Honeybee Cognition as a Tool for Scientific Engagement

Denton, Jai A.; Koludarov, Ivan; Thompson, Michele A.; Bryk, Jarosław; Velasque, Mariana

doi:10.3390/insects12090842

Cited by 3 publications

(4 citation statements)

References 58 publications

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“…The sub-lethal dose of thiacloprid used in our experiment was determined based on previous studies ( Tison et al, 2016 ; Shi et al, 2018 ). After the adult honeybees emerged, they were reared on 50% sucrose (w/w) in wooden cages, after which their learning and memory abilities were tested ( Denton et al, 2021 ) Electroantennography recording on honeybee antennae were conducted 7–8 days after emergence, from May to September 2022.…”

Section: Methodsmentioning

confidence: 99%

“…We tested the olfactory-associated learning acquisition and memory recall behaviors in 7-day-old adult honeybees exposed to thiacloprid during the larval stage. As the olfactory system does not fully develop until 2–3 days after emergence from the comb ( Denton et al, 2021 ), before the experiment, individual honeybees were habituated to the setup for 2 h, with the head restrained to a cylindrical copper tube and the abdomen free to move. Furthermore, honeybees that did not respond to the 30% sucrose (w/w) solution were eliminated from further testing.…”

Section: Methodsmentioning

confidence: 99%

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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: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

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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“…Associative olfactory learning and memory assays: A total of 68–76 honey bees per treatment group were used to evaluate their learning and memory performances on Day 21, which is the time when the honey bee’s olfactory system has fully developed [ 29 ]. We applied hexanal (66-25-1, Sigma, St. Louis, MO, USA) as a conditioned stimulus (CS+) paired with a 30% sugar stimulus (unconditioned stimulus, US), and R-limonene, which served as the other conditioned stimulus (CS-) (95327-98-3, Sigma, St. Louis, MO, USA), was not paired with any sucrose.…”

Section: Methodsmentioning

confidence: 99%

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

Chen,

Li,

Yin

et al. 2023

Toxics

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Honey bees have significant ecological and economic value as important pollinators, but they are continuously exposed to various environmental stressors, including insecticides, which can impair their health and cause colony decline. (1) Background: Cognitive abilities are vital for the functional maintenance of honey bees; however, it remains unknown if chronic, low-dose exposure to thiacloprid during the larval stage impairs the cognitive abilities of emerged adult honey bees. (2) Methods: To explore this question, honey bee larvae were fed 0, 0.5, and 1.0 mg/L thiacloprid during their developmental phase. Then, the cognitive (i.e., olfactory learning and memory) abilities of adult honey bees were quantified to assess the delayed impacts of early-stage thiacloprid exposure on adult honey bee cognition. Neural apoptosis and transcriptomic level were also evaluated to explore the neurological mechanisms underlying these effects. (3) Results: Our results revealed that chronic larval exposure to sublethal thiacloprid impaired the learning and memory abilities of adult honey bees by inducing neuronal apoptosis and transcriptomic alterations. (4) Conclusions: We highlighted a previously unknown impairment caused by thiacloprid in honey bees.

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“…The A. mellifera ligustica is a well-known and excellent insect for, how to establish a standard protocol for carrying out a study of behavioral plasticity under controlled conditions [6][7][8]. In honeybees, the proboscis extension response is a natural response in which they elongate their proboscis (elongated feeding tube) by touching the antenna with the sucrose solution.…”

Section: Introductionmentioning

confidence: 99%

Differential gene expression analysis following olfactory learning in honeybee (Apis mellifera L.)

et al. 2022

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Insects change their stimulus-response through the perception of associating these stimuli with important survival events such as rewards, threats, and mates. Insects develop strong associations and relate them to their experiences through several behavioral procedures. Among the insects, Apis species, Apis mellifera ligustica are known for their outstanding ability to learn with tremendous economic importance. Apis mellifera ligustica has a strong cognitive ability and promising model species for investigating the neurobiological basis of remarkable olfactory learning abilities. Here we evaluated the olfactory learning ability of A. mellifera by using the proboscis extension reflex (PER) protocol. The brains of the learner and failed-learner bees were examined for comparative transcriptome analysis by RNA-Seq to explain the difference in the learning capacity. In this study, we used an appetitive olfactory learning paradigm in the same age of A. mellifera bees to examine the differential gene expression in the brain of the learner and failed-learner. Bees that respond in 2nd and 3rd trials or only responded to 3rd trials were defined as learned bees, failed-learner individuals were those bees that did not respond in all learning trials The results indicate that the learning ability of learner bees was significantly higher than failed-learner bees for 12 days. We obtained approximately 46.7 and 46.4 million clean reads from the learner bees failed-learner bees, respectively. Gene expression profile between learners’ bees and failed-learners bees identified 74 differentially expressed genes, 57 genes up-regulated in the brains of learners and 17 genes were down-regulated in the brains of the bees that fail to learn. The qRT-PCR validated the differently expressed genes. Transcriptome analyses revealed that specific genes in learner and failed-learner bees either down-regulated or up-regulated play a crucial role in brain development and learning behavior. Our finding suggests that down-regulated genes of the brain involved in the integumentary system, storage proteins, brain development, sensory processing, and neurodegenerative disorder may result in reduced olfactory discrimination and olfactory sensitivity in failed-learner bees. This study aims to contribute to a better understanding of the olfactory learning behavior and gene expression information, which opens the door for understanding of the molecular mechanism of olfactory learning behavior in honeybees.

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Honeybee Cognition as a Tool for Scientific Engagement

Cited by 3 publications

References 58 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

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

Differential gene expression analysis following olfactory learning in honeybee (Apis mellifera L.)

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