Combining entomopathogenic Pseudomonas bacteria, nematodes and fungi for biological control of a below-ground insect pest

Below-ground insect pests are challenging to control because they are hard to target with control measures. Moreover, broad spectrum insecticides are or will soon be banned due to their negative effects on non-target organisms. In this study, we have developed a biological control method for the cabbage maggot Delia radicum (Diptera: Anthomyiidae), a significant pest of Brassicacean crops, based on a consortium of three biocontrol agents (BCAs). We chose the bacterium Pseudomonas chlororaphis because it can be used in a dual strategy against insect pests and fungal plant diseases, and combined it with the nematode Steinernema feltiae and the fungus Metarhizium brunneum that have a long history of commercial use against different pest insects. Our aim was to combine BCAs with different modes of action in order to achieve a stable and reliable biocontrol effect. We first tested double combinations of the bacterium with either the nematode or the fungus for improved potential to kill D. radicum in laboratory assays. We then evaluated the effect of double and triple combinations on D. radicum development and maggot-induced damage on radish bulbs in a series of pot experiments with artificial cabbage maggot infection performed in the greenhouse and outdoors and finally in a field trial with a natural infestation. Our results show that i) insecticidal pseudomonads are highly efficient in D. radicum control, ii) the three BCAs are compatible and neither inhibit each other’s infectiousness nor survival in the soil or on the roots, iii) synergistic effects of Pseudomonas-nematode and Pseudomonas-fungus combinations on maggot killing are possible, and iv) the triple combination reduced both pest survival in greenhouse experiments and maggot-induced damage on radish bulbs in the field by 50% each. The strategy we present here is a promising step forward to a reliable and efficient environmentally friendly biological control method for the cabbage maggot, which can also be adapted to other problematic below-ground pests.