The generalist entomopathogenic fungus, Metarhizium brunneum, has proved to have great potential as a versatile biological pest control agent. The gall midge Aphidoletes aphidimyza is a specialist predator that occurs naturally in Europe and has been successfully used for aphid suppression. However, the interaction between these two biological control organisms and how it may affect the biological control of aphids awaits further investigation. As part of the EU-supported project INBIOSOIL, this study was conducted in greenhouse conditions to assess the possible effects of combining both biological control agents. In a randomized complete block design, sweet corn (Zea mays var. saccharata) plants were grown in large pots filled with natural soil or natural soil inoculated with M. brunneum. At the third leaf stage, before being individually caged, plants were infested with Rhopalosiphum padi and A. aphidimyza pupae were introduced in the soil. Aphidoletes aphidimyza midge emergence, number of living midges and number of aphids were recorded daily. The presence of conidia in the soil and on leaves was assessed during the experiment. At the conclusion of the experiment, the number of live aphids and their developmental stage, consumed aphids, and A. aphidimyza eggs was assessed under stereomicroscope. This study’s findings showed that the presence of M. brunneum did not affect A. aphidimyza midge emergence. However, longevity was significantly affected. As the study progressed, significantly fewer predatory midges were found in cages treated with M. brunneum compared to untreated cages. Furthermore, by the end of the study, the number of predatory midges found in the Metarhizium-treated cages was four times lower than in the untreated cages. Both daily and final count of aphids were significantly affected by treatment. Aphidoletes aphidimyza applied alone suppressed the aphid population more effectively than M. brunneum applied alone. Additionally, the aphid population was most suppressed when both agents were combined, though the suppression was less than additive.

Biological control with entomopathogenic fungi is a feasible option for regulation of pest insect populations. However, possible effects on beneficial arthropods must be considered. We assessed the non-target effects of the microbial biological control agent Metarhizium brunneum (isolate BIPESCO 5/F 52) applied in soil on four different predatory arthropods: the predatory mite Gaeolaelaps aculeifer (Canestrini), the predatory bug Orius majusculus (Reuter), the rove beetle Dalotia coriaria (Kraatz) and the gall midge Aphidoletes aphidimyza Rondani. All are widespread and naturally occurring in Europe, they represent different classes of arthropods and different insect orders; furthermore, their life cycles involve different levels of contact with the soil. Adult G. aculeifer, O. majusculus, and D. coriaria, and last instar A. aphidimyza larvae were exposed to natural soil (control) or natural soil inoculated with M. brunneum at a concentration of 5 x 10 6 conidia/g of soil; this represents a worst-case scenario. Mortality, longevity, fecundity and Metarhizium outgrowth on dead individuals were assessed for the first three species; for A. aphidimyza, only mortality (non-emergence rate) and fecundity of emerged females were assessed. The fungal treatment resulted in a significantly higher mortality of O. majusculus and D. coriaria, 96%, and 7.3% respectively, compared with 19%, and 2% for their respective controls. Mortality of G. aculeifer was not significantly affected by exposure to the fungus in the soil. Longevity of O. majusculus and D. coriaria was significantly reduced following exposure to the fungus in the soil (log-rank test: p< 0.0001, Wilcoxon test p< 0.0001 and log-rank test: p=0.029, Wilcoxon test: p=0.027, respectively), while G. aculeifer longevity was not affected. Fecundity of O. majusculus and D. coriaria was negatively affected following exposure to the fungus in the soil, which reduced their oviposition by 20% and 4%, respectively, compared with the control, while G. aculeifer fecundity was not affected. Aphidoletes aphidimyza larval mortality was higher following exposure to the fungus in the soil (60% dead) than in the control (40% dead) but its fecundity was not statistically significantly affected by treatment. In conclusion, the predatory arthropods studied demonstrated a range of fitness responses to M. brunneum exposure in the soil, from no response (G. aculeifer), to intermediate (D. coriaria and A. aphidimyza) and high response (O. majusculus). This study demonstrates the relevance of using several fitness parameters and different arthropod species to determine whether a biological control agent should be considered a low-risk substance with respect to non-target effects.

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