Pesticide stress on plants negatively affects parasitoid fitness through a bypass of their phytophage hosts

Pesticides taken up by plants from the soil or interstitial (pore) water can cascade to higher trophic levels, which are expected to be more affected due to cumulative bottom-up effects. Knowledge about the impact of indirect exposure to pesticides on non-target terrestrial trophic chains, however, is still lacking. Therefore, we examined the direct and indirect effects of three concentrations of the herbicide 2,6-dichlorobenzonitrile (DCBN) and an insecticide with a similar molecular structure (1,4-dichlorobenzene, DCB) on the fitness traits of a tritrophic system: the wheat plant Triticum aestivum, the aphid Sitobion avenae and its specialist parasitoid Aphidius rhopalosiphi. To mimic exposure via interstitial water the toxicants were added to the growth medium of the plant. Passive dosing between the medium and a silicon layer was used to achieve constant exposure of the poorly soluble pesticides. Wheat plants exposed to both pesticides grew smaller and had reduced biomasses. Negative effects on the reproductive rate, biomass and the number of aphids were only observable at the highest concentration of DCBN. Overall parasitism rate decreased when exposed to both pesticides and parasitoid attack rates decreased at lower concentrations of DCBN and at the highest DCB concentration. The parasitoid sex ratio was extremely male-biased in the presence of DCBN. Our results demonstrate that pesticides can alter the performance of higher trophic levels by sublethal effects, through a bypass of the second trophic level. In addition, the novel test system used was suitable for detecting such carryover effects on non-target organisms.