Impairments in learning and memory performances associated with nicotinic receptor expression in the honeybee Apis mellifera after exposure to a sublethal dose of sulfoxaflor

Abstract

Sulfoxaflor is a new insecticide which acts on the nicotinic acetylcholine receptor (nAChRs) in a similar way to neonicotinoids. However, sufloxaflor (SFX) is thought to act in a different manner and is thus proposed as an alternative in crop protection. The goal of this study is to evaluate the toxicity of SFX and its sublethal effect on the honeybee Apis mellifera after acute exposure. In toxicological assay studies, the LD50 value and sublethal dose (corresponding to the NOEL: no observed effect level) were 96 and 15 ng/bee, respectively. Using the proboscis extension response paradigm, we found that an SFX dose of 15 ng/bee significantly impairs learning and memory retrieval when applied 12 h before conditioning or 24 h after olfactory conditioning. SFX had no effect on honeybee olfactory performance when exposure happened after the conditioning. Relative quantitative PCR experiments performed on the six nicotinic acetylcholine receptor subunits demonstrated that they are differently expressed in the honeybee brain after SFX exposure, whether before or after conditioning. We found that intoxicated bees with learning defects showed a strong expression of the Amelβ1 subunit. They displayed overexpression of Amelα9 and Amelβ2, and down-regulation of Amelα1, Amelα3 and Amelα7 subunits. These results demonstrated for the first time that a sublethal dose of SFX could affect honeybee learning and memory performance and modulate the expression of specific nAChR subunits in the brain.

Field-realistic exposure to neonicotinoid and sulfoximine insecticides impairs visual and olfactory learning and memory in Polistes paper wasps

“…As A. mellifera and P. fuscatus have similar body sizes, it is initially surprising that relatively low doses of sulfoxaflor caused increased wasp mortality. Similar doses did not increase mortality in A. mellifera (Barascou et al, 2022;Capela et al, 2022;Cartereau et al, 2022). One possibility is that training may be somewhat stressful, such that the combination of sulfoxaflor treatment and training could increase wasp death rates beyond what we would see with sulfoxaflor treatment alone.…”

“…Surprisingly, our study also found that wasps treated with sulfoxaflor had lower survival than wasps from other treatment groups. The median lethal dose (LD 50 ) of sulfoxaflor is estimated to be between 96 ng per bee (Cartereau et al, 2022) and 146 ng per bee (ESFA, 2014) in the honeybee Apis mellifera. The dose used in this study (20 ng per wasp) was 14-20% of the A. mellifera LD 50 .…”

“…These estimates consider measured nectar residue concentrations of the insecticides as well as typical daily nectar and/or pollen consumption. The dosages used in this study are also within the range used in other studies for both imidacloprid (Iqbal et al, 2019;Mustard et al, 2020;Siviter et al, 2021;Tan et al, 2015) and sulfoxaflor (Barascou et al, 2022;Capela et al, 2022;Cartereau et al, 2022). For the control treatment, equal aliquots of acetone were added to 50% (w/w) sucrose solution.…”

Critical roles of nicotinic acetylcholine receptors in olfactory memory formation and retrieval in crickets

“…In insects, many nAChR agonists other than nicotine (such as neonicotinoid: clothianidin, imidacloprid, thiacloprid, thiamethoxam, dinotefuran; sulfoximine: sulfoxaflor; butanolide: flupyradifurone) are applied as pesticides (Casida, 2018). The effects of these pesticides have attracted interest in the context of sublethal biological effects on beneficial insects, especially honey bees, and learning and memory is one of the extensively documented fields (Fischer et al, 2014;Hesselbach and Scheiner, 2018;Tison et al, 2019;Mustard et al, 2020;Tasman et al, 2021;Cartereau et al, 2022). Contrary to the effects of nicotine in the present study, all of the pesticidal nAChR agonists showed inhibitory effects on learning and memory in honey bees.…”

Sublethal Effects of Four Insecticides Targeting Cholinergic Neurons on Partner and Host Finding in the Parasitic Wasp Nasonia vitripennis

“…The compounds have a higher affinity for the nAChR in arthropods than for those of mammals, lowering their health risk for humans (Nauen et al, 2015; Watson et al, 2011; Yamada et al, 1999). However, recent studies on bees suggest that flupyradifurone (Siviter & Muth, 2022; Tan et al, 2017; Tosi & Nieh, 2019; Tosi et al, 2021) and sulfoxaflor (Cartereau et al, 2022; Siviter et al, 2018) may also cause negative sublethal effects, such as compromising the learning ability and performance of these pollinators, whereas other studies did not find any adverse effects of sulfoxaflor (Siviter et al, 2019; Tamburini et al, 2021). Another class of insecticides also targeting cholinergic neurons is the organophosphates.…”