ArticleProceedings. Biological sciences2016
Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees.
Article in Proceedings. Biological sciences, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 40 papers, 1 of them a synthesis that pooled it.
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Who cites it
40 citing papers in PubMed, 1 synthesis or guideline pooled it, 95 citations in OpenAlex.
- Fungicides, herbicides and bees: A systematic review of existing research and methods.PloS one · 2019Pooled it
- Article
- Review
- The Sublethal Effects of Neonicotinoids on Honeybees.Biology · 2025Review
- Microsporidian parasite impairs colony fitness in bumblebees.Open biology · 2025Article
- Evaluation of Functional Properties of Some Lactic Acid Bacteria Strains for Probiotic Applications in Apiculture.Microorganisms · 2024Article
- Honeybee visitation to shared flowers increasesEcology and evolution · 2023Article
- Acaricidal Toxicity of Four Essential Oils, Their Predominant Constituents, Their Mixtures againstInsects · 2023Article
- Contrasting effects of fungicide and herbicide active ingredients and their formulations on bumblebee learning and behaviour.The Journal of experimental biology · 2023Article
- Reduction of stress responses in honey bees by synthetic ligands targeting an allatostatin receptor.Scientific reports · 2022Article
- Field and Cage Studies Show No Effects of Exposure to Flonicamid on Honey Bees at Field-Relevant Concentrations.Insects · 2022Article
- Discovery of octopamine and tyramine in nectar and their effects on bumblebee behavior.iScience · 2022Article
- Thiamethoxam as an inadvertent anti-aphrodisiac in male bees.Toxicology reports · 2022Article
- Review
- Artificial Diets Modulate Infection Rates byMicroorganisms · 2021Article
- Viral impacts on honey bee populations: A review.Saudi journal of biological sciences · 2021Review
- The Power ofFrontiers in physiology · 2021Review
- Effects of Nosema ceranae (Dissociodihaplophasida: Nosematidae) and Flupyradifurone on Olfactory Learning in Honey Bees, Apis mellifera (Hymenoptera: Apidae).Journal of insect science (Online) · 2020Article
- Landscape-level toxicant exposure mediates infection impacts on wildlife populations.Biology letters · 2020Article
- Factors Associated with Honey Bee Colony Losses: A Mini-Review.Veterinary sciences · 2020Review
Corrections and comments
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Authors and funding
2 authors at 1 institution in 2 countries.
Funding
No grant is acknowledged in the PubMed record.
Abstract
Learning and memory are crucial functions which enable insect pollinators to efficiently locate and extract floral rewards. Exposure to pesticides or infection by parasites may cause subtle but ecologically important changes in cognitive functions of pollinators. The potential interactive effects of these stressors on learning and memory have not yet been explored. Furthermore, sensitivity to stressors may differ between species, but few studies have compared responses in different species. Here, we show that chronic exposure to field-realistic levels of the neonicotinoid clothianidin impaired olfactory learning acquisition in honeybees, leading to potential impacts on colony fitness, but not in bumblebees. Infection by the microsporidian parasite Nosema ceranae slightly impaired learning in honeybees, but no interactive effects were observed. Nosema did not infect bumblebees (3% infection success). Nevertheless, Nosema-treated bumblebees had a slightly lower rate of learning than controls, but faster learning in combination with neonicotinoid exposure. This highlights the potential for complex interactive effects of stressors on learning. Our results underline that one cannot readily extrapolate findings from one bee species to others. This has important implications for regulatory risk assessments which generally use honeybees as a model for all bees.
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Registered trials
Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.