Chronic larval exposure to thiacloprid impairs honeybee antennal selectivity, learning and memory performances

Li Ke; Xiasang Chen; Pingli Dai; Yong-Jun Liu

doi:10.3389/fphys.2023.1114488

Chronic larval exposure to thiacloprid impairs honeybee antennal selectivity, learning and memory performances

Front Physiol. 2023 Apr 20:14:1114488. doi: 10.3389/fphys.2023.1114488. eCollection 2023.

Authors

Li Ke^{1

2}, Xiasang Chen^{1

2}, Pingli Dai^{1

2}, Yong-Jun Liu^{1

2}

Affiliations

¹ State Key Laboratory of Resource Insects, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China.
² Key Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, China.

Abstract

The use of agricultural neonicotinoid insecticides has sub-lethal chronic effects on bees that are more prevalent than acute toxicity. Among these insecticides, thiacloprid, a commonly used compound with low toxicity, has attracted significant attention due to its potential impact on the olfactory and learning abilities of honeybees. The effect of sub-lethal larval exposure to thiacloprid on the antennal activity of adult honeybees (Apis mellifera L.) is not yet fully understood. To address this knowledge gap, laboratory-based experiments were conducted in which honeybee larvae were administered thiacloprid (0.5 mg/L and 1.0 mg/L). Using electroantennography (EAG), the impacts of thiacloprid exposure on the antennal selectivity to common floral volatiles were evaluated. Additionally, the effects of sub-lethal exposure on odor-related learning and memory were also assessed. The results of this study reveal, for the first time, that sub-lethal larval exposure to thiacloprid decreased honeybee antenna EAG responses to floral scents, leading to increased olfactory selectivity in the high-dose (1.0 mg/L) group compared to the control group (0 mg/L vs. 1.0 mg/L: p = 0.042). The results also suggest that thiacloprid negatively affected odor-associated paired learning acquisition, as well as medium-term (1 h) (0 mg/L vs. 1.0 mg/L: p = 0.019) and long-term memory (24 h) (0 mg/L vs. 1.0 mg/L: p = 0.037) in adult honeybees. EAG amplitudes were dramatically reduced following R-linalool paired olfactory training (0 mg/L vs. 1.0 mg/L: p = 0.001; 0 mg/L vs. 0.5 mg/L: p = 0.027), while antennal activities only differed significantly in the control between paired and unpaired groups. Our results indicated that exposure to sub-lethal concentrations of thiacloprid may affect olfactory perception and learning and memory behaviors in honeybees. These findings have important implications for the safe use of agrochemicals in the environment.

Keywords: Apis mellifera L.; antenna; electroantennography; learning and memory; thiacloprid.

Grants and funding

This work was supported by the National Natural Science Foundation of China (31772683) and Chinese Academy of Agricultural Sciences (Elite Youth Program to Y-JL).