Chronic Exposure to Field-Level Thiamethoxam Impairs Gut Tissue and Reduces Honeybee (Apis cerana) Survival

Pesticides such as neonicotinoids frequently harm beneficial insect pollinators and affect their survival, social behavior, digestive system, and metabolism. Investigating the mechanisms behind these impairments is crucial for enhancing pesticide risk assessments. <i>Apis cerana</i>, a native honeybee species in Asia, has received limited research attention regarding the toxicological mechanisms of thiamethoxam (TMX) exposure. We exposed newly emerged worker bees of <i>A. cerana</i> to a field-relevant dose of TMX (400 ng/g) under laboratory conditions to examine whether TMX exposure triggers similar or distinct effects in different biological processes and tissues. Our results demonstrate that TMX damages the gut cell structure and significantly increases mortality. Gut transcriptomic analysis revealed that the activation of signaling pathways such as glycosphingolipid biosynthesis, Notch signaling, and Wnt signaling likely contributed to structural damage in gut cells. Head transcriptomic results indicated that the activation of pathways including pyruvate metabolism, glycolysis/gluconeogenesis, thiamine metabolism, and riboflavin metabolism might negatively affect the stability of the neural system in <i>A. cerana</i>. The metabolic dysfunction of glycine, serine, threonine, as well as glycerophospholipids potentially impairs the neural system, leading to behavioral abnormalities and mortality. In summary, field-level TMX damages the gut cell structure, destabilizes the neural system, and increases the mortality rate of <i>A. cerana</i>. These findings demonstrate that TMX exposure induces complex, tissue-specific effects. This study provides a comprehensive understanding of the molecular and physiological impacts of TMX on <i>A. cerana</i>, offering valuable insights for the conservation and protection of this important pollinator species.