Abstract
Beauveria bassiana (Balsamo) Vuillemin and sublethal concentrations of the insect growth regulators (IGR) diflubenzuron and novaluron were applied simultaneously and sequentially to second-instar Locusta migratoria migratorioides (Sauss.) to determine the interaction between these materials and an entomopathogenic fungus. Nymphs were fed on corn leaf disks treated with several concentrations of each IGR, and a constant dose of B. bassiana was applied topically. Additive interaction was demonstrated in all instances when second-instar nymphs were exposed to diflubenzuron or novaluron simultaneously with B. bassiana treatment, and when the fungus was applied first and IGR after 48 h. Additive interaction was also exhibited when novaluron was applied first and B. bassiana after 48 h. Antagonism was demonstrated when nymphs were fed diflubenzuron-treated corn leaves first, then after 48 h were treated with B. bassiana. The additive interaction that was observed in our experiments could still be useful to achieve efficacious levels of acridid control at low rates of an IGR along with a biological control agent such as an entomopathogenic fungus.
Similar content being viewed by others
References
Anderson TE, Roberts DW (1983) Compatibility of Beauveria bassiana strain with formulations used in Colorado potato beetle (Coleoptera: Chrysomelidae) control. J Econ Entomol 76:1437–1441
Anderson TE, Hajek AE, Roberts DW, Preisler HK, Robertson JL (1989) Colorado potato beetle (Coleoptera: Chrysomelidae): effects of combinations of Beauveria bassiana with insecticides. J Econ Entomol 82:83–89
Bahiense TC, Bittencourt VREP (2004) Laboratory evaluation of the compatibility and the synergism between the entomopathogenic fungus Beauveria bassiana and deltamethrin to resistant strains of Boophilus microplus. Ann N Y Acad Sci 1026:319–322
Bajan C, Fedorko A, Kmitova K (1995) Reactions of entomopathogenic fungi to pesticides. Pol Ecol Stud 21(1):69–88
Bullen FT (1966) Locusts and grasshoppers as pests of crops and pasture—a preliminary economic approach. J Appl Ecol 3(1):147–168
De Faria MR, de O Almeida D, Magalhaes BP (1999) Food consumption of Rhammatocerus schistocercoides Rehn (Orthoptera: Acrididae) infected by the fungus Metarhizium flavoviride Gams & Rozsypal. An Soc Entomol Brasil 28(1):91–99
Delgado FX, Britton JH, Onsager JA, Swearingen W (1999) Field assessment of Beauveria bassiana (Balsamo) Vuillemin and potential synergism with diflubenzuron for control of savanna grasshopper complex (Orthoptera) in Mali. J Invertebr Pathol 73:34–39
Dubovskiy IM, Slyamova ND, Kryukova VY, Yaroslavtseva ON, Levchenko MV, Belgibaeva AB, Adilkhankyzy A, Glupov VV (2012) The activity of nonspecific esterases and glutathione-S-transferase in Locusta migratoria larvae infected with the fungus Metarhizium anisopliae (Ascomycota, Hypocreales). Entomol Rev 92:27–32
Foster RN, Reuter KC, Black L, Britton J (1996) Evaluation of the fungus Beauveria bassiana with selected insecticide stressors for control of unconfined rangeland grasshoppers. Arthropod Manag Tests 21:280
Harvey A (1990) Rearing and breeding of locusts in the laboratory. Natural Resources Institute, Chatham
Hassan AEM, Charnley AK (1989) Ultrastructural study of the penetration by Metarhizium anisopliae through dimilin-affected cuticle of Manduca sexta. J Invertebr Pathol 54:117–124
Horowitz AR, Ishaaya I (2004) Insect pest management—field and protected crops. Springer, Berlin
Hunt VL, Charnley AK (2011) The inhibitory effect of the fungal toxin, destruxin A, on behavioural fever in the desert locust. J Insect Physiol 57:1341–1346
Ibrahim L, Hamieh A, Ghanem H, Ibrahim SK (2011) Pathogenicity of entomopathogenic fungi from Lebanese soils against aphids, whitefly and non-target beneficial insects. Int J Agric Sci 3(3):156–164
Irigaray FJSC, Marco-Mancebón V, Pérez-Moreno I (2003) The entomopathogenic fungus Beauveria bassiana and its compatibility with triflumuron: effects on the twospotted spider mite Tetranychus urticae. Biol Control 26:168–173
Ishaaya I (1990) Benzoylphenyl ureas and other selective control agents—mechanism and application. In: Casida JE (ed) Pesticides and alternatives. Elsevier, Amsterdam, pp 363–376
Ishaaya I, Casida JE (1974) Dietary TH 6040 alters cuticle composition and enzyme activity of house fly larval cuticle. Pesticide Biochem Physiol 4:484–490
Ishaaya I, Horowitz AR (1998) Insecticides with novel modes of action: an overview. In: Ishaaya I, Degheele D (eds) Insecticides with novel modes of action, mechanism and application. Springer, Berlin, pp 1–24
Jaronski ST, Goettel MS (1997) Development of Beauveria bassiana for control of grasshoppers and locusts. Mem Entomol Soc Can 171:225–237
Johnson DL, Goettel MS, Bradley C, Van der Paauw H, Maiga B (1992) Field trials with the entomopathogenic fungus Beauveria bassiana against grasshoppers in Mali, West Africa, July 1990. In: Lomer CJ, Prior C (eds) Biological control of locusts and grasshoppers. CABI, Wallingford, pp 296–310
Keller S (1978) Investigations on the influence of Dimilin (diflubenzuron) on growth and germination of conidia of some insect pathogenic fungi. Anz Schadlingskde Pflanzenschutz Umweltschutz 51:81–83
Lomer CJ, Bateman RP, Johnson DL, Langewald J, Thomas M (2001) Biological control of locusts and grasshoppers. Annu Rev Entomol 46:667–702
Magalhães BP, de Faria MR, Lecoq M, Schmidt FGV, Silva JBT, Frazão HS, Balança G, Foucart A (2001) The use of Metarhizium anisopliae var. acridum against the grasshopper Rhammatocerus schistocercoides in Brazil. J Orthoptera Res 10(2):199–202
Mohan MC, Reddy NP, Devi UK, Kongara R, Sharma HC (2007) Growth and insect assays of Beauveria bassiana with neem to test their compatibility and synergism. Biocontrol Sci Technol 17(10):1059–1069
Mondal K, Parween S (2000) Insect growth regulators and their potential in the management of stored-product insect pests. Integr Pest Manag Rev 5:255–295
Morales-Rodriguez A, Peck DC (2009) Synergies between biological and neonicotinoid insecticides for the curative control of the white grubs Amphimallon majale and Popillia japonica. Biol Control 51(1):69–180
Nevo D (1996) The desert locust, Schistocerca gregaria, and its control in the land of Israel and the near east in antiquity, with some reflections on its appearance in Israel in modern times. Phytoparasitica 24:7–32
Nishimatsu T, Jackson JJ (1998) Interaction of insecticides, entomopathogenic nematodes, and larvae of the western corn rootworm. (Coleoptera: Chrysomelidae). J Econ Entomol 91(2):410–418
Olmert I, Kenneth RG (1974) Sensitivity of the entomopathogenic fungi Beauveria bassiana, Verticillium lecanii and Verticillium sp. to fungicides and insecticides. Environ Entomol 3:33–38
Olson DL, Oetting RD (1999) Compatibility of insect growth regulators and Beauveria bassiana (Balsamo) Vuillemin in controlling green peach aphids (Homoptera: Aphididae) on greenhouse chrysanthemums. J Entomol Sci 34:286–294
Ouedraogo RM, Goettel MS, Brodeur J (2004) Behavioral thermoregulation in the migratory locust: a therapy to overcome fungal infection. Oecologia 138:312–319
Prior C, Greathead DJ (1989) Biological control of locusts: the potential for the exploitation of pathogens. FAO Plant Prot Bull 37:37–48
Prior C, Streett DA (1997) Strategies for the use of entomopathogens in the control of desert locust and other Acridoid pests. Mem Entomol Soc Can 171:5–25
Purwar JP, Sachan GC (2006) Synergistic effect of entomogenous fungi on some insecticides against Bihar hairy caterpillar Spilarctia oblique (Lepidoptera: Arctiidae). Microbiol Res 161(1):38–42
Quintela ED, McCoy CW (1997) Pathogenicity enhancement of Metarhizium anisopliae and Beauveria bassiana to first instars of Diaprepes abbreviatus (Coleoptera: Curculionidae) with sublethal doses of imidacloprid. Environ Entomol 26:1173–1182
Reuter KC, Foster RN, Tompkins MT, Bradley C, Britton J, Underwood N, Black LR, Vigil E, Daye G, Radsick B, Fuller B, Brinkman M, Kahler E (1993) Development of the fungus Beauveria bassiana as a bio-insecticide for grasshoppers on rangeland. 1993 Annual Report, Grasshopper Integrated Pest Management Project. USDA/APHIS/PPQ, Boise, pp. 233–238
Reuter KC, Foster RN, Black L, Britton J (1996) Laboratory evaluation of Beauveria bassiana with an added chemical stressor. Arthropod Manag Tests 21:415–416
Russell CW, Ugine TA, Hajek AE (2010) Interactions between imidacloprid and Metarhizium brunneum on adult Asian longhorned beetles (Anoplophora glabripennis (Motschulsky)) (Coleoptera: Cerambycidae). J Invertebr Pathol 105(3):305–311
Serebrov VV, Kiselev AA, Glupov VV (2003) The study of some synergistic factors between entomopathogenic fungi and chemical insecticides. Mikol Fitopatol 37(1):76–82
Serebrov VV, Gerber ON, Malyarchuk AA, Martemyanov VV, Alekseev AA, Glupov VV (2006) Effect of entomopathogenic fungi on detoxification enzyme activity in greater wax moth Galleria mellonella L. (Lepidoptera, Pyralidae) and role of detoxification enzymes in development of insect resistance to entomopathogenic fungi. Biol Bull 33:581–586
Tingle CCD (1996) Sprayed barrier of diflubenzuron for control of the migratory locust Locusta migratoria capito (Sauss.) [Orthoptera:Acrididae] in Madagascar: short-term impact on relative abundance of terrestrial non-target invertebrates. Crop Prot 15:579–592
Zibaee A, Bandani AR, Tork M (2009) Effect of the entomopathogenic fungus, Beauveria bassiana, and its secondary metabolite on detoxifying enzyme activities and acetylcholinesterase (AChE) of the Sunn pest, Eurygaster integriceps (Heteroptera: Scutellaridae). Biocontrol Sci Tech 19:485–498
Acknowledgments
We thank Galina Gindin and Marina Hazanovski for advice and all workers of Entomology Department of Gilat Research Center for their help. This research was supported (in part) under Grant No. CA23-022 funded by the US Israel Cooperative Development Research Program, Bureau for Economic Growth, Agriculture, and Trade, US Agency for International Development.
Conflict of interest
None of the authors have any conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Traugott.
Rights and permissions
About this article
Cite this article
Bitsadze, N., Jaronski, S., Khasdan, V. et al. Joint action of Beauveria bassiana and the insect growth regulators diflubenzuron and novaluron, on the migratory locust, Locusta migratoria . J Pest Sci 86, 293–300 (2013). https://doi.org/10.1007/s10340-012-0476-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-012-0476-4