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

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.

Early-Life Sublethal Thiacloprid Exposure to Honey Bee Larvae: Enduring Effects on Adult Bee Cognitive Abilities

“…We showed that chronic larval exposure to thiacloprid impaired honey bee response to sucrose in emerged bees along with olfactory associative learning and memory performance. The results are consistent with previous research that indicated thiacloprid adversely affected honey bee cognitive performance [ 17 , 24 ]. Sucrose sensitivity was used as an important indicator of foraging efficiency.…”

“…Similar adverse effects on learning and memory have been mentioned in previous research on adult bees (honey bee or stingless bees) exposed to thiacloprid [11,16,24]. Furthermore, these findings demonstrated that despite surviving to adulthood, honey bee larvae exposed to thiacloprid experience cognitive disorders after emerging, which aligns with the impaired olfactory associative behavior identified in honey bees exposed to imidacloprid or thiacloprid [17].…”

“…Honey bee decline is correlated with the use of neonicotinoid insecticides [ cloprid, a widely used neonicotinoid, has been found at high field-realistic levels pollen and nectar [30]. Studies have shown the adverse effects of thiacloprid on ho health [12,17,24], foraging [16], homing [31], social abilities [32], and cognitive b [33].…”

“…Thiacloprid has been found to disrupt honey bee physiological homeostasis [ 12 ], decrease survival rates in honey bee colonies, compromise immunocompetence [ 13 ], disrupt metabolism [ 14 ], and induce transcriptional alterations in the brain of honey bee [ 15 ]. Furthermore, thiacloprid exposure has been shown to disturb foraging and homing behaviors [ 16 ] as well as cognitive performance [ 17 ] of honey bees. While previous investigations have mostly concentrated on the harmful toxic impacts of thiacloprid on adult honey bees, it is worth mentioning that honey bees can transport thiacloprid to the hive through the collection of nectar or pollen during foraging.…”

Architecture and potential roles of a delta-class glutathione S-transferase in protecting honey bee from agrochemicals

“…In agroecosystems, honey bees are also likely to be exposed to numerous agrochemicals, including insecticides, herbicides, and fungicides (Mullin et al, 2010;Johnson, 2015). Accumulated studies have provided insights into the acute toxicity and sublethal impacts of xenobiotic exposure on bees' foraging, learning, memory, gut microbiota, and immunity (El Hassani et al, 2005Yang et al, 2008;Hladun et al, 2012;Williamson et al, 2014;Balbuena et al, 2015;Wright et al, 2015;Di et al, 2016;Motta et al, 2018;DesJardins et al, 2021;Kadlikova et al, 2021;Ke et al, 2023). Interestingly, when present at low concentrations, certain xenobiotics have been found to exhibit hormetic effects that can benefit honey bee health (Köhler et al, 2012;Wright et al, 2013;Cutler et al, 2022).…”