We thank Dr Georgios Leontidis (The School of Natural and Computing Science, University of Aberdeen) for his valuable support during the selection and implementation of the ML models, and the two anonymous reviewers for providing useful feedback that helped improve the clarity and soundness of the manuscript. We are also grateful to NERC (Natural Environment Research Council) for funding this project and supporting MV's salary over 10 weeks through their Research Experience Placement programme (DTG reference: NE/S007377/1). The honeybee work that was performed to obtain the sequencing data used in this study was funded by the European Research Council under the European Union's Horizon 2020 research and innovation programme (grant no. 638873 to EL). This funding also supported FM during the execution of the field and molecular work. ; Peer reviewed ; Publisher PDF
1. Sulfoximine‐based insecticides, such as sulfoxaflor, are of increasing global importance and have been registered for use in 81 countries, offering a potential alternative to neonicotinoid insecticides. 2. Previous studies have demonstrated that sulfoxaflor exposure can have a negative impact on the reproductive output of bumblebee colonies, but the specific life‐history variables that underlie these effects remain unknown. 3. Here, we used a microcolony‐based protocol to assess the sub‐lethal effects of chronic sulfoxaflor exposure on egg laying, larval production, ovary development, sucrose consumption, and mortality in bumblebees. Following a pre‐registered design, we exposed colonies to sucrose solutions containing 0, 5, 10 and 250ppb of sulfoxaflor. Exposure at 5 ppb has been previously shown to negatively impact colony reproductive success. 4. Our results showed that sulfoxaflor exposure at 5 ppb (lowest exposure tested) reduced the number of eggs found within the microcolonies (Hedge's d = −0.37), with exposed microcolonies also less likely to produce larvae (Hedge's d = −0.36). Despite this, we found no effect of sulfoxaflor exposure on ovarian development. Sulfoxaflor‐exposed bumblebees consumed less sucrose solution, potentially driving the observed reduction in egg laying. 5. Policy implications. Regulatory bodies such as the European Food Safety Authority (EFSA) are under increasing pressure to consider the potential impact of insecticides on wild bees, such as bumblebees, but sublethal effects can go undetected at lower‐tier testing. In identifying just such an effect for bumblebees exposed to sulfoxaflor, this study highlights that microcolony‐based protocols are a useful tool that could be implemented within an ecotoxicology framework. Furthermore, the results provide evidence for potentially negative consequences of pollinator exposure to an insecticide that is currently undergoing the licensing process in several EU member states.
Most insecticides are insect neurotoxins. Evidence is emerging that sublethal doses of these neurotoxins are affecting the learning and memory of both wild and managed bee colonies, exacerbating the negative effects of pesticide exposure and reducing individual foraging efficiency.Variation in methodologies and interpretation of results across studies has precluded the quantitative evaluation of these impacts that is needed to make recommendations for policy change. It is not clear whether robust effects occur under acute exposure regimes (often argued to be more field‐realistic than the chronic regimes upon which many studies are based), for field‐realistic dosages, and for pesticides other than neonicotinoids.Here we use meta‐analysis to examine the impact of pesticides on bee performance in proboscis extension‐based learning assays, the paradigm most commonly used to assess learning and memory in bees. We draw together 104 (learning) and 167 (memory) estimated effect sizes across a diverse range of studies.We detected significant negative effects of pesticides on learning and memory (i) at field realistic dosages, (ii) under both chronic and acute application, and (iii) for both neonicotinoid and non‐neonicotinoid pesticides groups.We also expose key gaps in the literature that include a critical lack of studies on non‐Apis bees, on larval exposure (potentially one of the major exposure routes), and on performance in alternative learning paradigms. Policy implications. Procedures for the registration of new pesticides within EU member states now typically require assessment of risks to pollinators if potential target crops are attractive to bees. However, our results provide robust quantitative evidence for subtle, sublethal effects, the consequences of which are unlikely to be detected within small‐scale prelicensing laboratory or field trials, but can be critical when pesticides are used at a landscape scale. Our findings highlight the need for long‐term postlicensing environmental safety monitoring as a ...
