Control of mushroom sciarid fly Lycoriella inguena (Dufour) with an azadirachtin-based insecticide

  • Tanja M Drobnjaković Institute of Pesticides and Environmental Protection, Banatska 31B, 11080, Belgrade
  • Dejan Marčić Institute of Pesticides and Environmental Protection, Banatska 31B, 11080, Belgrade
  • Ivana Potočnik Institute of Pesticides and Environmental Protection, Banatska 31B, 11080, Belgrade
  • Emil Rekanović Institute of Pesticides and Environmental Protection, Banatska 31B, 11080, Belgrade
  • Mirjana Prijović Institute of Pesticides and Environmental Protection, Banatska 31B, 11080, Belgrade
  • Svetlana Milijašević-Marčić Institute of Pesticides and Environmental Protection, Banatska 31B, 11080, Belgrade
  • Miloš Stepanović Institute of Pesticides and Environmental Protection, Banatska 31B, 11080, Belgrade
Keywords: mushroom sciarid flies, Lycoriella inguena, Agaricus bisporus, azadirachtin, biopesticides,

Abstract


The impact of a bioinsecticide based on azadirachtin (Ozoneem trishul 1 %) on the abudance of mushroom flies (Sciaridae: Diptera) was compared to the effect of a commercial formulation of the malathion-based chemical insecticide Etiol tečni. Experiments were conducted in three growing chambers (B6, B7 and B8) of a commercial mushrom farm “Delta Danube” d.o.o., Kovin. Casing treatments were performed in eight replications in a random block design. The azadirachtin-based bioinsecticide was applied in chamber B8 four times (0.5 ml/m2): during casing and later at seven-day intervals. The standard chemical insecticide based on malathion was applied in chambers B6 and B7 twice (2 x 0.3 ml/m2), on the third and sixth day after casing. In all three chambers, the abudance of mushroom flies was monitored by using yellow sticky traps, which were collected weekly and replaced with new ones four times at seven days intervals. The yellow sticky traps were examined in the laboratory under a binocular microscope to determine the presence and density of mushroom flies. Only one species of mushroom fly, Lycoriella ingenua (Dufour), was found on the yellow sticky traps throughout the experimental period. The average number of sciarid flies per mushroom block 15 and 22 days after treatment (DAT) was significantly lower in the test chamber B8 than in chambers B7 and B6, while there was no significant difference 30 and 36 DAT, compared to the control chamber B6. The average number of sciarid flies per mushroom row throughout the experiment was significantly lower in the test chamber B8 than in chambers B6 and B7. The results of our study suggest that the azadirachtin-based bioinsecticide can suppress populations of the mushroom fly L. ingenua and may provide a good alternative to conventional chemical insecticide.

Author Biography

Tanja M Drobnjaković, Institute of Pesticides and Environmental Protection, Banatska 31B, 11080, Belgrade
Laboratory of applied entomology

References

Amadioha, A.C., & Obi, V.I. (1998). Fungitoxic activity of extracts from Azadirachta indica and Xylopia aethiopica on Colletotrichum lindemuthianum in cowpea. Journal of Herbs Spices and Medicinal Plants, 6(2), 33-40. doi.org/10.1300/j044v06n02_04

Bartlett, G.R., & Keil, C.B.O. (1997). Identification and characterization of a permethrin resistance mechanism in populations of the fungus gnat Lycoriella Mali (Fitch) (Diptera: Sciaridae). Pesticide Biochemistry and Physiology, 58(3), 173-181. doi.org/10.1006/pest.1997.2306

Binns, E.S. (1980). Field and laboratory observations on the substrates of the mushroom fungus gnat Lycoriella auripila (Diptera: Sciaridae). Annals of Applied Biology, 96(2), 143-152. doi.org/10.1111/j.1744-7348.1980.tb02973.x

Cantelo, W.W. (1983). Control of a mushroom infesting fly (Diptera: Sciaridae) with insecticides applied to the casing layer. Journal of Economic Entomology, 76(6), 1433–1436. doi.org/10.1093/jee/76.6.1433

EPPO (2004). Insects and mites on mushrooms, PP 1/167(2). In Efficacy evaluation of plant protection products, Insecticides & Acaricides, 3. Paris, France: EPPO.

Erler, F., & Cetin, H. (2007). Mortality of brown-tail moth, Euproctis chrysorrhoea (L.), larvae in response to neembased products. Journal of Entomological Science, 42(4), 593-595. doi.org/10.18474/0749-8004-42.4.593

Erler, F., Polat, E., Demir, H., Catal, M., & Tuna, G. (2011). Control of mushroom sciarid gnut Lycoriella ingénue populations with insect growth regulators applied by soil drench. Journal of Economic Entomology, 104(3), 839-844. doi.org/10.1603/EC10292

Erler, F., Polat, E., Demir, H., Cetin, H., & Erdemir, T. (2009). Control of the mushroom phorid f ly, Megaselia halterata (Wood), with plant extracts. Pest Management Science, 65(2), 144-149. doi.org/10.1002/ps.1658

Geels, F.P., & Rutjens, A.J. (1992). Bendiocarb and dif lubenzuron as substitute insecticides for endosulfan in commercial mushroom growing. Annals of Applied Biology, 120(2), 215-224. doi.org/10.1111/j.1744-7348.1992.tb03419.x

Greenberg, S.M., Showler, A.T., & Liu, T.X. (2005). Effects of neem-based insecticides on beet armyworm (Lepidoptera: Noctuidae). Insect Science, 12(1), 17-23. doi.org/10.1111/j.1672-9609.2005.00003.x

Greenslade, P., & Clift, A.D. (2004). Review of pest arthropods recorded from commercial mushroom farms in Australia. Australasian Mycologist 23(3), 77-93.

Hussey, N.W., & Gurney, B. (1968). Biology and control of the sciarid Lycoriella auripila Winn. (Diptera: Lycoriidae) in mushroom culture. Annals of Applied Biology, 62(3), 395-403. doi.org/10.1111/j.1744-7348.1968.tb05451.x

Hussey, N.W., Read, W.H., & Hesling, J.J. (1974). The pests of protected cultivation: The biology and control of glasshouse and mushroom pests (2nd ed.). London, UK: Arnold.

Ignatowicz, S., Mietkiewski, R., & Pezowicz, E. (1998). Compatibility of botanical insecticides with entomopathogenic fungi and entomogenous nematodes. IOBC Bulletin, 2, 9-12.

Isman, M.B. (1993). Growth inhibitory and antifeedant effects of azadirachtin on six noctuids of regional economic importance. Pesticide Science, 38(1), 57-63. doi.org/10.1002/ps.2780380109

Jess, S., & Bingham, J.F.W. (2004). Biological control of sciarid and phorid pests of mushroom with predatory mites from the genus Hypoaspis (Acari: Hypoaspidae) and the entomopathogenic nematode Steinernema feltiae. Bulletin of Entomological Research, 94(2), 159-167. doi.org/10.1079/BER2003286

Keil, C. (2002). Field trials of the Gnatrol WDG formulation of Bacillus thuringiensis var. israelensis for control of mushroom flies in Pennsylvania and California. Mushroom News 50(4), 12-19.

Keil, C.B.O., & Bartlett, G.R. (1995). Azatin for control of Lycoriella mali in Agaricus mushroom production. Mushroom News, 43(4), 10-13.

Khan, M.W., Alam, M.M., Khan, A.M., & Saxena, S.K. (1974). Effect of water soluble fractions of oil cakes and bitter principles of neem on some fungi and nematodes. Acta Botanica Indica, 2, 120-128.

Kielbasa, R., & Snetsinger, R. (1980). Life history of a sciarid fly, Lycoriella mali, and its injury threshold on the commercial mushroom [Includes taxonomy]. Bulletin-Pennsylvania State University, Agricultural Experiment Station, 833, 14.

Kim, K.J., & Hwang, C.Y. (1996). An investigation of insect pest on the mushroom (Lentinus edodes, Pleurotus ostreatus) in south region of Korea. Korean Journal of Applied Entomology, 35, 45-51.

Lewandowski, M., Sznyk, A., & Bednarek, A. (2004). Biology and morphometry of Lycoriella ingenua (Diptera: Sciaridae). Biology Letters, 41(1), 41-50.

Liang, G.M., Chen, W., & Liu, T.X. (2003). Effects of three neem-based insecticides on diamondback moth (Lepidoptera: Plutellidae). Crop Protection, 22(2), 333-340. doi.org/10.1016/S0261-2194(02)00175-8

Ludwig, S.W., & Oetting, R.D. (2001). Evaluation of medium treatments for management of Frankliniella occidentalis (Thripidae: Thysanoptera) and Bradysia coprophila (Diptera: Sciaridae). Pest Management Science, 57(12), 1114-1118. doi.org/10.1002/ps.404

Menzel, F., & Mohrig, W. (1999). Revision der palaarktischen Trauermucken (Diptera: Sciaridae) [A revision of the Palaearctic black fungus gnats (Diptera: Sciaridae).]. Studia Dipterologica, 6 (Supplement).

Milijašević-Marčić, S., Todorović, B., Potočnik, I., Stepanović, M., & Rekanović, E. (2012). First report of Pseudomonas tolaasii on Agaricus bisporus in Serbia. Phytoparasitica, 40(3), 299-303. doi.org/10.1007/s12600-011-0215-z

Naumann, K., & Isman, M.B. (1995). Evaluation of neem Azadirachta indica seed extracts and oils as oviposition deterrents of noctuid moths. Entomologia Experimentalis et Applicata, 76(2), 115-120. doi.org/10.1111/j.1570-7458.1995.tb01953.x

Navarro, M.J., & Gea, F.J. (2006). Estudio de la fitotoxicidad del insecticida diflubenzuron en el cultivo de champinon. Determinacion del nivel de residuos. Boletín de la Asociación Española de Cultivadores de Champiñón, 48, 32-34.

Okumu, F.O., Knols, B.G.J., & Fillinger, U. (2007). Larvicidal effects of a neem (Azadirachta indica) oil formulation on the malaria vector Anophele gambiae. Malaria Journal, 6, 63-68. doi: 10.1186/1475-2875-6-63

Park, I.K., Choi, K.S., Kim, D.H., Choi, I.H., Kim, L.S., Bak, W.C., Choi, J.W., & Shin, S.C. (2006). Fumigant activity of plant essential oils and components from horseradish (Armoracia rusticana), anise (Pimpinella anisum) and garlic (Allium sativum) oils against Lycoriella ingénue (Diptera: Sciaridae). Pest Management Science, 62(8), 723- 728. doi: 10.1002/ps.1228

Raguraman, S., & Kannan, M. (2014). Non-target effects of botanicals on beneficial arthropods with special reference to Azadirachta indica. In Singh, Dwijendra (Ed.), Advances in plant biopesticides (pp 173-205). New Delhi, India: Springer.

Rinker, D.L. (2017). Insect, mite, and nematode pests of commercial mushroom production.In D.C. Zied, & A. Pardo-Gimenez (Eds.), Edible and medicinal mushrooms: technology and applications (1st ed.) (pp 221-237). New Jersey, USA: John Wiley.

Rovesti, L., Viccinelli, R., & Barbarossa, B. (1996). Biological contol of sciarid flies. Bulletin OILB SROP, 19, 20-23.

Scheepmaker, J.W.A., Geels, F.P., Smits, P.H., & Van Griensven, L.J.L.D. (1997). Control of the mushroom pests Lycoriella auripila (Diptera: Sciaridae) and Megaselia halterata (Diptera: Phoridae) by Steinernema feltiae (Nematoda: Steinernematidae) in field experiments. Annals of Applied Biology, 131(3), 359-368. doi.org/10.1111/j.1744-7348.1997.tb05165.x

Scheepmaker, J.W.A., Geels, F.P., Van Griensven, L.J.L.D., & Smits, P.H. (1995). Control of the mushroom sciarid (Lycoriella auripila) and the mushroom phorid (Megaselia halterata) by entomopathogenic nematodes. Mushroom Science, 14(2), 491-498.

Shamshad, A. (2010). The development of integrated pest management for the control of mushroom sciarid flies, Lycoriella ingenua (Dufour) and Bradysia ocellaris (Comstock), in cultivated mushrooms. Pest Management Science, 66(10), 1063-1074. doi.org/10.1002/ps.1987

Siegwart, M., Graillot, B., Blachere Lopez, C., Besse, S., Bardin, M., Nicot, P.C., & Lopez-Ferber, M. (2015). Resistance to bio-insecticides or how to enhance their sustainability: a review. Frontiers in Plant Science, 6, 381. doi.org/10.3389/fpls.2015.00381

Smith, J.E. (2002). Dimilin resistance in mushroom sciarids. Mushroom Journal, 656, 15-19.

Stark, J.D., Vargas, R.I., & Wong, T.Y. (1990). Effects of neem seed extracts on tephritid fruit flies (Diptera: Tephritidae) and their parasitoids in Hawaii. ARS-US Department of Agriculture, Agricultural Research Service (USA), 86, 106-112.

StatSoft Inc. (2004). STATISTICA (data analysis software system), version 7. Retrieved from www.statsoft.com

Steinhauer, B. (1996). Fungicidal activity of commercial neem products. In IVth Workshop Proceedings on Practice Oriented Results in Use and Production of Neem Ingredients and Pheromones, Bordigherra, Italy, 1994 (pp 105-108). Giessen, DE: Druck & Graphic.

Villaverde, J.J., Sevilla-Moran, B., Sandin-Espana, P., Lopez-Goti, C., & Alonso-Prados, J.L. (2014). Biopesticides in the framework of the European Pesticide Regulation (EC) No. 1107/2009. Pest Management Science, 70(1), 2-5. doi.org/10.1002/ps.3663

White, P.F. (1985). Pests and pesticides: The biology and technology of the cultivated mushroom. Chichester, UK: Wiley Publishers.

White, P.F. (1986). The effect of sciarid larvae (Lycoriella auripila) on cropping of the cultivated mushroom (Agaricus bisporus). Annals of Applied Biology, 109(1), 11-17. doi.org/10.1111/j.1744-7348.1986.tb03179.x

Wuest, P.J., & Bengston, G.D. (Eds.). (1982). Handbook for commercial mushroom growers. University Park, PA, USA: Pennsylvania State University.

Published
2019/12/30
Section
Original Scientific Paper