ISOLATION OF ENTOMOPATHOGENIC FUNGI FROM TURKEY SOIL AND TESTING OF DIFFERENT DOSES ON GALLERIA MELLONELLA (LEPIDOPTERA: PYRALIDAE)

Abstract

Isolation of biological control agents which would be used with pests control could be done with different methods. The most sensitive of these methods is the insect bait method. Besides, it is known that the effects of different entomopathogen fungi isolates, which would be used as biological control agents varies in different hosts. In this study, since the target pest organism is the larval period of Galleria mellonella Linnaeus (Lepidoptera: Pyralidae), this pest is used for insect bait method and as a result of isolation from 180 soil samples, 48 Beauveria bassiana Bals.-Criv. Vuill. (Hypocreales: Cordycipitaceae) and 1 Beauveria brongniartii (Sacc.) Petch (Hypocreales: Cordycipitaceae) was detected but Metarhizium spp. wasn’t detected. Furthermore, it is known that the precise determination of the entomopathogen fungi isolates, plays a crucial role in the success of a biological control program. In this study, as biological control agent, four concentrations (1x104, 1x105, 1x106 and 1x107 conidiya/ml) of 10 different isolates of Beauveria bassiana Bals.-Criv. Vuill. (Hypocreales: Cordycipitaceae), which were obtained from soils of our country and a standard strain from Denmark were applied to Galleria mellonella Linnaeus (Lepidoptera: Pyralidae) larvae. When Lethal times (LT50) compared, it was found that the highest concentration of each isolates was also the most effective one.

Keywords

• Biological control
• Entomoğathogen fungi
• Insect bait method
• Beauveria bassiana
• Galleria mellonella

References

1. Van Driesche, R.G., Bellows Jr., T.S., Biological Control, An International Thomson Publishing, New York, 1996.
2. Bourguet, D., and Guillemaud, T., The hidden and external costs of pesticide use, Sustainable agriculture reviews, 19 (2016), 35–120.
3. Alagesan A., Padmanaban B., Tharani G., Jawahar S., Manivannan S., An assessment of biological control of the banana pseudostem weevil Odoiporus longicollis (Olivier) by entomopathogenic fungi Beauveria bassiana, Biocatalysis and Agricultural Biotechnology, 20 (2019), https://doi.org/10.1016/j.bcab.2019.101262.
4. Bottrell, D. G., and P.L. Adkisson, Cotton insect pest management. Annual Review of Entomology, 22 (1977), 451-481.
5. Smith, R. and Watson, A., Working with nature to improve the environment and profitability of irrigated cotton production at ‘Kilmarnock’, Namoi Valley, New South Wales, Ecological Management & Restoration, 19(S1) (2018), 63-72.
6. Zélé, F., Altıntaş, M., Santos, I., Cakmak, I., Magalhães, S., Inter‐ and intraspecific variation of spider mite susceptibility to fungal infections: Implications for the long‐term success of biological control, Ecology and Evolution, 10(1447) (2020), 1-13.
7. Attia, S., Grissa, K.L., Lognay, G., Bitume, E., Hance, T., & Mailleux, A. C. A review of the major biological approaches to control the worldwide pest Tetranychus urticae (Acari: Tetranychidae) with special reference to natural pesticides biological approaches to control, Tetranychus urticae. Journal of Pest Science, 86 (2013), 361–386.
8. Monzon, A.J., Guharay, F., Kingen, I., Natural occurrence of Beauveria bassiana in Hypothenemus hampei (Coleoptera: Curculionidae) populations in unsprayed coffee fields, Journal of Invertebrate Pathology, 97 (2008), 134-141.

9. Parolin, P., Bresch, C., Desneux, N., Brun, R., Bout, A., Boll, R., & Poncet, C., Secondary plants used in biological control: A review. International Journal of Pest Management, 58 (2012), 91–100.
10. Wekesa, V.W., Maniania, N.K., Knapp, M., Boga, H.I., Pathogenicity of Beauveria bassiana and Metarhizium anisopliae to the tobacco spider mite Tetranychus evansi, Experimental and Applied Acarology, 36 (2005), 41- 50.
11. Garkoti, A., Kumar, V., Tripathi, H., Control of wilt disease of lentil through bio control agents and organic amendments in Tarai region of Uttarakhand, India, Journal of Environmental Biology, 35 (2014), 1067–1070.
12. Mukherjee, A., Debnath, P., Ghosh, S.K., Biological control of papaya aphid (Aphis gossypii Glover) using entomopathogenic fungi, Vegetos 33 (2020), 1–10, https:// doi.org/10.1007/s42535-019-00072-x.
13. Pan X.Y. and Zhang F., Advances in Biological Control of the German cockroach, Blattella germanica (L.), Biological Control, 142 (2019), 13, https://doi.org/10.1016/ j.biocontrol.2019.104104.
14. Oğurlu, İ., Biyolojik Mücadele, SDÜ Basımevi, Isparta, Turkey, 2000.
15. Kamp, A.M., and Bidochka, M.J., Conidium production by insect pathogenic fungi on commercially available agars, Letters in Applied Microbiology, 35 (2002), 74–77.
16. Trudel, R., Lavallee R., Guertin, C., Cote, C., Todorova, S.I., Alfaro, R., and Kope, H., Potential of Beauveria bassiana (Hyphomycetes: Moniliales) for controlling the white pine weevil, Pissodes strobi (Col., Curculionidae). Journal of Applied Entomology, 131(2) (2007), 90-97.
17. De La Rosa, W., Lopez F.L., and Liedo, P., Beauveria bassiana as a pathogen of the mexican fruit fly (Diptera: Tephritidae) under laboratory conditions, Journal of Economic Entomology, 95(1) (2002), 36-43.
18. Gutiérrez-Cárdenas O.G., Cortez-Madrigal H., Malo E.A., Nord R., Physiological and Pathogenical Characterization of Beauveria bassiana and Metarhizium anisopliae Isolates for Management of Adult Spodoptera frugiperda, Southwestern Entomologist, 44(2) (2019), 409-421.
19. Eken, C., Tozlu, G., Dane, E., Çoruh, S., and Demirci, E., Pathogenicity of Beauveria bassiana (Deuteromycotina: Hypomycetes) to larvae of the small poplar longhorn beetle, Saperda populnea (Coleoptera: Cerambycidae), Mycopathologia, 162 (2006), 69-71.
20. Van Lenteren J.C., Bolckmans K.. Köhl J., Ravensberg W. J., Urbaneja A., Biological control using invertebrates and microorganisms: plenty of new opportunities, BioControl, 63 (2018), 39 – 59.
21. Doolotkeldieva T., Bobusheva S., Kulmanbetova A., Zholdoshbekova S., Kyzy A.A.,Characterization of Beauveria bassiana isolates from Kyrgyzstan, Journal of Invertebrate Pathology, 167 (2019), 107243.
22. Glare, T., Caradus, J., Gelernter, W., Jackson, T., Keyhani, N., Kohl, J., Marrone, P., Morin, L., Stewart, A., Have biopesticides come of age?, Trends in Biotechnology, 30 (2012), 250–258.
23. Hicks, B.J., Watt, A.D., Cosens, D., The potential of Beauveria bassiana (Hyphomycetes: Moniliales) as a biological control agent against to pine beauty moth, Panolis flammea (Lepidoptera: Noctuidae), Forest Ecology and Management, 149 (2001), 275-281.
24. Azmi W.A., Sulaiman Z.A., Ishak I., Kin P.K., Lin G.L.E., Addis S.N.K., Virulence evaluation of entomopathogenic fungi to subterranean termites, Globitermes sulphureus (Insecta: Isoptera), Malaysian Journal of Microbiology, 12(6) (2016), 492–497.
25. Ibrahim R.A., Laboratory evaluation of entomopathogenic fungi, commercial formulations, against the rhinoceros beetle, Oryctes agamemnon arabicus (Coleoptera: Scarabaeidae), Egyptian Journal of Biological Pest Control, 27(1) (2017), 49–55.
26. Mondal, S., Baksi, S., Koris, A., Vataig, G., Journey of enzymes in entomopathogenic fungi. Pacific Science Review A, Natural Science and Engineering, 18 (2016), 85–99.
27. Saleem, A.R. and Ibrahim, R.A., Assessment of the virulence and proteolytic activity of three native entomopathogenic fungi against the larvae of Oryctes agamemnon (Burmeister) (Coleoptera: Scarabaeidae), Egyptian Journal of Biological Pest Control, 29(21) (2019), 1-8.
28. Beron, C.M., and Diaz, B.M., Pathogenicity of hyphomycetous fungi against Cyclocephala signaticollis, BioControl, 50 (2005), 143-150.
29. Vilcinskas A., Evolutionary ecology of parasitic fungi and their host insects, Fungal Ecology, 38 (2019), 12-20.
30. De La Cruza, M.T., Madrigalb, H.C., Garcíac, C.F.O., Garcíaa, S.C., de la Cruz, M.P., Monosporic strains of Metarhizium anisopliae and its pathogenicity to Galleria mellonella in Tabasco, Mexico, Revista Mexicana de Ciencias Pecuarias, 5(2) (2014), 171-180.
31. Keppanan, R., Sivaperumal, S., Aguila, L.C.R., Hussain, M., Bamisile, B.S., Dash, C.K., Wang, L., Isolation and characterization of Metarhizium anisopliae TK29 and its mycoinsecticide effects against subterranean termite Coptotermes formosanus, Microbial Pathogenesis, 123 (2018), 52-59.
32. Keppanan, R., Sivaperumal, S., Kanta, D.C., Akutse, K.S., Wang, L., Molecular docking of protease from Metarhizium anisopliae and their toxic effect against model insect Galleria mellonella, Pesticide Biochemistry and Physiology, 138 (2017), 8–14.
33. Meyling, N.V., Methods for isolation of entomopathogenic fungi from the soil environment. Laboratory manual. (2007), http://orgprints.org/11200.
34. Asensio, L., Carbonell, T., Lopez-Jimenez, J.A., and Lopez-Llorca, L.V., Entomopathogenic fungi in soils from Alicante province, Spanish Journal of Agricultural Research, 1(3) (2003), 34-75.
35. Ali-Shtayeh, M.S., Mara’i, A.B.M., and Jamous, R.M., Distribution, occurrence and characterization of entomopathogenic fungi in agricultural soil in the Palestinian area, Mycopathologia, 156 (2002), 235- 244.
36. Botelho, A.B.R.Z., Alves-Pereira, A., Prado, R.C., Zucchi, M.I., Júnior, I.D., Metarhizium species in soil from Brazilian biomes: a study of diversity, distribution, and association with natural and agricultural environments, Fungal Ecology, 41(2019), 289-300.
37. Keller, S., Kessler, P., and Schweizer, C., Distribution of insect pathogenic soil fungi in Switzerland with special reference to Beauveria brongniartii and Metharhizium anisopliae, BioControl, 48 (2003), 307–319.
38. Kessler, P., Enkerli, J., Schweizer, C., and Keller, S., Survival of Beauveria brongniartii in the soil after application as a biocontrol agent against the European cockchafer Melolontha melolontha, BioControl, 49 (2004), 563–581.
39. Ramos, Y., Portal, O., Lysøe, E., Meyling, N.V., Klingen, I., Diversity and abundance of Beauveria bassiana in soils, stink bugs and plant tissues of common bean from organic and conventional fields, Journal of Invertebrate Pathology,150 (2017), 114-120.
40. Sonia, R., Peveling, R., Nagel, P., Keller, S., The natural distribution of the entomopathogenic fungus Metarhizium anisopliae in different regions and habitat types in Switzerland, IOBC Bulletein, 28(2) (2005), 185-188.
41. Hazır, S., Keskin, N., Stock, S.P., Kaya, H.K., and Özcan, S., Diversity and distribution of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in Turkey, Biodiversity and Conservation, 12 (2003), 375–386.
42. Zimmermann, G., The Galleria bait method for detection of entomopathogenic fungi in soil, Journal of Applied Entomology, 102 (1986), 213-215.
43. Chandler, D., Hay, D., Reid, A.P., Sampling and occurrence of entomopathogenic fungi and nematodes in UK soils, Applied Soil Ecology, 5 (1997), 133-141.
44. Klingen, I., Meadow, R., and Aandal, T., Mortality of Delia floralis, Galleria mellonella and Mamestra brassicae with insect pathogenic hyphomycetous fungi, Journal of Applied Entomology, 126 (2002), 231-237.
45. Meyling, V.M., and Eilenberg, J., Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: Potential for conservation biological control, Biological Control, 43 (2007), 145-155.
46. Kwadha, C.A., Ong’amo, G.O., Ndegwa, P.N., Raina, S.K., Fombong, A.T., The biology and control of the greater wax moth, Galleria mellonella, Insects, 8 (2017), 61–78.
47. Mietkiewski, R.T., Pell, J.K., Clark, S.T., Influence of pesticide use on the natural occurence of entomopathogenic fungi in arable soils in the UK field and laboratory comparisons, Biocontrol Science and Technology, 7 (1997), 565-575.
48. Zimmermann, G., Suggestion for a standardized method for reisolation of entomopathogenic fungi from soil using the bait method, IOBC Bulletein, 21(4) (1998), 289.
49. Hughes, W.O.H., Thomsen, L., Eilenberg, J., and Boomsma, J.J., Diversity of entomopathogenic fungi near leaf-cutting ant nests in a neotropical forest, with particular reference to Metarhizium anisopliae var. anisopliae, Journal of Invertebrate Pathology, 85 (2004), 46–53.
50. Dhoj, GC, Y., Keller, S., Nagel, P., Kafle, L., Virulence of Metarhizium anisopliae and Beauveria bassiana Against Common White Grubs in Nepal, Formosan Entomologist, 28 (2008), 11-20.
51. Bidochka, M.J., Kasperski, J.E., and Wild, G.A.M., Occurrence of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana in soils from temperate and near-northern habitats, Canadian Journal of Botany, 76(7) (1998), 1198-1204.
52. Keppanan, R., Akutse, K.S., Sivaperumal, S., Wang, L., Determination and characterization of destruxin production in Metarhizium anisopliae Tk6 and formulations for Aedes aegypti mosquitoes control at the field level, Toxicon 120 (2016), 89–96.
53. Lezama-Gutierrezet, R., Hamm, J.J., Molina-Ochoa, J., Lopez-Edwards, M., Pescador-Rubio, A., Gonzalez-Ramirez, M., and Styer, E.L., Occurrence of entomopathogens of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Mexican states of Michoacan, Colima, Jalisco and Tamaulipa, Florida Entomologist, 84(1) (2001), 23-30.
54. Quesada-Moraga, E., Navas-Cortes, J.A., Maranhao, E.A.A., Ortiz-Urquiza, A., Santiago-Alvarez, C., Factors affecting the occurrence and distribution of entomopathogenic fungi in natural and cultivated soils, Mycological Research, 111 (2007), 947-966.
55. De La Rosa, W., Segura H.R., Barrera, J.F., Williams, T., Laboratory evaluation of the impact of entomopathogenic fungi on Prorops nasuta (Hymenoptera: Bethylidae), a parasitoid of Coffee Berry Borer, Environmental Entomology, 29 (2000), 126-131.
56. Vivekanandhan, P., Bedini, S., Shivakumar, M.S., Isolation and identification of entomopathogenic fungus from Eastern Ghats of South Indian forest soil and their efficacy as biopesticide for mosquito control, Parasitology International, 76 (2020), https://doi.org/10.1016/j.parint.2020.102099.
57. Bello, G.D., Padin, S., Lastra, C.L., Fabrizio, M., Laboratory evaluation of chemical biological control of rice weevil (Sitophilus oryzae L.) stored in grains, Journal of stored Products Research, 37(1) (2000), 77-84.
58. Saharayaj, K., and Namasivayam S.K.R., Mass production of entomopathogenic fungi using agricultural products and by products, African Journal of Biotechnology, 7(12) (2008), 1907-1910.
59. Vänninen, I., Husberg, G.B., Hokkanen, H.M.T., Occurence of entomopathogenic fungi and entomoparasitic nematodes in cultivated soils in Finland, Entomologica Fennica, 53 (1989), 65-71. [ Vänninen, I., Hokkanen, H., Tyni-Juslin, J., Attemtps to control cabbage root flies Delia radicum L. and Delia floralis (Fall.) (Dipt.) Anthomyiidae, with entomopathogenic fungi; Laboratory and greenhouse tests, Journal of Applied Entomology, 123 (1999), 107-113.
60. Abdullah S.K., Mustafa R.A., Assaf L.H., Isolation of Entomopathogenic and Opportunistic Fungi from Soil in Duhok Province,Kurdistan Region of Iraq by Different Selective Isolation Media, Journal of Biology Agriculture and Healthcare, 5(4) (2015), 73-79.
61. Chase, A.R., Osborne, L.S., and Ferguson, V.M., Selective isolation of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae from an artificial potting medium, Florida Entomologist, 69(2) (1986), 285-292.
62. Goettel, M.S., and Inglis, G.D., Fungi: Hyphomycetes in Manual of Techniques in Insect Pathology (L. Lacey ed), Academic Press, San Diego, CA., 1997.
63. Shimazu, M., Sato, H., and Maehara, N., Density of the entomopathogenic fungus, Beauveria bassiana Vuillemin (Deuteromycotina: Hyphomycetes) in forest air and soil, Applied Entomology and Zoology, 37(1) (2002), 19–26.
64. Hasenekoğlu, İ., Toprak mikrofungusları, Atatürk Üniversitesi Yayınları, No:689, Kazım Karabekir Eğitim Fakültesi Yayınları, No:II, Cilt:II, 1991.
65. Masoudi, A., Koprowski, J.L., Bhattarai, U.R., Wang, D., Elevational distribution and morphological attributes of the entomopathogenic fungi from forests of the Qinling Mountains in China. Applied Microbiology and Biotechnology, 102 (2018), 1483–1499. https://doi.org/10.1007/s00253-017-8651-4.
66. Zimmermann, G., Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii, Biocontrol Science and Technology, 17(5/6), (2007), 553.
67. Abebe, H., Potential of entomopathogenic fungi for the control of Macrotermes subhyalinus (Isoptera: Termitidae), Ph.D. thesis, Addis Ababa University, International Institute of Tropical Agriculture (IITA), Ethiopia, (2002).
68. Hu, S. and Bidochka, M.J., DNA methyltransferase implicated in the recovery of conidiation, through successive plant passages, in phenotypically degenerated Metarhizium, Applied Microbiology and Biotechnology, (2020), https://doi.org/10.1007/s00253-020-10628-6.
69. Butt, T.M., and Goettel, M.S., Bioassays of entomopathogenic fungi. Bioassays of entomopathogenic microbes and nematodes. Navon, A., and Ascher, K.R.S. (eds.), CABI, New York, 2002.
70. Studdert, J.P., and Kaya, H.K., Effect of water potential, temperature and clay coating on survival of Beauveria bassiana conidia in Loam and Peat soil, Journal of Invertebrate Pathology, 55 (1990a), 417-427.
71. Oudor, G.I., Smith S.M., Chandi, E.A., Karanja, L.W., Agano, J.O., Moore, D., Occurrence of Beauveria bassiana on insect pests of stored maize in Kenya, Journal of Stored Products Research, 36 (2000), 177-185.
72. Zamani, Z., Aminaee, M. M., & Khaniki, G. B., Introduction of Beauveria bassiana as a biological control agent forTribolium castaneumin Kerman province, Archives Of Phytopathology And Plant Protection, 46(18) (2013), 2235–2243.
73. Draganova, S., Takov, D., Doychev, D., Bioassays with isolates of Beauveria bassiana (Bals.) Vuill. and Paecilomyces farinosus (Holm.) Brown & Smith against Ips sexdentatus Boerner and Ips acuminatus Gyll. (Coleoptera: Scolytidae), Plant Science, 44 (2007), 24 – 28.
74. Humber, R.A., Entomopathogenic Fungal Identification. APS/ESA Joint Annual Meeting, 8-12 November, Las Vegas, NV., 1998.
75. Imoulan, A., Li Y., Wang, W.J., El Meziane, A., Yao, Y.J., New record of Beauveria pseudobassiana to Morocco. Mycotaxon, 131 (2016), 913–923.
76. Luz, C., Silva, I.G., Cordeiro, C.M.T., Tigano, M.S., Sporulation of Beauveria bassiana on cadavers of Triatoma infestans after infection at different temperatures and doses of inoculum, Journal of Invertebrate Pathology, 73 (1999), 223-225.
77. Kreutz, J., Vaupe, O., and Zimmermann, G., Efficacy of Beauveria bassiana (Bals.) Vuill. Against the spruce bark beetle, Ips typographus L., in the laboratory under various conditions, JEN, 128(6) (2004), 384-389.
78. Akyol, E., Korkmaz, A., Peteklerin büyük mum güvesi (Galleria mellonella L.)’ne karşı korunmasında -5 °C soğuk uygulamasının etkisi, Uludağ Arıcılık Dergisi. 8(1) (2008), 26-29.
79. Haewoon, O., Young, M., Chang, Y., Developing periods of damage patterns of combs by the wax moth, Galleria mellonella, Journal of Apiculture Research, 10 (1995), 5–10.
80. Hussein, K.A., Abdel-Rahman, M.A.A., Abdel-Mallek, A.Y., El-Maraghy, S. S., Joo, J. H., Pathogenicity of Beauveria bassiana and Metarhizium anisopliae against Galleria mellonella, Phytoparasitica, 40 (2012), 117–126.
81. Mohamed, H.F., Sileem, T.M., El-Naggar, S.E.M., El-Mohsen, Sweilem, M.A., Ibrahim, A.A.M., Al-azem, O. E. S. A., & El-khawaga, A. E. R., Effect of gamma irradiation and/or certain entomopathogenic fungi on the larval Mortality of Galleria mellonella L., Egyptian Journal of Biological Pest Control, 28(95) (2018).
82. Akhurst, R., and Smith, K., Regulation and Safety. Entomopathogenic Nematology. Gaugler, R. (ed), CABI, Wallingford UK, (2002), 311-332.
83. Barker, C.W., and Barker, G.M., Generalist entomopathogens as biological indicators of deforestation and agricultural land use impacts on Waikato soils, New Zealand Journal of Ecology, 22(2) (1998), 189-196.
84. Gürlek, S., Sevim, A., Sezgin, F.M., Sevim, E., Isolation and characterization of Beauveria and Metarhizium spp. from walnut fields and their pathogenicity against the codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), Egyptian Journal of Biological Pest Control, 28(50) (2018), https://doi.org/10.1186/s41938-018-0055-y.
85. Imoulan, A., Wei, X.D, Wang, W.J., Li, Y., Lu, W.L., Yang, R. H., ... & Yao, Y. J., Distribution and genetic diversity of Beauveria species at different soil depths in natural and agricultural ecosystems, Mycological Progress, 18 (2019), 1241–1252.
86. Meyling, N.V., and Eilenberg J., Occurrence and distribution of soil borne entomopathogenic fungi within a single organic agroecosystem. Agriculture Ecosystems and Environment, 113 (2006), 336-341.
87. Tkaczuk, C., Tipping, C., Majchrowska-Safaryan, A., Król A., Wyrzykowska M., The occurrence of entomopathogenic fungi in soils from apple orchards protected in different farming systems, Fresenius Environmental Bulletin, 28 (2019), 7906-7914.
88. Sahin, H., Çam Kesetırtılı (Thaumetopoea pityocampa (Den and Schiff)) (Lepidopters: Thaumetopoeidae) ’na karşı farklı entomopatojen fungus izolatlarının etkilerinin araştırılması. Yüksek Lisans Tezi. Kahramanmaraş Sütçü İmam Üniversitesi Fen Bilimleri Enstitüsü, Kahramanmaraş, Turkey, 2006.
89. Sevim, A., Demir, I., Höfte, Humber R. A., Demirbag Z., Isolation and characterization of entomopathogenic fungi from hazelnut-growing region of Turkey. BioControl 55 (2010), 279–297 https://doi.org/10.1007/s10526-009-9235-8.
90. Sun, B.-D., Yu, H.-Y., Chen, A.J., Liu, X.-Z., Insect-associated fungi in soils of field crops and orchards, Crop Protection, 27 (2008), 1421-1426.
91. Vänninen, I., Distribution and occurrence of four entomopathogenic fungi in Finland: Effect of geographical location, habitat type and soil type, Mycological Research, 100 (1995), 93-101.
92. Brownbridge, M., Costa, S., Jaronski, S.T., Effects of in Vitro Passage of Beauveria bassiana on Virulence to Bemisia argentifolii, Journal of Invertebrate Pathology, 77, (2001), 280-283.
93. Luz, C., Rocha, L.F.N., Nery G.V., Detection of Entomopathogenic Fungi in Peridomestic Triatomine-Infested Areas in Central Brazil and Fungal Activity Against Triatoma infestans (Klug) (Hemiptera: Reduviidae), Neotropical Entomology, 33(6), (2004), 783-791.
94. Bugeme, D.M., Maniania, N.K., Knapp, M., Boga, H.I., Effect of temperature on virulence of Beauveria bassiana and Metarhizium anisopliae isolates to Tetranychus evansi, Experimental and Applied Acarology, 46 (2008), 275- 285.
95. Pliz, C., Wegensteiner, R., and Keller, S., Selection of entomopathogenic fungi for the control of the western corn rootworm Diabrotica virgifera virgifera, Journal of Applied Entomology, 131(6) (2007), 426-431.
96. Ozdemir, I.O., Tuncer, C., Erper, I., Kushiyev, R., Efficacy of the entomopathogenic fungi; Beauveria bassiana and Metarhizium anisopliae against the cowpea weevil, Callosobruchus maculatus F. (Coleoptera: Chrysomelidae: Bruchinae), Egyptian Journal of Biological Pest Control, 30(24) (2020), https://doi.org/10.1186/s41938-020-00219-y.
97. Kim, J.J., Kim K.C., Selection of a highly virulent isolate of Lecanicillium attenuatum against cotton aphid, Journal of Asia-Pacific Entomology, 11 (2008), 1-4.
98. Santaro, P.H., Neves, P.M.O.J., Alexandre, P.M., Sartori, D., Alves, L.F.A., Fungaro, M.H.P., Selection of Beauveria bassiana isolates to control Alphitobius diaperinus, Journal of Invertebrate Pathology, 97 (2008), 83-90.
99. Yucel, B., Gozuacik, C., Gencer, D., Demir İ., Demirbağ Z., Determination of fungal pathogens of Hypera postica (Gyllenhall) (Coleoptera: Curculionidae): isolation, characterization, and susceptibility, Egyptian Journal of Biological Pest Control, 28(39) (2018), https://doi.org/10.1186/s41938-018-0043-2.
100. Dogan, Y. O., Hazir, S., Yildiz, A., Butt, T.M., Cakmak I., Evaluation of entomopathogenic fungi for the control of Tetranychus urticae (Acari: Tetranychidae) and the effect of Metarhizium brunneum on the predatory mites (Acari: Phytoseiidae), Biological Control, 111 (2017), 6-12, https://doi.org/10.1016/ j.biocontrol.2017.05. 001.
101. Wu, S., Xie, H., Li, M., Xu, X., Lei, Z., Highly virulent Beauveria bassiana strains against the two-spotted spider mite, Tetranychus urticae, show no pathogenicity against five phytoseiid mite species, Experimental and Applied Acarology, 70 (2016), 421–435. http://dx.doi.org/10.1007/s10493-016-0090-x.
102. Vu, V.H., Hong, S.I., and., Kim, K., Selection of Entomopathogenic Fungi for Aphid Control, Journal of Bioscience and Bioengineering, 104(6) (2007) 498-505.
103. Oreste, M., Bubici, G., Poliseno, M., Triggiani, O., Tarasco, E., Pathogenicity of Beauveria bassiana (Bals.-Criv.) Vuill. And Metarhizium anisopliae (Metschn.) Sorokin against Galleria mellonella L. And Tenebrio molitor L. In laboratory assays. Redia 95 (2012), 43–48.
104. Sohrabi, F., Jamali, F., Morammazi, S., Saber, M., Kamita, S.G., Evaluation of the compatibility of entomopathogenic fungi and two botanical insecticides tondexir and palizin for controlling Galleria mellonella L. (Lepidoptera: Pyralidae), Crop Protection, 117 (2019), 20-25, https://doi.org/10.1016/j.cropro.2018.11.012.
105. Liu, H., Skinner, M., Parker, B.L., Brownbridge, M., Pathogenicity of Beauveria bassiana; Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) and other entomopathogenic fungi against Lygus lineolaris (Hemiptera: Miridae), Journal of Economical Entomology, 95(4) (2002), 675-681.
106. Miranpuri, G.S., and Khachatourians, G.C, 1995, Entomopathogenicity of Beauveria bassiana toward flea beetles, Phyllotreta crucifera goeze (Col., Chrysomellidae), Journal of Applied Entomology, 119 (1995), 167-170.
107. Mukherjee A., Debnath P., Ghosh S. K., Medda P. K., Biological control of papaya aphid (Aphis gossypii Glover) using entomopathogenic fungi, Society for Plant Research, 33 (2019), 1-10.
108. Studdert, J.P., and Kaya H.K., Water potential, temperature and soil type on the formation of Beauveria bassiana soil colonies, Journal of Invertebrate Pathology, 56 (1990b), 380-386.
109. Chelico, L., Haughian, J.L., and Khachatourians, G.G., Nucleotide excision repeair and photoreactivation in the entomopathogenic fungi Beauveria bassiana, Beauveria brongniartii, Beauveria nivea, Metarhizium anisopliae, Paecilomyces farinosus and Verticillium lecanii, Journal of Applied Microbiology, 100 (2006), 964-972.
110. Fernandes, E.K.K., Rangel, D.E.N., Moraes, A.M.L., Bittencourt, V.R.E.P., Roberts, D.W., Variability in tolerance to UV-B radiation among Beauveria spp. isolates, Journal of Invertebrate Pathology, 96 (2007), 237-243.
111. Wojda, I., Kowalski, P., Jakubowicz, T., Humoral immune response of Galleria mellonella larvae after infection by Beauveria bassiana under optimal and heat-shock conditions, Journal of Insect Physiology, 55 (2009), 525-531.