Sub-lethal doses of sulfoxaflor impair honey bee homing ability

Capela, Nuno; Sarmento, Artur; Simões, Sandra; Azevedo-Pereira, Henrique M.V.S.; Sousa, José Paulo

doi:10.1016/j.scitotenv.2022.155710

Cited by 14 publications

(8 citation statements)

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“…Prior studies have extensively investigated the negative impacts of sub-lethal doses of neonicotinoid insecticides on honeybees ( Blacquiere et al, 2012 ; Singla et al, 2020 ), including physiological changes ( Catae et al, 2018 ; Roat et al, 2020 ; Lv et al, 2023 ), delayed development ( Li et al, 2022 ), weakened immune response ( Chmiel et al, 2019 ; Annoscia et al, 2020 ; Zhang et al, 2022 ), and impaired colony reproduction ( Schott, et al, 2021 ). Specifically, neonicotinoids disturb honeybee behaviors, including waggle dancing ( Tison et al, 2020 ), foraging and homing ( Capela et al, 2022 ), and colony performance ( Negi et al, 2022 ; Reiner et al, 2022 ). These impacts interact with honeybee pathogens (deformed wing virus, Israeli acute honeybee paralysis virus, etc.)…”

Section: Introductionmentioning

confidence: 99%

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

Chen

Dai

et al. 2023

Front. Physiol.

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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.

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Section: Introductionmentioning

confidence: 99%

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

Chen

Dai

et al. 2023

Front. Physiol.

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“…Newly emerged worker bees were collected from a normal colony and marked with paint, and then were returned to their colonies. After 20 days, we collected the marked 20-day-old forager bees that carried pollen to the entrances of hives during the morning, as described by Capela et al [ 64 ]. Then, all the foragers were placed randomly into cages (11 cm × 11 cm × 11 cm, n = 60 bees per cage) with a feeder.…”

Section: Methodsmentioning

confidence: 99%

Ternary Mixture of Azoxystrobin, Boscalid and Pyraclostrobin Disrupts the Gut Microbiota and Metabolic Balance of Honeybees (Apis cerana cerana)

Dong

Huang

Guo

et al. 2023

IJMS

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There is a growing risk of pollinators being exposed to multiple fungicides due to the widespread use of fungicides for plant protection. A safety assessment of honeybees exposed to multiple commonly used fungicides is urgently required. Therefore, the acute oral toxicity of the ternary mixed fungicide of ABP (azoxystrobin: boscalid: pyraclostrobin = 1:1:1, m/m/m) was tested on honeybees (Apis cerana cerana), and its sublethal effect on foragers’ guts was evaluated. The results showed that the acute oral median lethal concentration (LD50) of ABP for foragers was 12.6 μg a.i./bee. ABP caused disorder of the morphological structure of midgut tissue and affected the intestinal metabolism; the composition and structure of the intestinal microbial community was perturbed, which altered its function. Moreover, the transcripts of genes involved in detoxification and immunity were strongly upregulated with ABP treatment. The study implies that exposure to a fungicide mixture of ABP can cause a series of negative effects on the health of foragers. This work provides a comprehensive understanding of the comprehensive effects of common fungicides on non-target pollinators in the context of ecological risk assessment and the future use of fungicides in agriculture.

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“…Aliquots of the stock solutions were added to a 50% (w/w) sucrose solution to obtain the following treatment group concentrations: imidacloprid low dose (IMDL) 0.5 ng per wasp, imidacloprid high dose (IMDH) 2.0 ng per wasp, sulfoxaflor (SUL), 20 ng per wasp. Reports of fieldrealistic ranges for imidacloprid in a day's nectar load are 0.024-3.50 ng (Byrne et al, 2014;Cresswell, 2011) or 1-50 ppb (Goulson, 2013) and 1.4-142 ng for sulfoxaflor (Arnet, 2022;Barascou et al, 2022;Capela et al, 2022). These estimates consider measured nectar residue concentrations of the insecticides as well as typical daily nectar and/or pollen consumption.…”

Section: Insecticide Treatmentmentioning

confidence: 99%

“…Harnessed olfactory learning provides a well-controlled method for assessing learning, but wild bee behavior involves cues in multiple sensory modalities and movement. As a result, there has been increasing focus on insecticide effects on learning in multiple sensory modalities (Ludicke and Nieh, 2020;, natural foraging behavior (Barascou et al, 2022;Siviter et al, 2021) and motor abilities (Capela et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

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

Corcoran,

Tibbetts

2023

Journal of Experimental Biology

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Exposure to insecticides may contribute to global insect declines due to sublethal insecticide effects on non-target species. Thus far, much research on non-target insecticide effects has focused on neonicotinoids in a few bee species. Much less is known about effects on other insect taxa or newer insecticides, such as sulfoxaflor. Here, we studied the effects of an acute insecticide exposure on both olfactory and visual learning in free-moving Polistes fuscatus paper wasps. Wasps were exposed to a single, field-realistic oral dose of low-dose imidacloprid, high-dose imidacloprid or sulfoxaflor. Then, visual and olfactory learning and short-term memory were assessed. We found that acute insecticide exposure influenced performance, as sulfoxaflor- and high-dose imidacloprid-exposed wasps made fewer correct choices than control wasps. Notably, both visual and olfactory performance were similarly impaired. Wasps treated with high-dose imidacloprid were also less likely to complete the learning assay than wasps from the other treatment groups. Instead, wasps remained stationary and unmoving in the testing area, consistent with imidacloprid interfering with motor control. Finally, wasps treated with sulfoxaflor were more likely to die in the week after treatment than wasps in the other treatment groups. Our findings demonstrate that sublethal, field-realistic dosages of both neonicotinoid- and sulfoximine-based insecticides impair wasp learning and short-term memory, which may have additional effects on survival and motor functioning. Insecticides have broadly detrimental effects on diverse non-target insects that may influence foraging effectiveness, pollination services and ecosystem function.

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Sub-lethal doses of sulfoxaflor impair honey bee homing ability

Cited by 14 publications

References 50 publications

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

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

Ternary Mixture of Azoxystrobin, Boscalid and Pyraclostrobin Disrupts the Gut Microbiota and Metabolic Balance of Honeybees (Apis cerana cerana)

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

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