Investigating on the potential of local isolates of entomopathogenic fungi as biological control agents against greenhouse whitefly Trialeurodes vaporariorum

Document Type : Research Paper

Authors

Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extention

Abstract

The initial step to mass production and commercialization of native entomopathogenic fungal isolates includes collection as well as evaluation of their pathogenesis on the pest. This research aims to investigate the pathogenicity of 36 local fungal isolates collected from the Iranian Research Institute of Plant Protection, Tehran, Iran against greenhouse whitefly Trialeurodes vaporariorum. Due to the variation of the collected isolates volume, a preliminary screening test carried out on the fourth instars of a model insect Galleria mellonella. Based on the obtained results, the Beauveria bassiana A1–1 isolate showed the highest mortality with an average of 75%, followed by IRAN1787C, IRAN1751C, IRAN1395C, IRAN428C and IRAN441C with mean mortality rates of 57.50, 55, 52.50, 50 and 45%, respectively. Subsequently, the isolates were selected for evaluation of vegetative growth, sporulation and bioassay tests on greenhouse whitefly. In the bioassay test, five concentrations of the isolates (104, 105, 106, 107 and 108 conidia/ml) were tested on the third–instar of whitefly nymphs, and then the parameters LC50 and LT50 of the isolates were calculated. The highest vegetative growth rate belonged to IRAN428C, IRAN1395C, A1–1, IRAN1787C, IRAN441C and IRAN1751C isolates while the highest sporulation rate belonged to IRAN1787C, A1–1, IRAN428C, IRAN1395C, IRAN441C and IRAN1751C, respectively. The results showed that the A1–1 isolate indicated the lowest LC50 and LT50 values among all used concentrations. Moreover, its vegetative growth and sporulation ranked third and second among all the collected isolates, respectively. Therefore, the A1–1 isolate is being introduced as the most effective biocontrol agent to control greenhouse whitefly.

Keywords


Abbott, W.S. 1925. A method of computing the effectiveness of an insecticide. Journal of Economic Entomolgy, 18(2): 265–267.
Asadalapour, M., Zafari, D. & Zare, R. 2011. Hyphomycetous fungi isolated from insects and their pathogenic effect on colorado beetle in Hamedan province. Journal of Plant Protection (Agricultural Science and Technology), 24(4): 465– 470. (In Persian with English summary).
Asensio, L., Lopez–Llorca, L.V. & López–Jiménez, J.A. 2005. Use of light, scanning electron microscopy and bioassays to evaluate parasitism by entomopathogenic fungi of the red scale insect of palms (Phoenicococcus marlatti Ckll., 1899). Micron, 36(2): 169–175.
Bidochka,M.J.,Kamp, A.M. & De Croos, J.N.A.2000. Insect pathogenic fungi: from genes to populations.pp. 171–193. In: Кronstad, J.W. (ed.), Fungal Pathology. Springer Science.
Bouhous, M. & Larous, L. 2012. Efficiency of the entomopathogenic fungus Verticillium lecanii in the biological control of Trialeurodes vaporariorum, (Homoptera: Aleyrodidae), a greenhouse culture pest. African Journal of Microbiology Research, 6(10): 2435–2442.
Eslamizadeh, R., Sajap, A.S.S., Omar, D.B. & Adam, N.A.B. 2015. Evaluation of different isolates of entomopathogenic fungus, Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) against Bemisia tabaci (Hemiptera: Aleyrodidae). Biocontrol in Plant Protection. 2(2): 82–91.
Fransen, J.J., Winkelman, K. & van Lenteren, J. 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). Journal of Invertebrate Pathology, 50: 158–165.
Fransen, J.J. 1990. Natural enemies of whiteflies, Fungi. In: Gerling, D. (Eds.), Whiteflies: Their Bionomics, Pest Status and Management Intercept. Andover, UK, 187–210 pp.
Francisco, E.A., Mochi, D.A., Correia, A.D.C.B. & Monteiro, A.C. 2006. Influence of culture media in viability test of conidia of entomopathogenic fungi. Ciência Rural, 36(4): 1309–1312.
Gerling, D. 1990. Whiteflies: their bionomics, pest status and management (Volume 18 of International congress of entomology). Intercept, Andover, Hants, UK, 348 pp.
Ghazavi, M., Zangeneh, S. & Abaii, M. 2005. New records of some entomopathogenic fungi from Iran. Rostaniha, 6: 119–130. (In Persian with English summary).
Gökçe, A. & Kubilay Er, M. 2005. Pathogenicity of Paecilomyces spp. to the Glasshouse Whitefly, Trialeurodesvaporariorum, with Some Observations on the Fungal Infection Process. Turkish Journal of Agriculture and Forestry, 29: 331–339.
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.
Humber, R. 1997. Fungi: Identification, 153–185pp. In: Lacey, L.A., & Lacey, L.A. (eds.). Biological Techniques Manual of Techniques in Insect Pathology, chapterV–1. Academic Press.
Kapantaidaki, D.E., Sadikoglou, E., Tsakireli, D., Kampanis, V., Stavrakaki, M., Schorn, C., Aris Ilias, A., Riga, M., George Tsiamis, G., Nauen, R., Skavdis, G., Vontas, J., & Tsagkarakou, A. 2018. Insecticide resistance in Trialeurodes vaporariorum populations and novel diagnostics for kdr mutations. Pest Management Science, 74: 59–69.
Kavanagh, K &Fallon, J.P. 2010. Galleria mellonella larvae as models for studying fungal virulence. Fungal Biology Reviews, 24(1–2): 79–83. 

Keppanan, R., Sivaperumal, S.D.C., Akutse, K.S. & Wang, L. 2017. Molecular docking of protease from Metarhizium anisopliae and their toxic effect against model insect Galleria mellonella. Pesticide Biochemistry and Physiology, 138: 8–14.

Khan, S., Nadir, S., Lihua, G., JianchuXu, J., Keith A., Holmes, K.A. & Dewen, Q. 2016. Identification and characterization of an insect toxin protein, Bb70p, from the entomopathogenic fungus, Beauveria bassiana, using Galleria mellonella as a model system. Journal of Invertebrate Pathology, 133: 87–94.
Kim, C.S., Lee, J.B., Kim, B.S., Nam, Y.H., Shin, K.S., Kim, J.W., Kim, J.E. & Kwon, G.S. 2014. A technique for the prevention of greenhouse whitefly (Trialeurodes vaporariorum) using the entomopathogenic fungus Beauveria bassiana M130. Journal of Microbiology and Biotechnology, 24(1): 1–7.
Luz, C. & Fargues, J. 1997. Temperature and moisture requirements for conidial germination of an isolate of Beauveria bassiana, pathogenic to Rhodnius prolixus. Mycopathologia, 138(3): 117–125.
Malekan, N., Hatami, B., Ebadi, R., Akhavan, A. & Radjabi, R. 2015. Evaluation of entomopathogenic fungi Beauveria bassiana and Lecanicillium muscarium on different nymphal stages of greenhouse whitefly Trialeurodes vaporariorum in greenhouse conditions. Biharean Biologist, 9(2): 108–112.
Malsam, O., Kilian, M., Oerke, E. & Dehne, H.W. 2002. Oils for increased effcacy of Metarhizium anisopliae to control whiteflies. Biocontrol Science and Technology, 12: 337–348.
Martin, J.H., Mifsud, D. & Rapisarda, C. 2000. The whiteflies (Hemiptera: Aleyrodidae) of Europe and the Mediterranean Basin. Bulletin of Entomological Research, 90: 407–448.
Meekes, E.T.M., Fransen, J.J. & van Lenteren, J.C. 2000. Pathogenicity of Aschersonia spp. against whiteflies Bemisia argentifolii and Trialeurodes vaporariorum. Journal of Invertebrate Pathology, 81: 1–11.
Meyling, N.V., & Eilenberg, J. 2007. Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biological control, 43(2): 145–155.
Mishra, S., Kumar, P. & Malik, A. 2015. Effect of temperature and humidity on pathogenicity of native Beauveria bassiana isolate against Musca domestica L. Journal of Parasitic Diseases, 39(4): 697–704.
NouriAiin, M., Askary, H., Imani, S. & Zare, R. 2014. Isolation and characterization of entomopathogenic fungi from hibernating sites of Sunn Pest (Eurygaster integriceps) on Ilam Mountains, Iran. International Journal of Current Microbiology and Applied Sciences, 3(12): 314–325.
Oreste, M., Giovanni Bubici, G., Michele Poliseno, M. & Eustachio Tarasco, E. 2015. Effect of Beauveria bassiana and Metarhizium anisopliae on the Trialeurodes vaporariorumEncarsia formosa system. Journal of Pest Science, DOI 10.1007/s10340–015–0660–4.
Ouedraogo, A., Fargues, J., Goettel, M.S. & Lomer, C.J. 1997. Effect of temperature on vegetative growth among isolates of Metarhizium anisopliae and M. flavoviride. Mycopathologia, 137: 37–43.
Quesada–Moraga, E., Maranhao, E.A.A., Valverde–Garcıa, P. & Santiago–Alvarez, C. 2006. Selection of Beauveria bassiana isolates for control of the whiteflies Bemisia tabaci and Trialeurodes vaporariorum on the basis of their virulence, thermal requirements, and toxicogenic activity. Biological Control, 36: 274–287.
Ranjbar Aghdam, H., Yousefi Porshokouh, A. & Sedighi, L. 2015. Temperature–dependent life table parameters of Galleria mellonella (L.) (Lepidoptera: Pyralidae). Journal of Crop Protection, 4 (Supplementary): 727–738.
Ravensberg, W.J., Malais, M. & Schaaf, D.A. 1990. Verticillium lecanii as a microbial insecticide against glasshouse whitefly. Brighton Crop Protection Conference, Pests and Diseases. Vol. 1: 265–268.
Sayed, S.M., Ali, E.F. & Al–Otaibi, S.S. 2019. Efficacy of indigenous entomopathogenic fungus, Beauveria bsiana (Balsamo) Vuillemin, isolates against the rose aphid, Macrosiphum rosae L. (Hemiptera: Aphididae) in rose production. Egyptian Journal of Biological Pest Control, 29 (19). https://doi.org/10.1186/s41938–019–0123–y.
Schaaf, D.A., Malais, M. & Ravensberg, W.J. 1999. The use of Verticillium lecanii against whitefly and thrips in glasshouse vegetables in the Netherlands. Conference paper : Proceedings and abstracts, Vth International Colloquium on Invertebrate Pathology and Microbial Control, Adelaide, Australia, 20–24 August 1990. 391 pp.
Sharififard, M., Mossadegh, M.S. & Vazirianzadeh, B. 2012. Effects of temperature and humidity on the pathogenicity of the entomopathogenic fungi in control of the house fly, Musca domestica L. (Diptera: Muscidae) under laboratory conditions. Journal of Entomology, 9(5): 282–288.
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: 156–165.
Zayed, A. 2003. Pathogenecity of two Beauveria bassiana indigenous isolates towards the greater wax moth Galleria mellonella L. larvae in Egypt. Efflatounia, 3: 10–14.
Zimmermann, G. 1986. The Galleria bait method for detection of entomopathogenic fungi in soil. Journal of Applied Entomology, 102(1–5): 213–215.