Journal of Crop Protection

Virulence of two entomopathogenic nematodes through their interaction with Beauveria bassiana and Bacillus thuringiensis against Pieris brassicae (Lepidoptera: Pieridae)

10.48311/jcp.2017.1355
Volume 6, Issue 2
June 2017
Pages 287-299
Journal of Crop Protection

Authors

A. Abdolmaleki 1
H. Rafiee Dastjerdi 1
Z. Tanha Maafi 2
B. Naseri 1

1 Department of Entomology, Agricultural Sciences Faculty, University of Mohaghegh Ardabili, Ardabil, Iran.

2 Iranian Research Institute of Plant Protection, Agricultural Research Education and Extension Organization (AREEO), Tehran, Iran.

Abstract
Pieris brassicae L. is one of the most important pests of Brassicaceae. The insecticidal effect of two entomopathogenic nematodes (EPNs), Heterorhabditis bacteriophora and Steinernema feltiae, was determined through their interaction with Beauveria bassiana and Bacillus thuringiensis subsp. kurstaki (Btk) against P. brassicae. In the interaction tests, the EPNs were applied at LC50 level 0, 12 or 24h after treating the larvae with LC10 or LC25 of the B. bassiana or Btk. The interaction between the EPNs and B. bassiana was entirely different from the interaction of the EPNs and Btk. The interaction with B. bassiana was dependant on time intervals, while the interaction of the EPNs with Btk was almost additive or synergistic. An antagonistic effect was seen when the EPNs were applied immediately after the B. bassiana. However, the application of the EPNs 24h after their treatment with B. bassiana caused additive or synergistic effects. The results also showed the best mortality effect when the EPNs were used with Btk at 12 h and 24 h time intervals. Based on the results, a simultaneous use of the EPNs and B. bassiana is not recommended against P. brassica. However, the EPNs could be used simultaneously after Btk but it is better to allow a time interval to increase mortality.

Keywords

Biological control
Heterorhabditis bacteriophora
IPM
Steinernema feltiae
Abbott, W. S. 1925. A method for computing the effectiveness of an insecticide. Journal of Economic Entomology, 18: 265-267.
Abdolmaleki, A., Tanha Maafi, Z., Rafiee Dastjerdi, H. and Lewis, E. 2015. Potential efficacy of Iranian isolates of Heterorhabditis bacteriophora and Steinernema feltiae on Pieris brassicae (Lepidoptera: Pieridae). Russian Journal of Nematology, 23 (2): 91-97.
Abdolmaleki, A., Tanha Maafi, Z., Rafiee Dastjerdi, H., Naseri, B. and Ghasemi, A. 2016. Isolation and identification of entomopathogenic nematodes and their symbiotic bacteria from Kurdistan province in Iran. Journal of Crop Protection, 5 (2): 259-271.
Akhurst, R. J. 1983. Neoaplectana species: specificity of association with bacteria of the genus Xenorhabdus. Experimental Parasitology, 55: 258-263.
Ansari, M. A., Tirry, L. and Moens, M. 2004. Interaction between Metarhizium anisopliae CLO 53 and entomopathogenic nematodes for the control of Hoplia philanthus. Biological Control, 31: 172-180.
Arand, R., Prasad, B. and Tiwary, B. N. 2009. Relative susceptibility of Spodoptera litura pupae to selected entomopathogenic fungi. BioControl, 54: 85-92.
Asi, M. R., Bashir, M. H., Afzal, M., Zia, K. and Akram, M. 2013. Potential of entomopathogenic fungi for biocontrol of Spodoptera litura Fabricus (Lepidoptera: Noctuidae). The Journal of Animal and Plant Sciences, 23 (3): 913-918.
Barbercheck, M. E. and Kaya, H. K. 1990. Interactions between Beauveria bassiana and the Entomogenous Nematodes, Steinernema feltiae and Heterorhabditis heliothidis. Journal of Invertebrate Pathology, 55: 225-234.
Barbercheck, M. E. and Kaya, H. K. 1991. Competitive interactions between entomopathogenic nematodes and Beauveria bassiana (Deuteromycotina: Hyphomycetes) in soil borne larvae of Spodotera exigua (Lepidoptera: Noctuidae). Environmental Entomology, 20 (2): 707-712.
Boemare, N. E. 2002. Biology, taxonomy and systematics of Photorhabdus and Xenorhabdus, In: Gaugler J. (Ed.), Entomopathogenic Nematology. CABI Publishing, Wallingford, pp. 35-56.
Cartea, M. E., Padilla, G., Vilar, M. and Velasco, P. 2009. Incidence of the major Brassica pests in Northwestern Spain. Journal of Economic Entomology, 102 (2): 767-73.
Choo, H. Y., Kaya, H. K., Huh, J., Lee, D. W., Kim, H. H., Lee, S. M. and Choo, Y. M. 2002. Entomopathogenic nematodes (Steinernema spp. And Heterorhabditis bacteriophora) and a fungus Beauveria brongniartii for biological control of the white grubs, Ectinohoplia rufipes and Exomala orientalis, in Korean golf courses. BioControl,47: 177-192.
Dubois, N. R. and Dean, D. H. 1995. Synergism between CryIA insecticidal crystal proteins and spores of Bacillus thuringiensis, other bacterial spores, and vegetative cells against Lymantria dispar (Lepidoptera: Lymantriidae) larvae. Environmental Entomology,24: 1741-1747.
Eilenberg, J., Damgaard, P. H. and Thomsen, L. 1998. Activity of Bacillus thuringiensis strains against Pieris brassicae. Danish Ministry of the Environment, Environmental Protection Agency, København.
Forst, S. and Clarke, D. 2002. Bacteria–nematode symbiosis. In: Gaugler, R. (Ed.), Entomopathogenic Nematology. CABI Publishing, London, pp. 57-77.
Furlong, M. J. and Groden, E. 2001. Evaluation of synergistic interactions between the Colorado potato beetle (Coleoptera: Chrysomelidae) pathogen Beauveria bassiana and the insecticides imidacloprid and cyromazine. Journal of Economic Entomology, 94: 344-356.
García-Gutiérrez, C., Rosas-García, N. M., Norzagaray-Campos, M. and Isaías Chaírez-Hernández, I. 2010. Efficacy of Beauveria bassiana and Metarhizium anisopliae to Control Pieris rapae on Cabbage in the Field.Southwestern Entomologist, 35 (1): 75-83.
Glare, T. R. 1994. Stage-dependent synergism using Metarhizium anisopliae and Serratia entomophila against Costelytra zealandica. Biocontrol Science and Technology, 4: 321-329.
Hatting, J. L. 2012. Comparison of Three Entomopathogenic Fungi against the Bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), Employing Topical vs per os Inoculation Techniques. African Entomology, 20 (1): 91-100.
Helson, G. A. H. 1960. Bacillus thuringiensis Berl. As a potential means of control of cabbage white butterfly (Pieris rapae L.), diamond-back moth (Plutella maculipennis Curt.), and some other lepidoptera. New Zealand Journal of Agricultural Research, 3: 1009-1014.
Jaques, R. P. and Morris, O. N. 1981. Compatibility of pathogens with other methods of pest control and with different crops. In: Burges, H. D. (Ed.), Microbial Control of Pests and Plant Diseases. Academic Press, London, pp. 695-715.
Kamionek, M., Sandner, H. and Seryczynska, H. 1974a. The combined action of Beauveria bassiana (BalsNuill.) (Fungi Imperfecti: Moniliales) and Neoaplectana carpocupsae Weiser (Nematoda: Steinemematidae). Bull of Polish Academy of Sciences, 22: 253-257.
Kamionek, M., Sandner, H. and Seryczynska, H. 1974b. Combined action of Paecilomyces farinosus Dicks (Brown et Smith) (Fungi Imp.: Moniliales) and Neoaplectuna carpocapsae Weiser, 1955 (Nematoda: Steinemematidae) on certain insects. Acta Parasitologica Polonica, 22: 357-363.
Karowe, D. N. and Schoonhoven, L. M. 1992. Interactions among three trophic levels: the influence of host plant on performance of Pieris brassicae and its parasitoid, Cotesia glomerata. Entomologia Experimentalis Et Applicata, 62 (3): 241–251.
Kaya, H. K. and Gaugler, R. 1993. Entomopathogenic nematodes. Annual Review of Entomology, 38: 181-206.
KoppenhÖfer, A. M. and Kaya, H. K. 1996. Additive and synergistic interaction between entomopathogenic nematodes and Bacillus thuringiensis for scarab grub control. Biological Control, 8: 131-137.
Lecadet, M. M. and Martouret, D. 1987. Host specificity of the Bacillus thuringiensis delta-endotoxin toward Lepidopteran species: Spodoptera littoralis Bdv. and Pieris brassicae L. Journal of Invertebrate Pathology, 49: 37-48.
Lewis, E. E., Gaugler, R. and Harrison, R. 1993. Response of cruiser and ambusher entomopathogenic nematodes (Steinernematidae) to host volatile cues. Canadian Journal of Zoology, 71: 765-769.
Mbata, G. N. and Shapiro-Ilan, D. I. 2010. Compatibility of Heterorhabditis indica (Rhabditida: Heterorhabditidae) and Habrobracon hebetor (Hymenoptera: Braconidae) for biological control of Plodia interpunctella (Lepidoptera: Pyralidae). Biological Control, 54: 75-82.
Metaspalu, L., Hiiesaar, K., Jogar, K., Svilponis, E., Ploomi, A., Kivimagia, I., Luik, A. and Menshikova, N. 2009. Oviposition preference of Pieris brassicae (L.) on different Brassica oleracea var. Capitatal. Cultivars.Agronomy Research, 7: 411-456.
Morris, O. N., Trottier, M., Converse, V. and Kanagaratnam, P. 1996. Toxicity of Bacillus thuringiensis subsp. aizawai for Mamestra configurata (Lepidoptera: Noctuidae). Journal of Economic Entomology,89: 359-365.
Nguyen, N. T. H., Borgemeister, C., Poehling, H. M. and Zimmermann, G. 2007. Laboratory investigations on the potential of entomopathogenic fungi for biocontrol of Helicoverpa armigera (Lepidoptera: Noctuidae) larvae and pupae. Biocontrol Science and Technology, 17 (8): 853-864.
Oestergaard, J., Belau, C., Strauch, O., Ester, A., Rozen, K. V. and Ehlers, R. U. 2006. Biological control of Tipula paludosa (Diptera: Nematocera) using entomopathogenic nematodes (Steinernema spp.) and Bacillus thuringiensis subsp. israelensis Jesko. Biological Control, 39: 525-531.
Peters, A. and Ehlers, R.-U. 1994. Susceptibility of leatherjackets (Tipula paludosa and T. oleracea, Tipulidae: Nematocera) to the entomopathogenic nematode Steinernema feltiae. Journal of Invertebrate Pathology, 63: 163-171.
Poinar GO., Jr. 1990. Taxonomy and biology of Steinernematidae and Heterorhabditidae. In: Gaugler, R. and Kaya, H. K. (Eds), Entomopathogenic Nematodes in Biological Control. CRC Press, Boca Raton, pp. 23-61.
Robertson, J. L., Russell, R. M., Preisler, H. K. and Savin, N. E. 2007. Bioassays with Arthropods. CRC Press, Boca Raton, US.
SPSS Inc. 2010. SPSS for Windows User's Guide Release 6. SPSS Inc, Chicago.
Tanada, Y. 1985. A synopsis of studies of the synergistic property of an insect baculovirus: A tribute to Edward A. Steinhaus. Journal of Invertebrate Pathology,45: 125-138.
Wraight, S. P., Ramos, M. E., Avery, P. B., Jaronski, S. T. and Vandenberg, J. D. 2010. Comparative virulence of Beauveria bassiana isolates against lepidopteran pests of vegetable crops.Journal of Invertebrate Pathology, 103: 186-199.

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