniques in Insect Pathology. London: Academic Press; p. 213–249.
   Google Scholar
• Goettel MS, Koike M, Kim JJ, Aiuchi D, Shinya R, Brodeur J. 2008. Potential of Lecanicillium spp. for management of insects, nematodes and plant diseases. J Invertebr Pathol. 98:256–261.
   PubMed Web of Science ®Google Scholar
• Hall R. 1984. Epizootic potential for aphids of different isolates of the fungus, Verticillium lecanii. Entomophaga 29:311–321.
   Google Scholar
• Hoddle M, Van Driesche R, Sanderson J. 1998. Biology and use of the whitefly parasitoid Encarsia formosa. Annu Rev Entomol. 43:645–669.
   PubMed Web of Science ®Google Scholar
• Huang Z, Sahar F, Ren S, Ali S. 2010. Effect of Isaria fumosoroseus on Eretmocerus sp. nr. furuhashii (Hymenoptera: Aphelinidae), a Parasitoid of Bemisia tabaci (Hemiptera: Aleyrodidae). Pakistan J Zool. 42:121–127.
   Web of Science ®Google Scholar
• Jackson C, Heale J, Hall R. 1985. Traits associated with virulence to the aphid Macrosiphoniella sanborni in eighteen isolates of Verticillium lecanii. An Appl Biol. 106:39–48.
   Web of Science ®Google Scholar
• Khan MA, Khan H, Ruberson JR. 2015. Lethal and behavioral effects of selected novel pesticides on adults of Trichogramma pretiosum (Trichogrammatidae: Hymenoptera). Pest Manag Sci. 71:1640–1648.
   PubMed Web of Science ®Google Scholar
• Kim JJ, Goettel MS, Gillespie DR. 2007. Potential of Lecanicillium species for dual microbial control of aphids and the cucumber powdery mildew fungus, Sphaerotheca fuliginea. Biol Control 40:327–332.
   Web of Science ®Google Scholar
• Kim JJ, Goettel MS, Gillespie DR. 2008. Evaluation of Lecanicillium longisporum, Vertalec® for simultaneous suppression of cotton aphid, Aphis gossypii, and cucumber powdery mildew, Sphaerotheca fuliginea, on potted cucumbers. Biol Control 45:404–409.
   Web of Science ®Google Scholar
• Kim JJ, Goettel MS, Gillespie DR. 2010. Evaluation of Lecanicillium longisporum, Vertalec® against the cotton aphid, Aphis gossypii, and cucumber powdery mildew, Sphaerotheca fuliginea in a greenhouse environment. Crop Prot. 29:540–544.
   Web of Science ®Google Scholar
• Labbe R, Gillespie D, Cloutier C, Brodeur J. 2009. Compatibility of an entomopathogenic fungus with a predator and a parasitoid in the biological control of greenhouse whitefly. Biocontrol Sci Tech. 19:429–446.
   Web of Science ®Google Scholar
• Lacey LA, Mesquita AL, Mercadier G, Debire R, Kazmer DJ, Leclant F. 1997. Acute and sublethal activity of the entomopathogenic fungus Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) on adult Aphelinus asychis (Hymenoptera: Aphelinidae). Environ Entomol. 26:1452–1460.
   Web of Science ®Google Scholar
• Lacey LA, Solter LF. 2012. Initial handling and diagnosis of diseased invertebrates. In: Lacey LA, editor. Manual of techniques in invertebrate pathology. 2nd ed. Amsterdam: Academic Press; p. 1–14.
   Google Scholar
• Laznik Z, Znidarcic D, Trdan S. 2011. Control of Trialeurodes vaporariorum (Westwood) adults on glasshouse-grown cucumbers in four different growth substrates: an efficacy comparison of foliar application of Steinernema feltiae (Filipjev) and spraying with thiamethoxamn. Turk J Agric For. 35:631–640.
   Web of Science ®Google Scholar
• Lazreg F, Huang Z, Ali S, Ren S. 2009. Effect of Lecanicillium muscarium on Eretmocerus sp. nr. furuhashii (Hymenoptera: Aphelinidae), a parasitoid of Bemisia tabaci (Hemiptera: Aleyrodidae). J Pest Sci. 82:27–32.
   Web of Science ®Google Scholar
• Lenteren JC, Fransen JJ. 1994. Survival of the parasitoid Encarsia formosa after treatment of parasitized greenhouse whitefly larvae with fungal spores of Aschersonia aleyrodis. Entomol Exp Appl. 71:235–243.
   Web of Science ®Google Scholar
• Li SJ, Ren SL, Xue X, Ren SX, Cuthbertson AG, van Dam NM, Qiu BL. 2014. Efficiency of plant induced volatiles in attracting Encarsia formosa and Serangium japonicum, two dominant natural enemies of whitefly Bemisia tabaci in China. Pest Manag Sci. 70:1604–1610.
   PubMed Web of Science ®Google Scholar
• Masuda T, Kikuchi O. 1992. Pathogenicity of Verticillium lecanii isolates to whitefly and aphids. Jpn J Appl Entomol Zool. 36:239–245.
   Web of Science ®Google Scholar
• McGregor RR, Gillespie DR, Quiring DMJ, Foisy MRJ. 1999. Potential Use of Dicyphus hesperus Knight (Heteroptera: Miridae) for biological control of pests of greenhouse tomatoes. Biol Control 16:104–110.
   Web of Science ®Google Scholar
• Meade DL, Byrne DN. 1991. The use of Verticillium lecanii against subimaginal instars of Bemisia tabaci. J Invertebr Pathol. 57:296–298.
   Web of Science ®Google Scholar
• Mesquita AL, Lacey LA. 2001. Interactions among the entomopathogenic fungus, Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes), the parasitoid, Aphelinus asychis (Hymenoptera: Aphelinidae), and their aphid host. Biol Control 22:51–59.
   Web of Science ®Google Scholar
• Moravej G, Karimi J. 2014. Pathogenicity of Lecanicillium longisporum (Ascomycota: Hypocreomycetidae) on the aphid Cinara pini (Hemiptera: Lachnidae) in laboratory condition. J Crop Prot. 3:159–171.
   Google Scholar
• Moreno-Ripoll R, Gabarra R, Symondson WOC, King RA, Agustí N. 2014. Do the interactions among natural enemies compromise the biological control of the whitefly Bemisia tabaci? J Pest Sci. 87:133–141.
   Web of Science ®Google Scholar
• Nielsen C, Skovgård H, Steenberg T. 2005. Effect of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) on survival and reproduction of the filth fly parasitoid, Spalangia cameroni (Hymenoptera: Pteromalidae). Environ Entomol. 34:133–139.
   Web of Science ®Google Scholar
• Oreste M, Bubici G, Poliseno M, Tarasco E. 2016. Effect of Beauveria bassiana and Metarhizium anisopliae on the Trialeurodes vaporariorum-Encarsia formosa system. J Pest Sci. 89:153–160.
   Web of Science ®Google Scholar
• Panahi O, Loni A. 2013. Bioassay evaluation of the entomopathogenic fungus, Lecanicillium longisporum (Petch) Zare & Gams against egg and nymphs of Trialeurodes vaporariorum Westwood in laboratory conditions. Arch Phytopathol Plant Prot. 46:849–861.
   Google Scholar
• Park H, Kim K. 2010. Selection of Lecanicillium strain with high virulence against developmental stages of Bemisia tabaci. Mycobiol. 38:210–214.
   PubMedGoogle Scholar
• Pérez-Hedo M, Urbaneja-Bernat P, Jaques JA, Flors V, Urbaneja A. 2015. Defensive plant responses induced by Nesidiocoris tenuis (Hemiptera: Miridae) on tomato plants. J Pest Sci. 88:543–554.
   Web of Science ®Google Scholar
• Powell W, Wilding N, Brobyn PJ, Clark SJ. 1986. Interference between parasitoids (Hymenoptera: Aphidiidae) and fungi (Entomophthorales) attacking cereal aphids. Entomophaga 31:293–302.
   Google Scholar
• Rana SM, Khan EA, Yaqoob A, Latif AA, Abbasi MM. 2014. Susceptibility and irritability of adult forms of main malaria vectors against insecticides used in the indoor residual sprays in Muzaffargarh district, Pakistan: a field survey. J Med Entomol. 51:387–391.
   PubMed Web of Science ®Google Scholar
• Rännbäck L-M, Cotes B, Anderson P, Rämert B, Meyling NV. 2015. Mortality risk from entomopathogenic fungi affects oviposition behavior in the parasitoid wasp Trybliographa rapae. J Invertebr Pathol. 124:78–86.
   PubMed Web of Science ®Google Scholar
• Raymond M. 1985. Log-probit analysis basic programme of microcomputer. Cahiers ORSTOM series. Ent Med Parasitol. 22:117–121.
   Google Scholar
• Ren S, Ali S, Huang Z, Wu J. 2010. Lecanicillium muscarium as microbial insecticide against whitefly and its interaction with other natural enemies. In: Méndez-Vilas A., editor. Current Research, Technology and Education in Topics in Applied Microbiology and Microbial Biotechnology. Badajoz, Spain: Formatex Research Center Pub.; p. 339–348.
   Google Scholar
• Robertson J, Preisler H, Russell R. 2002. Polo plus. Probit and logit analysis user's guide. Petaluna, CA: LeOra Software.
   Google Scholar
• Robertson J, Preisler H, Russell R. 2007. PoloPlus: Probit and logit analysis user's guide. Petaluna, CA: LeOra Software.
   Google Scholar
• Roditakis E, Couzin ID, Franks NR, Charnley AK. 2008. Effects of Lecanicillium longisporum infection on the behaviour of the green peach aphid Myzus persicae. J Insect Physiol. 54:128–136.
   PubMed Web of Science ®Google Scholar
• Roy HE, Pell JK. 2000. Interactions between entomopathogenic fungi and other natural enemies: implications for biological control. Biocontrol Sci Tech. 10:737–752.
   Web of Science ®Google Scholar
• SAS Institute. 2005. SAS 9.1.3., Cary, NC: SAS Institute Inc.
   Google Scholar
• Sugimoto M, Koike M, Hiyama N, Nagao H. 2003. Genetic, morphological, and virulence characterization of the entomopathogenic fungus Verticillium lecanii. J Invertebr Pathol. 82:176–187.
   PubMed Web of Science ®Google Scholar
• Zhang GF, Lövei GL, Hu M, Wan FH. 2014. Asymmetric consequences of host plant occupation on the competition between the whiteflies Bemisia tabaci cryptic species MEAM1 and Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). Pest Manag Sci. 70:1797–1807.
   PubMed Web of Science ®Google Scholar