Effectiveness of Bacillus thuringiensis -Transgenic Chickpeas and the Entomopathogenic Fungus Metarhizium anisopliae in Controlling Helicoverpa armigera (Lepidoptera: Noctuidae)

Abstract

The use of genetically modified (Bt) crops expressing lepidopteran-specific Cry proteins derived from the soil bacterium Bacillus thuringiensis is an effective method to control the polyphagous pest Helicoverpa armigera. As H. armigera potentially develops resistance to Cry proteins, Bt crops should be regarded as one tool in integrated pest management. Therefore, they should be compatible with biological control. Bioassays were conducted to understand the interactions between a Cry2Aa-expressing chickpea line, either a susceptible or a Cry2A-resistant H. armigera strain, and the entomopathogenic fungus Metarhizium anisopliae. In a first concentration-response assay, Cry2A-resistant larvae were more tolerant of M. anisopliae than susceptible larvae, while in a second bioassay, the fungus caused similar mortalities in the two strains fed control chickpea leaves. Thus, resistance to Cry2A did not cause any fitness costs that became visible as increased susceptibility to the fungus. On Bt chickpea leaves, susceptible H. armigera larvae were more sensitive to M. anisopliae than on control leaves. It appeared that sublethal damage induced by the B. thuringiensis toxin enhanced the effectiveness of M. anisopliae. For Cry2A-resistant larvae, the mortalities caused by the fungus were similar when they were fed either food source. To examine which strain would be more likely to be exposed to the fungus, their movements on control and Bt chickpea plants were compared. Movement did not appear to differ among larvae on Bt or conventional chickpeas, as indicated by the number of leaflets damaged per leaf. The findings suggest that Bt chickpeas and M. anisopliae are compatible to control H. armigera.

Susceptibility of Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) to the Entomopathogenic Fungus Metarhizium anisopliae when Feeding on Bacillus thuringiensis Cry3Bb1-Expressing Maize

“…Although 18 to 60% of dead larval and adult bodies lacked signs of fungal development, those larvae and adults might still have died because of the fungus, but the fungus may have failed to develop further under the given conditions (e.g., because the body cavity was damaged or because the fungus was unable to compete with other microorganisms in the dead insect). Similar findings were reported by Lawo et al (22) and Pilz et al (37). Death may also have been caused, however, by other pathogens or nutritional deficiencies, which is evident from the mortality in the control treatments without fungal exposure.…”

“…Multitrophic relationships may also be influenced by insect movement and behavior. Lawo et al (22) found no differences in the feeding behavior of the lepidopteran larvae on Bt or control plants, suggesting that the larvae had similar exposures to fungal spores, which had been applied to the leaf surface before the leaves were provided to the larvae. However, depending on the insect species and the B. thuringiensis protein concentrations, feeding on Bt plants may result in reduced movement due to sublethal damage or, in contrast, in higher activity if the larvae search for better food (40).…”

“…This indicates that the effects of Bt maize and M. anisopliae on D. v. virgifera were additive rather than synergistic or antagonistic in our laboratory assays. The interaction between plant-expressed, genetically engineered Cry2Aa protein, herbivorous Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), and M. anisopliae was studied by Lawo et al (22). Larvae of a Cry2Aa-susceptible H. armigera strain fed on chickpea leaves containing the B. thuringiensis protein were more sensitive to the fungus than those fed on control leaves, while the sensitivities of larvae from a strain resistant to Cry2Aa were similar on both kinds of leaves.…”

“…The interactions of B. thuringiensis proteins produced in genetically engineered plants and entomopathogenic fungi, however, have been examined so far only for lepidopteran pests. Lawo et al (22) demonstrated that B. thuringiensis-susceptible caterpillars were more sensitive to the fungus when feeding on Bt chickpea than when feeding on nontransformed control plants, while infection rates were similar for a B. thuringiensis-resistant strain. In addition, Johnson et al (16,17) reported that B. thuringiensissusceptible caterpillars showed higher infection rates than B. thuringiensis-resistant ones when feeding on Bt tobacco.…”

Ecological compatibility of GM crops and biological control

“…Research in this area includes experiments in which Cry toxin or bacteria (e.g., Bacillus thuringiensis kurstaki) were added to the surface of plants or were media-incorporated. Sublethal exposure of the host to Bt chickpea enhanced pest susceptibility to the entomopathogenic fungus Metarhizium anisopliae (Lawo et al, 2008). Synergistic interactions also were found between Cry toxin and entomopathogenic fungi (Reardon et al, 2004;Wraight and Ramos, 2005).…”