Annals of Microbiology

, Volume 63, Issue 3, pp 1083–1091

Interaction between the entomopathogenic bacterium Bacillus thuringiensis subsp. kurstaki and two entomopathogenic fungi in bio-control of Sesamia nonagrioides (Lefebvre) (Lepidoptera: Noctuidae)

  • Spiridon Mantzoukas
  • Panagiotis Milonas
  • Dimitris Kontodimas
  • Kostas Angelopoulos
Original Article


The interactions between the entomopathogenic bacterium Bacillus thuringiensis ssp. kurstaki and two entomopathogenic fungi Beauveria bassiana Balsamo (Vuillemin) (Hypocreales: Cordycipitaceae) and Metarhizium robertsii (Metchnikoff) Sorokin (Hypocreales: Clavicipitaceae) were examined on larvae of Sesamia nonagrioides (Lefebvre) (Lepidoptera: Noctuidae) in 8, 13 and 16 days post-treatment intervals. An overall positive interaction between the pathogens was observed and the larval mortality at 16 days was 56–100 % exposed to M. robertsii combined with B. thuringiensis subsp. kurstaki, whereas B. bassiana combined with B. thuringiensis ssp. kurstaki killed 54–100 % of exposed larvae. After 8 days, in 6 of the combinations, we found an additive relationship between the pathogens, whereas, a negative interaction was observed in 10 of them. In contrast, after 13 days, in 2 of the combinations the positive interaction could be considered as synergistic between pathogens, in 10 as additive, and in only 4 as negative. Finally, after 16 days, in 11 of the combinations we found an additive connection between the pathogens, wheras a negative interaction was seen in 5. Applying both pathogens simultaneously offers a method of Sesamia nonagrioides control that could be more effective than using each pathogen separately.


Pathogen interaction Beauveria bassiana Metarhizium robetsii Bacillus thuringiensis subsp. kurstaki Sesamia nonagrioides 


  1. Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267Google Scholar
  2. Avantaggiato G, Quaranta F, Desiderio E, Visconti A (2002) Fumonisin contamination of maize hybrids visible damaged by Sesamia. J Sci Food Agric 83:13–18Google Scholar
  3. Bauer LS, Miller DL, Maddox JV, McManus ML (1998) Interactions between a Nosema sp. (Microspora: Nosematidae) and nuclear polyhedrosis virus infecting the gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae). J Invertebr Pathol 74:147–153CrossRefGoogle Scholar
  4. Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae line age. Mycologia 101:512–530PubMedCrossRefGoogle Scholar
  5. Butron A, Malvar RA, Carteam E, Ordas A, Velasco P (1999) Resistance of maize in breds to pink stem borer. Crop Prot 39:102–107Google Scholar
  6. Butron A, Sandoya G, Santiago R, Ordas A, Rial A, Malvar RA (2006) Searching for new sources of pink stem borer resistance in maize. Genet Resour Crop Evol 53:1455–1462CrossRefGoogle Scholar
  7. Costa SD, Barbercheck ME, Kennedy GG (2001) Mortality of Colorado potato beetle (Leptinotarsa decemlineata) after sublethal stress with the CRYIIIA deltaendotoxin of Bacillus thuringiensis and subsequent exposure to Beauveria bassiana. J Invertebr Pathol 77:173–179PubMedCrossRefGoogle Scholar
  8. Dias C, Garcia P, Simoes N, Oliveira L (2005) Efficacy of Bacillus thuringiensis Against Phyllocnistis citrella (Lepidoptera: Phyllocnistidae). J Econ Entomol 98:1880–1883PubMedCrossRefGoogle Scholar
  9. Dimas I, Pitta E, Angelopoulos K (2007) Corn Stalk Borer (Sesamia nonagrioides) Infestation on Sorghum in Central Greece. Phytoparasitica 35:191–193CrossRefGoogle Scholar
  10. Eizaguirre M, Fantinou A (2012) Abundance of Sesamia nonagrioides (Lef.) (Lepidoptera: Noctuidae) on the edges of the Mediterranean Basin. Psyche, Article ID 854045, doi:10.1155/2012/854045
  11. Eizaguirre M, Tort S, Lopez C, Albajes R (2005) Effects of Sublethal Concentrations of Bacillus thuringiensis on larval Development of Sesamia nonagrioides. J Econ Entomol 98:464–470PubMedCrossRefGoogle Scholar
  12. Furlong MJ, Groden EJ (2001) Evaluation of synergistic interactions between the Colorado potato beetle (Coleoptera: Chrysomelidae) pathogen Beauveria bassiana and the insecticides, imidacloprid and cyromazine. Econ Entomol 94:344–356CrossRefGoogle Scholar
  13. Goettel MS, Inglis GD, Wraight SP (2000) Fungi. In: Lacey LA, Kaya HK (eds) Field Manual in Invertebrate Pathology. Kluwer, Dordrecht, pp 255–282CrossRefGoogle Scholar
  14. Gonzalez-Cabrera J, Molla O, Monton H, Urbaneja A (2011) Efficacy of Bacillus thuringiensis (Berliner) in controlling the tomato borer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). BioControl 56:71–80CrossRefGoogle Scholar
  15. Hajek AE, McManus ML, Delalibera I Jr (2007) A review of introductions of pathogens and nematodes for classical biological control of insects and mites. Biol Control 41:1–13CrossRefGoogle Scholar
  16. Hilder VA, Boulter D (1999) Genetic engineering of crop plants for insect resistance—a critical review. Crop Prot 18:177–191CrossRefGoogle Scholar
  17. Inglis DG, Goettel SM, Butt MT, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CABI, Wallingford, pp 23–69Google Scholar
  18. International Programme on Chemical Safety (IPCS-WHO) (2000) Microbial Pest Control Agent Bacillus thuringiensis. Environmental Health Criteria 217. Available online at:
  19. Jacques RP, Morris ON (1981) Compatibility of pathogens with other methods of pest control and with different crops. In: Burges HD, Hussey NW (eds) Microbial Control of Insect and Mites. Academic, New YorkGoogle Scholar
  20. Kryukov VY, Khodyrev VP, Yaroslavtseva ON, Kamenova AS, Duisembekov BA, Glupov VV (2009) Synergistic Action of Entomopathogenic Hyphomycetes and the Bacteria Bacillus thuringiensis ssp. morrisoni in the Infection of Colorado Potato Beetle Leptinotarsa decemlineata. Appl Biochem Microbiol 45:511–516CrossRefGoogle Scholar
  21. Lefebvre A (1827) Description de divers insects in edits. Ann Soc Linn (Paris) 6:98Google Scholar
  22. Lewis LC, Bing LA (1991) Bacillus thuringiensis Berliner and Beauveria bassiana (Balsamo) Vuillemin for European corn borer control: program for immediate and season long suppression. Can Entomol 123:387–393CrossRefGoogle Scholar
  23. Lewis LC, Berry EC, Obrycki JJ, Bing LA (1996) Aptness of insecticides (Bacillus thuringiensis and carbofuran) with endophytic Beauveria bassiana, in suppressing larval populations of the European corn borer. Agric Ecosyst Environ 57:27–34CrossRefGoogle Scholar
  24. Lewis LC, Bruck DJ, Gunnarson RD (2002) On-farm evaluation of Beauveria bassiana for control of Ostrinia nubilalis in Iowa, USA. Biocontrol 47:167–176CrossRefGoogle Scholar
  25. Lopez C, EIizaguirre M, Albajes R (2003) Courtship and mating behaviour of the Mediterranean corn borer, Sesamia nonagrioides (Lepidoptera: Noctuidae). Span J Agric Res 1:43–51Google Scholar
  26. Ma X-M, Liu X-X, Ning X, Zhang B, Han F, Guan X-M, Tan Y-F, Zhang Q-W (2008) Effects of Bacillus thuringiensis toxin Cry1Ac and Beauveria bassiana on Asiatic corn borer (Lepidoptera: Crambidae). J Invertebr Pathol 99:123–128PubMedCrossRefGoogle Scholar
  27. Malvar RA, Buton A, Ordas B, Santiago R (2008) Causes of natural resistance to stem borers in maize. In: Burton EN, Williams PV (eds) Crop Protection Research Advances, Nova, New York, p 57–100Google Scholar
  28. Mietkiewski R, Gorski R (1995) Growth of selected entomopathogenic fungi species and isolates on media containing insecticides. Acta Mycol 30:27–33Google Scholar
  29. Moore D, Prior C (1996) Mycoinsecticides. In: Upadhyay RK, Mukerjee KG, Rajak RL (eds) IPM system in Agriculture, Vol. II Biocontrol in Emerging Biotechnology. Aditya, New Delhi, pp 25–56Google Scholar
  30. Pevling R, Weyrich J (1992) Effects of neem oil, B. bassiana and Dieldrin on non target tenebrionid beetle in desert zone of the Republic of Niger. Biological control of Locusts and Gras hoppers: Proceedings of the Workshop held at International Institute of Tropical Agriculture: Cotonou, Republic of Nenin, April–May 1991, CABI, Wallingford, p 321–336Google Scholar
  31. Quesada-Moraga E, Navas-Cortez JA, Maranhao EAA, Ortiz-Urquiza A, Santiago Alvarez C (2007) Factors affecting the occurrence and distribution of entomopathogenic fungi in natural and cultivated soils. Mycol Res III:947–966CrossRefGoogle Scholar
  32. Rahman KMA, Barta M, Cagan L (2010) Effect of combining Beauveria bassiana and Nosema pyrausta on the mortality of Ostrinia nubilalis. Cent Eur J Biol 5:472–480CrossRefGoogle Scholar
  33. Sandner H, Cichy D (1967) Research on the effectiveness of fungal and bacterial insecticides. Ekol Pol Ser A 15:325–333Google Scholar
  34. SAS Institute (2011) SAS User’s Guide: Statistics. Version 18. SAS Institute, CaryGoogle Scholar
  35. St. Leger RJ, Wang C, Fang W (2011) New perspectives on insect pathogens. Fungal Biol Rev 25:84–88CrossRefGoogle Scholar
  36. Thomas MB, Watson EL, Valverde-Garcia P (2003) Mixed infections and insect pathogen interactions. Ecol Lett 6:183–188CrossRefGoogle Scholar
  37. Tsitsipis JA (1984) Rearing the corn borer, Sesamia nonagrioides on the artifiacial media in the lab. XVII International Congress of Entomology, Hamburg, Abstract Volume, pp 316Google Scholar
  38. Tsitsipis JA (1990) Contribution toward the development of an integrated control method for the corn stalk borer Sesamia nonagrioides (Lef.). In: Casida JE (ed) Pesticides and Alternatives. Elsevier, Amsterdam, pp 217–228Google Scholar
  39. Velasco P, Revilla P, Butron B, Ordas B, Ordas A, Malvar RA (2002) Ear damage of sweet corn inbreds and their hybrids under multiple corn borer infestation. Crop Sci 42:724–729CrossRefGoogle Scholar
  40. Wraight SP, Ramos ME (2005) Synergistic interaction between Beauveria bassiana- and Bacillus thuringiensis tenebrionis-based biopesticides applied against field populations of Colorado potato beetle larvae. J Invertebr Pathol 90:139–150PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg and the University of Milan 2012

Authors and Affiliations

  • Spiridon Mantzoukas
    • 1
  • Panagiotis Milonas
    • 2
  • Dimitris Kontodimas
    • 2
  • Kostas Angelopoulos
    • 1
  1. 1.Laboratory of Plant Physiology, Department of BiologyUniversity of PatrasPatrasGreece
  2. 2.Department of Entomology and Agricultural ZoologyBenaki Phytopathological InstituteAthensGreece

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