Direct and indirect side effects of pesticides used in German apple production on the braconid wasp Ascogaster quadridentata (Hymenoptera: Braconidae), a key natural enemy of the codling moth

In laboratory experiments, side effects ((sub-)lethal, behavioral, and transgenerational) of five pesticide formulations used in German apple production were investigated for the first time on the codling moth parasitoid Ascogaster quadridentata and its offspring. Adult parasitoid males were directly exposed to formulated products of azadirachtin, chlorantraniliprole, pyrethrine, quassin and lime sulfur, applied in field recommended rates on treated glass plates. Direct toxicity was assessed daily after treatment until all wasps died. Female wasps were exposed to treated host eggs and subsequent parasitism behavior and olfactory responses were evaluated to determine sublethal and behavioral effects. Successful reproduction of females exposed to treated host eggs and the emergence of their offspring was recorded, allowing assessment of potential transgenerational effects. While pyrethrin and sulfur formulation caused significant higher mortality in adult wasps, the other pesticides did not reduce survival probability in comparison to the control. The larvicides (chlorantraniliprole, azadirachtin) induced transgenerational effects by increased host mortality and interference with host recognition. Quassia and lime sulfur caused only negligible impacts. Behavioral assays indicated that treatment of codling moth eggs with the formulated azadirachtin as well as its blank formulation alone obviously masked necessary cues for successful host location, thus reducing parasitism. Such indirect and transgenerational effects can substantially affect A. quadridentata performance, even when direct adult mortality is low. Our findings demonstrate that evaluating only acute adult mortality may underestimate side effects of pesticides on crop-specific key natural enemies and highlight the importance of incorporating sublethal and transgenerational effects into pesticide risk assessment and IPM decision-making.