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 AE  Vol.8 No.3 , July 2020
Interactions between Entomopathogenic Fungi and Entomophagous Insects
Abstract: Direct treatment of predators with entomopathogenic fungi (EPF) at different concentrations revealed that some species, like Beauveria bassiana and Metarhizium anisopliae, were found to have detrimental effects on all developmental stages of some predator species. Other species, like Numoraea rileyi and Paecilomycis fumosorosius, showed little or no effect on treated predators. Adult predators were found to avoid feeding on fungi-infected prey. EPF could be isolated from hibernating or field-collected coccinellids. Some studies indicated that combining a fungus with a predator could increase the rate of insect control in the field. As for parasitoids, this review indicates that the developmental stages of the egg parasitoids can develop successfully in host eggs treated with fungi. However, fungus-infected hosts negatively impact the development of larval parasitoids inside such hosts and this impact depends on the species and concentration of the fungus as well as the time between infection and parasitism. Some parasitoid females can discriminate between fungus-infected and uninfected hosts and do not parasitize the infected hosts. With appropriate timing, the parasitoids or predators could be combined with fungi for the biological control of insects in the field.
Cite this paper: Abbas, M. (2020) Interactions between Entomopathogenic Fungi and Entomophagous Insects. Advances in Entomology, 8, 130-146. doi: 10.4236/ae.2020.83010.
References

[1]   Rosenheim, J.A., Kaya, H.K., Ehler, L.E., Marois, J.J. and Jaffee, B.A. (1995) Intraguild Predation among Biological Control Agents: Theory and Evidence. Biological Control, 5, 303-335.
https://doi.org/10.1006/bcon.1995.1038

[2]   Labauda, S. and Griffin, C.T. (2018) Transmission Success of Entomopathogenic Nematodes Used in Pest Control. Insects, 9, 72-91.
https://doi.org/10.3390/insects9020072

[3]   Beline, T. (2018) Entomopathogenic Nematodes as Biocontrol Agents of Insect Pests. CAB Reviews, 13, No. 58.
http://www.cabi.org/cabreviews
http://www.iobcwprs.org/ip_ipm/03021_IOBCWorkingDocumentPesticides_Explanation.pdf
https://doi.org/10.1079/PAVSNNR201813058


[4]   Ferguson, K.I. and Stiling, P. (1996) Non-Additive Effects of Multiple Natural Enemies on Aphid Populations. Oecologia, 108, 375-379.
https://doi.org/10.1007/BF00334664

[5]   Hajek, A.E. and Butler, L. (2000) Predicting the Host Range of Entomopathogenic Fungi. In: Follete, P.A. and Duan, J.J., Eds., Non Target Effect of Biological Control, Kluwer Academic Publishers, Dordrecht, 263-276.
https://doi.org/10.1007/978-1-4615-4577-4_15

[6]   Pendland, J.C. and Boucias, D.G. (1982) Ultrastructural Aspects of Conidogenesis in the Entomogenous Hyphomycete, Nomuraea rileyi. Canadian Journal of Botany, 60, 26-33.
https://doi.org/10.1139/b82-004

[7]   Nalepa, C.A. and Weir, A. (2007) Infection of Harmonia axyridis (Coleoptera: Coccinellidae) by Hesperomyces virescens (Ascomycetes: Laboulbeniales): Role of Mating Status and Aggregation Behavior. Journal of Invertebrate Pathology, 94, 196-203.
https://doi.org/10.1016/j.jip.2006.11.002

[8]   Scorsetti, A.C., Pelizza, S. and Cabello, M.N. (2012) New Records of Hypocrealean Fungi Infecting Aphids and Whiteflies: Pathogenicity against Myzus persicae and Interaction with Its Predator, Eriopis connexa. Biocontrol Science and Technology, 22, 1099-1105.
https://doi.org/10.1080/09583157.2012.710320

[9]   Kiselek, E.V. (1975) The Effect of Bio-Preparations on Insect Enemies. Zashchita Rastenii, 12, 23-25.

[10]   James, R.R. and Lighthart, B. (1994) Susceptibility of the Convergent Lady Beetle (Coleoptera: Coccinellidae) to Four Entomogenous Fungi. Environmental Entomology, 23, 190-192.
https://doi.org/10.1093/ee/23.1.190

[11]   Mahmoud, B.A. (2011) The Effects of Beauveria bassiana and Methylamineavermectin (Radical) on Spodoptera littoralis and Two Non-Target Insects, Coccinella septempunctata and Chrysoperla carnea. Journal of the Egyptian Society of Parasitology, 44, 85-93.

[12]   Trizelia, L., Munzir, B. and Agung, P. (2017) Pathogenicity of Entomopathogenic Fungi, Metarhizium spp. against Predator, Menochilus sexmaculatus Fabricius (Coleoptera: Coccinelidae). Asian Journal of Agriculture, 1, 1-5.
https://doi.org/10.13057/asianjagric/g010101

[13]   Sewify, G.H. and El-Arnaouty, S.A. (1998) The Effect of Verticillium lecanii (Zimm.) on Larvae of Chrysoperla carnea in the Laboratory. Acta Zoologica Fennica, 209, 233-237.

[14]   Aqueel, M. and Leather, S.R. (2013) Virulence of Verticillium lecanii (Z.) against Cereal Aphids: Does Timing of Infection Affect the Performance of Parasitoids and Predators? Pest Management Science, 69, 493-498.
https://doi.org/10.1002/ps.3398

[15]   Valez, M.P.J. (2008) Compatibility of the Entomopathogenic Fungus, Lecanicillium longisporum with the Predatory Midge, Aphidoletes aphidimyza. M.Sc. Thesis, Dept. Biological Sciences, Simon Fraser University, Burnaby.

[16]   Scorsetti, A.C., Pelizza, S., Fogel, M.N., Vianna, F. and Schneider, M.I. (2017) Interactions between the Entomopathogenic Fungus, Beauveria bassiana and the Neotropical Predator, Eriopis connexa (Coleoptera: Coccinellidae): Implications in Biological Control of Pests. Journal of Plant Protection Research, 57.
https://doi.org/10.1515/jppr-2017-0053

[17]   Ignoffo, C.M. (1981) The Fungus Nomuraea rileyi as a Microbial Insecticide. In: Burges, H.D., Ed., Microbial Control of Pests and Plant Diseases, 1970-1980, Academic Press, San Diego.

[18]   Bourassa, C., Vincent, C.J. and Mauffette, Y. (2001) Effect of Entomopathogenic Hyphomycetes against the Larger Grain Borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae), and Its Predator, Tretriosova nigriscens Lewis (Coleoptera: Histeridae). Journal of Invertebrate Pathology, 77, 75-80.
https://doi.org/10.1006/jipa.2000.4986

[19]   Roy, H.E., Brown, P.M.J., Rothery, P. and Majerus, M.E.N. (2008) Interaction between the Fungal Pathogen, Beauveria bassiana and Three Species of Coccinellid: Harmonia axyridis, Coccinella septempunctata and Adalia bipunctata. Bio-Control, 53, 265-276.
https://doi.org/10.1007/s10526-007-9122-0

[20]   Cottrell, T.E. and Shapiro-Ilan, D.I. (2008) Susceptibility of Endemic and Exotic North American Ladybirds (Coleoptera: Coccinellidae) to Endemic Fungal Entomopathogens. European Journal of Entomology, 105, 455-460.
https://doi.org/10.14411/eje.2008.058

[21]   Ana, C.S., Sebastian, P., Marilina, N.F., Florencia, V. and Marcela, I.S. (2017) Interactions between the Entomopathogenic Fungus, Beauveria bassiana, and the Neotropical Predator, Eriopis connexa (Coleoptera: Coccinellidae) Implications in Biological Control of Pests. Journal of Plant Protection Research, 57, 389-395.

[22]   Saito, T. and Brownbridge, M. (2016) Compatibility of Soil-Dwelling Predators and Microbial Agents and Their Efficacy in Controlling Soil-Dwelling Stages of Western Flower Thrips, Frankleniella occidentalis. Biological Control, 92, 92-100.
https://doi.org/10.1016/j.biocontrol.2015.10.003

[23]   Wang, L., Huang, J., You, M. and Liu, B. (2005) Effect of Toxins from Two Strains of Verticillium lecanii (Hyphomycetes) on Bio-Attributes of Predatory Ladybeetle, Delphastus catalinae (Col., Coccinellidae). Journal of Applied Entomology, 129, 32-38.
https://doi.org/10.1111/j.1439-0418.2005.00929.x

[24]   Alma, C.R. (2005) Intraguild Interactions between Two Natural Enemies of the Greenhouse Whitefly, Trialieurodes vaporariorum (Hom.: Aleyrodidae), the Predator, Dicyphus hesperus (Het.: Miridae) and the Fungus Paecilomyces fumosoroseus. M.Sc. Thesis, Dept. of Biological Sciences, Simon Fraser University, Burnaby.

[25]   Pell, J.K., Pluke, R., Clark, S.J., Kenward, M.G. and Alderson, P.G. (1997) Interactions between Two Aphid Natural Enemies, the Entomopathogenic Fungus Erynia neoaphidis Remaudière & Hennebert (Zygomycetes: Entomophthorales) and the Predatory Beetle Coccinella septempunctata L. (Coleoptera: Coccinellidae). Journal of Invertebrate Pathology, 69, 261-268.
https://doi.org/10.1006/jipa.1996.4651

[26]   Roy, H.E., Pell, J.K., Clark, S.J. and Alderson, P.G. (1998) Implication of Predator Foraging on Aphid Pathogen Dynamics. Journal of Invertebrate Pathology, 71, 236-247.
https://doi.org/10.1006/jipa.1997.4736

[27]   Pell, J.K. and Vandenberg, J.D. (1998) Paecilomyces fumosoroseus, Convergent Ladybirds and Russian Wheat Aphid: Potential Interactions. Insect Pathogens and Insect Parasitic Nematodes. IOBC Bulletin, 21, 133.

[28]   Ormond, E.L., Thomas, A.P.M., Pell, J.K., Freeman, S.M. and Roy, H.E. (2011) Avoidance of a Generalist Entomopathogenic fungus by the Ladybird, Coccinella septempunctata. FEMS Microbiology Ecology, 77, 229-237.
https://doi.org/10.1111/j.1574-6941.2011.01100.x

[29]   Ormond, E.L., Thomas, A.P.M., Pell, J.K. and Roy, H.E. (2006) Overwintering Ecology of Coccinella septempunctata, Beauveria bassiana and Dinocampus coccinellae. In: Rossing, W.A.H., Eggenschwiler, L. and Poehling, H.-M., Eds., Working Group ‘‘Landscape Management for Functional Biodiversity’’, IOBC/WPRS Bulletin 29, 85-88.

[30]   Mills, N.J. (1981) The Mortality and Fat Content of Adalia bipunctata during Hibernation. Entomologia Experimentalis et Applicata, 30, 265-268.
https://doi.org/10.1111/j.1570-7458.1981.tb03109.x

[31]   Toledo, A.V., Remes Lincov, A.M.M. and Lopez Lastra, C.C. (2008) Host Range Findings on Beauveria bassiana and Metarhizium anisopliae (Ascomycota: Hypocreales) in Argentina. Boletin de la Sociedad Argentina de Botanica, 43, 211-220.

[32]   Cottrell, T.E. and Shapiro-Ilan, D.I. (2003) Susceptibility of a Native and an Exotic Lady Beetle (Coleoptera: Coccinellidae) to Beauveria bassiana. Journal of Invertebrate Pathology, 84, 137-144.
https://doi.org/10.1016/j.jip.2003.09.003

[33]   Harwood, J.D., Ricci, C., Romani, R., Weir, A. and Obrycki, J.J. (2006) Prevalence and Association of the Fungus, Hesperomyces virescens (Laboulbenialis: Laboulbeniaceae) on Coccinellid Hosts (Coleoptera: Coccinellidae) in Kentucky, USA. European Journal of Entomology, 103, 799-804.
https://doi.org/10.14411/eje.2006.109

[34]   Reddick, E.W., Cottrell, T.E. and Kidd, K.A. (2009) Natural Enemies of the Coccinellidae: Parasites, Pathogens and Parasitoids. Biological Control, 51, 306-312.
https://doi.org/10.1016/j.biocontrol.2009.05.008

[35]   Roy, H.E. and Cottrell, T.E. (2008) Forgotten Natural Enemies: Interactions between Coccinellids and Insect Parasitic Fungi. European Journal of Entomology, 105, 391-398.
https://doi.org/10.14411/eje.2008.049

[36]   Steenberg, T. and Harding, S. (2009) Entomopathogenic Fungi Recorded from the Ladybird, Harmonia axiridis. Journal of Invertebrate Pathology, 102, 88-89.
https://doi.org/10.1016/j.jip.2009.07.002

[37]   James, R.R., Shaffer, B.T., Croft, B. and Lighthart, B. (1995) Field Evaluation of Beauveria bassiana: Its Persistence and Effects on the Pea Aphid and Non-Target Coccinellids in Alfalfa. Bio-Control Science and Technology, 5, 425-437.
https://doi.org/10.1080/09583159550039620

[38]   Jacobson, R.J., Chandler, D., Fenlon, J. and Russell, K.M. (2001) Compatibility of Beauveria bassiana (Balsamo) Vuillemin with Amblyseius cucumeris Oudemans (Acarina: Phytoseiidae) to Control Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) on Cucumber Plants. Biocontrol Science and Technology, 11, 391-400.
https://doi.org/10.1080/09583150120055808

[39]   Cloyd, R.A., Timmons, N.R., Goebel, J.M. and Kemp, K.E. (2009) Effect of Pesticides on Adult Rove Beetle Atheta coriaria (Coleoptera: Staphylinidae) Survival in Growing Medium. Journal of Economic Entomology, 102, 1750-1758.
https://doi.org/10.1603/029.102.0504

[40]   Bayissa, W., Ekesia, S., Mohamed, S.A., Kayaab, G.P., Wagachab, J.M. and Maninia, N.K. (2016) Interactions among Vegetable-Infesting Aphids, the Fungal Pathogen Metarhizium anisopliae (Ascomycota: Hypocreales) and the Predatory Coccinellid Cheilomenes lunata (Coleoptera: Coccinellidae). Biological Science and Technology, 26, 274-290.
https://doi.org/10.1080/09583157.2015.1099148

[41]   Compos de Azevedo, A.G., Steinwender, B.M., Eilenberg, J. and Sigsgaard, L. (2017) Interactions among the Predatory Midge, Aphidoletis aphidimyza (Dip.: Cecidomyiidae), the Fungal Pathogen, Metarhizium brunneum (Ascomycota: Hypocreales) and Maize-Infesting Aphids in Greenhouse Mesocosms. Insects, 8, 44.
https://doi.org/10.3390/insects8020044

[42]   Roy, H.E. (1997) Interaction between Aphid Predators and the Entomopathogenic Fungus, Erynia neoaphidis. PHD Thesis, Nottingham University, Nottingham.

[43]   Roy, H.E. and Pell, J.K. (2000) Interactions between Entomopathogenic Fungi and Other Natural Enemies: Implication for Biological Control. Biocontrol Science and Technology, 10, 737-752.
https://doi.org/10.1080/09583150020011708

[44]   Emami, F., Alichi, M. and Minaei, K. (2013) Interaction between the Entomopathogenic Fungus, Beauveria bassiana (Ascomycota: Hypocreales) and the Parasitoid Wasp, Aphidius colemani Viereck (Hymenoptera: Braconidae). Journal of Entomological and Acarological Research, 45, 205-209.
https://doi.org/10.4081/jear.2013.e4

[45]   King, E.G. and Bell, V. (1978) Interaction between a Braconid, Microplitis croceipes, and a Fungus, Nomuraea rileyi, in Laboratory-Reared Bollworm Larvae. Journal of Invertebrate Pathology, 31, 337-340.
https://doi.org/10.1016/0022-2011(78)90225-2

[46]   Powell, W., Wilding, N., Brobyn, P.J. and Clark, S.J. (1986) Interference between Parasitoids [Hym.: Aphidiidae] and Fungi (Entomophthorales) Attacking Cereal Aphids. Entomophaga, 31, 293-302.
https://doi.org/10.1007/BF02373339

[47]   Van de Vier, M. and Degheee, D. (1996) Toxicity of the Fungal Pathogen, Paecilomysces fumosoroseus to the Greenhouse Whitefly, Trialeurodes vaporariorum and the Parasitoid, Encarsia formosa. The First Results of a Control Experiment in Glasshouses. OILB/SROP Bulletin: Proc. of the Meeting: Integrated Control in Glasshouses, Vienna, 20-25 May 1996, 191-194.

[48]   Askary, H. and Brodeur, J. (1999) Susceptibility of Larval Stage of the Aphid Parasitoid, Aphidius nigripes to the Entomopathogenic Fungus Verticillium lecanii. Journal of Invertebrate Pathology, 73, 129-132.
https://doi.org/10.1006/jipa.1998.4824

[49]   Rashki, M., Kharazi-Pakdel, A., Allahyari, H. and 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.
https://doi.org/10.1016/j.biocontrol.2009.04.016

[50]   Narouzi, Y. (2013) Compatibility of the Parasitoid, Aphidius matricareae with BotaniGard for the Control of Greenhouse Aphids. M.S. Thesis, Dept. Biological Science, Faculty of Science, Simon Fraser University, Burnaby.

[51]   Martins, I.C.F., Silva, R.J., Alencar, D.C.C., Silva, K.P. and Polanczyk, R.A. (2014) Interactions between the Entomopathogenic Fungi Beauveria bassiana (Ascomycota: Hypocreales) and the Aphid Parasitoid Diaeretiella rapae (Hymenoptera: Braconidae) on Myzus persicae (Hemiptera: Aphididae). Journal of Economic Entomology, 107, 933-938.
https://doi.org/10.1603/EC13542

[52]   Mahdavi, V., Saber, M., Rafiee-Dastjerdi, H. and Mehrvar, A. (2013) Susceptibility of the Hymenopteran Parasitoid, Habrobracon hebetor (Say) (Braconidae) to the Entomopathogenic Fungi, Beauveria bassiana and Metarhizium anisopliae Sorokin. Jordan Journal of Biological Sciences, 6, 17-20.
https://doi.org/10.12816/0000253

[53]   Jarrahi, A. and Safavi, S.A. (2016) Sub-Lethal Effects of Metarhizium anisopliae on Life Table Parameters of Habrobracon hebetor Parasitizing Helicoverpa armigera Larvae at Different Time Intervals. Bio-Control, 61, 167-175.
https://doi.org/10.1007/s10526-015-9707-y

[54]   Tamayo-Mejia, F., Tamezguera, P., Guzman-Franco, A.W. and Gomez-Flores, R. (2015) Can Beauveria bassiana and Tamarixia triozae (Hym.: Eulophidae) Be Used Together for Improved Biological Control of Bactericera cockerelli (Hemiptera: Triozidae)? Biological Control, 90, 42-48.
https://doi.org/10.1016/j.biocontrol.2015.05.014

[55]   Tamayo-Mejia, F., Tamez-Guerra, P., Guzman-Franco, A.W. and Gomez-Flores, R. (2016) Developmental Stage Affects Survival of the Ectoparasitoid, Tamarixia triozae Exposed to the Fungus Beauveria bassiana. Biological Control, 93, 30-36.
https://doi.org/10.1016/j.biocontrol.2015.11.006

[56]   Chow, A., Dunlap, C.A., Jackson, M.A., Flores, D., Patt, J.M. and Setamou, M. (2016) Oviposition Behavior and Survival of Tamarixia radiata (Hym.: Eulophidae), an Ectoparasitoid of Diaphorina citri (Hem.: Liviidae) on Hosts Exposed to the Entomopathogenic Fungus Isaria fumosorosea (Hypocreales: Cordycipitaceae) under Laboratory Conditions. Journal of Economic Entomology, 2016, 1-11.

[57]   Hall, R.A. (1981) The Fungus, Verticillium lecanii as a Microbial Insecticide against Aphids and Scales. In: Burges, H.D., Ed., Microbial Control of Pest and Plant Diseases, 1970-1980, Academic Press, San Diego.

[58]   Furlong, M.J. and Pell, J.K. (2000) Conflicts between a Fungal Entomopathogen Zoophthora radicans and Two Larval Parasitoids of the Diamond-Back Moth. Journal of Invertebrate Pathology, 76, 85-94.
https://doi.org/10.1006/jipa.2000.4943

[59]   Furlong, M.J. and Pell, J.K. (1996) Interaction between the Fungus Entomopathogen Zoophthora radicans Brefeld (Entomophthorales) and Two Hymenopteran Parasitoids Attacking the Diamond-Back Moth, Plutella xylostella. Journal of Invertebrate Pathology, 68, 15-21.
https://doi.org/10.1006/jipa.1996.0053

[60]   Aristizabal, I., Pardey, A. and Cordoba, B.C. (1995) Effect of Beauvaria bassiana and Metarhizium anisopliae on the Coffee Berry Borer Parasitoid, Cephalonomia stephannoderis. Revista Colombiana de Entomologia, 21, 199-204.

[61]   Danfa, A. and Van den Valk, H.C.H.G. (1999) Laboratory Testing of Metarhizium spp. and Beauveria bassiana on Sahelian Non-Target Arthropods. Bio-Control Science and Technology, 9, 187-198.
https://doi.org/10.1080/09583159929776

[62]   Madurappulige, P. (2005) Effect of Beauveria bassiana on Diadegma semiclausum (Ichneumonidae), a Parasitoid of Plutella xylostella (Lep.: Yponomeutidae). PhD Thesis, Lincoln University, Lincoln, 171 p.

[63]   Rannback, L.M., Cotes, B., Anderson, P., Rämert, B. and Meyling, N.V. (2014) Mortality Risk from Entomopathogenic Fungi Affects Oviposition Behavior in the Parasitoid Wasp Trybliographa rapae. Journal of Invertebrate Pathology, 124, 78-86.
https://doi.org/10.1016/j.jip.2014.11.003

[64]   Baverstock, J., Clark, S.J., Alderson, P.G. and Pell, J.K. (2009) Intraguild Interactions between the Fungus, Pandora neoaphidis and an Aphid Predator at Population Scales. Journal of Invertebrate Pathology, 102, 167-172.
https://doi.org/10.1016/j.jip.2009.07.014

[65]   Akalach, M., Fernandez-Garcia, E. and Moore, D. (1992) Interaction between Rastrococcus invadens (Hom.: Pseudococcidae) and Two Natural Enemies. Entomophaga, 37, 99-106.
https://doi.org/10.1007/BF02372978

[66]   Mesquita, A.L.M., Lacey, L.A. and Leclant, F. (1997) Individual and Combined Effects of the Fungus, Paecilomyces fumosoroseus and Parasitoid, Aphelinus asychis Walker (Hym., Aphelinidae) on Confined Populations of Russian Wheat Aphid, Diuraphis noxia (Mordvilko) (Hom., Aphididae) under Field Conditions. Journal of Applied Entomology, 121, 155-163.
https://doi.org/10.1111/j.1439-0418.1997.tb01386.x

[67]   Jaber, R. and Araj, S.E. (2018) Interactions among Endophytic Fungal Entomopathogens (Ascomycota: Hypocreales), the Green Peach Aphid Myzus persicae Sulzer (Homoptera: Aphididae), and the Aphid Endoparasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Biological Control, 116, 53-61.
https://doi.org/10.1016/j.biocontrol.2017.04.005

[68]   Mohammed, A.A. and Hatcher, P.E. (2017) Combining Entomopathogenic Fungi and Parasitoids to Control the Green Peach Aphid, Myzus persicae. Biological Control, 110, 44-55.
https://doi.org/10.1016/j.biocontrol.2017.03.012

[69]   Brobyn, P.J., Clark, S.J. and Wilding, N. (1988) The Effect of Fungus Infection of Metopolophium dirhodum [Hom.: Aphididae] on the Oviposition Behaviour of the Aphid Parasitoid Aphidius rhopalosiphi [Hym.: Aphidiidae]. Entomophaga, 33, 333-338.
https://doi.org/10.1007/BF02372623

[70]   Tounou, A.K., Agboka, A., Poehling, H.M., Ranpack, K. and Borgemeister, C. (2003) Evaluation of the Entomopathogenic Fungi Metarhizium anisopliae and Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) for Control of the Green Leafhopper Empoasca decipiens (Homoptera: Cicadellidae) and Potential Side Effects on the Egg Parasitoid Anagrus atomus (Hymenoptera: Mymaridae). Biocontrol Science and Technology, 13, 715-728.
https://doi.org/10.1080/09583150310001606534

[71]   Fransen, J.J. and 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.
https://doi.org/10.1111/j.1570-7458.1993.tb01747.x

[72]   Lord, J. (2001) Response of the Wasp Cephalonomia tarsalis (Hymenoptera: Bethylidae) to Beauveria bassiana (Hyphomycetes: Moniliales) as Free Conidia or Infection in Its Host, the Sawtoothed Grain Beetle, Oryzaephilus surinamensis (Coleoptera: Silvanidae). Biological Control, 21, 300-304.
https://doi.org/10.1006/bcon.2001.0942

 
 
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