Thiacloprid impairs honeybee worker learning and memory with inducing neuronal apoptosis and downregulating memory-related genes

Neonicotinoids are among the most widely used insecticides in the world and are recognized as a potential cause of pollinator decline. Previous studies have demonstrated that the neonicotinoid thiacloprid has adverse effects on forag-ing and memory behaviors. However, there is no direct evidence linking thiacloprid-induced neuronal cell damage in the brains of honeybees to learning and memory dysfunction. Adult honeybee (Apis mellifera L.) workers were chron-ically exposed to sub-lethal concentrations of thiacloprid. We discovered that thiacloprid negatively affected their sur-vival, food consumption, and body weight. In addition, sucrose sensitivity and memory performance were impaired. We evaluated the apoptosis of honeybee brain cells using TUNEL (Terminal deoxynucleotidyl transferase-mediated digoxigenin-dUTP-biotin nick-end labeling) and Caspase-3 assays, which revealed that thiacloprid increases the dose-dependent apoptosis of neurons in the mushroom bodies (MB) and antennal lobes (AL). We also determined the abnormal transcripts of multiple genes, including vitellogenin (Vg), immune system genes (apidaecin and catalase), and memory-associated genes (pica, creb, Nmdar1, Dop2, Oa1, Oa-2R, and Oa-3R). These results indicate that exposure to sublethal concentrations of thiacloprid cause abnormal expression of memory-related genes and apoptosis of brain cells in the AL and MB, which may contribute to the memory disorder induced by thiacloprid exposure.

Automated summary

This study found that sub-lethal concentrations of thiacloprid not only negatively affected the survival, food consumption, and body weight of honeybees, but also impaired their sucrose sensitivity and memory performance. Furthermore, thiacloprid increased the dose-dependent apoptosis of neurons in the mushroom bodies and antennal lobes, as well as caused abnormal expression of memory-associated genes. These findings suggest that exposure to sublethal concentrations of thiacloprid can induce memory disorder through the disruption of sucrose perception and apoptosis of brain cells.