Novel neonicotinoid flupyradifurone exhibits sublethal toxicity to natural enemies ladybeetles Propylea japonica by disturbing multi-level metabolic systems.

Abstract

Flupyradifurone, a novel neonicotinoid insecticide widely used against sap-sucking pests, has poorly characterized sublethal effects on non-target natural enemies. We assessed sublethal effects of 0.5 and 3 mg/L flupyradifurone on Propylea japonica using biological, biochemical, transcriptomic, and metabolomic assays. Flupyradifurone significantly prolonged larval development and reduced adult body weight and fecundity, without affecting survival, pupation, or emergence. Enzyme activities (GST, POD and AChE) and nutritional substance contents (glycogen and free fatty acids) generally decreased at 12 and 24 h. However, CarE activity and total protein content showed no significant changes at 24 h. Transcriptomics analysis identified 1798 and 1607 differentially expressed genes, enriched in xenobiotic metabolism, immunity, and nutrient metabolism. Key genes GST, UGT, Duox, and TPS were significantly downregulated, whereas GLD was significantly upregulated, and Lys and FASN were significantly induced only at the low concentration. RNAi silencing of GST, UGT, Duox, TPS, and GLD increased ladybeetles susceptibility to flupyradifurone. Metabolomics analysis identified 483 and 508 differentially accumulated metabolites, with disruptions in glutathione, amino acid, and lipid metabolism. Thus, flupyradifurone suppresses detoxification and immunity, depletes energy reserves, and inhibits development and reproduction in P. japonica, highlighting the need to incorporate sublethal effects into ecological risk assessments.