Abstract

Accumulating evidence suggests that neonicotinoids may have long-term adverse effects on bee health, yet our understanding of how this could occur is incomplete. Pesticides can act as endocrine disrupting chemicals (EDCs) in animals providing characteristic multiphasic dose-response curves and non-lethal endpoints in toxicity studies. However, it is not known if neonicotinoids act as EDCs in bees. To address this issue, we performed oral acute and chronic toxicity studies including concentrations recorded in nectar and pollen, applying acetamiprid, clothianidin, imidacloprid, and thiamethoxam to bumble bees, honey bees and leafcutter bees, the three most common bee species managed for pollination. In acute toxicity studies, late-onset symptoms, such as ataxia, were recorded as non-lethal endpoints for all three bee species. Clothianidin and thiamethoxam produced biphasic dose-response curves for all three bee species. Clothianidin and thiamethoxam were extremely toxic to winter worker honey bees prior to brood production in spring, making this the most sensitive bee stage identified to date. Chronic exposure to field-realistic levels of neonicotinoids reduced bee survival and caused significant late-onset symptoms for all three bee species. Given these findings, neonicotinoid risk should be reevaluated to address the EDC-like behavior and the sensitivity of winter worker honey bees.

Highlights

  • Bees maintain biodiversity and agricultural productivity by pollinating a wide range of flowering crops and wild plants

  • Clothianidin (χ2 = 319.6, df = 8, P < 0.01), imidacloprid (χ2 = 119.12, df = 8, P < 0.01) and thiamethoxam (χ2 = 113.19, df = 8, n = 48, P < 0.01) exposure resulted in biphasic dose-response curves illustrating an endocrine disrupting chemicals (EDCs)-like behavior

  • Delayed-onset symptoms (5 to 7 days after exposure) recorded for moderate to low exposure doses were specific to each neonicotinoid: clothianidin and thiamethoxam caused intermittent hyperactivity; acetamiprid, imidacloprid and thiamethoxam caused abnormal stance and slow movements

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Summary

Introduction

Bees maintain biodiversity and agricultural productivity by pollinating a wide range of flowering crops and wild plants. At field-realistic concentrations, the most common early-onset symptoms in pest insects and worker honey bees are behavioral changes including reduced responses to sex pheromones[29], impaired associative learning[30], impaired short-term memory[31], and impaired movement[32]. These behavioral changes were observed in oral chronic toxicity studies applying field-realistic concentrations of thiamethoxam to bumble bee colonies[33]. No studies have examined the outcome of winter honey bee susceptibility to neonicotinoids in spring, when the hormone systems are upregulated

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