To increase the development potential of botanical pesticides, it is necessary to expand the toxicology research on plant secondary metabolites. Herein, the Hyphantria cunea larvae were exposed to tannic acid concentrations consistent with those found in larch needles, and, subsequently, the growth and nutrient utilization, oxidative damage, and detoxification abilities in the larval midgut, as well as the changes in the gut microbiome, were analyzed. Our results revealed that tannic acid treatment significantly increased the mortality of H. cunea larvae and inhibited larval growth and food utilization. The contents of malondialdehyde and hydrogen peroxide in the larval midgut were significantly elevated in the treatment group, along with a significant decrease in the activities of antioxidant enzymes and detoxifying enzymes. However, the non-enzymatic antioxidants showed a significant increase in the tannic acid-treated larvae. From gut microbiome analysis in the treatment group, the abundance of gut microbiota related to toxin degradation and nutrient metabolism was significantly reduced, and the enrichment analysis also suggested that all pathways related to nutritional and detoxification metabolism were substantially inhibited. Taken together, tannic acid exerts toxic effects on H. cunea larvae at multiple levels and is a potential botanical pesticide for the control of H. cunea larvae.

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