Abstract
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 requirement within licensing policy for plant protection products.
Highlights
A wealth of empirical evidence for global pollinator decline has driven unprecedented interest in the mechanisms by which anthropogenic changes influence both domestic honeybees (Apis spp.) and native wild bees (e.g., Bombus spp.; Aizen & Harder, 2009; Goulson, Nicholls, Botias, & Rotheray, 2015; Potts et al, 2010)
Chronic pesticide exposure had a stronger effect on bee memory than acute exposure, the same effect was not found in relation to learning score
Current interest in the effects of pesticides on pollinators is based upon the need to understand the nature of negative effects in order that they can be reduced via policy change
Summary
A wealth of empirical evidence for global pollinator decline has driven unprecedented interest in the mechanisms by which anthropogenic changes influence both domestic honeybees (Apis spp.) and native wild bees (e.g., Bombus spp.; Aizen & Harder, 2009; Goulson, Nicholls, Botias, & Rotheray, 2015; Potts et al, 2010). The mushroom bodies are a neural region associated with olfactory learning and memory in bees (Devaud et al, 2015; Hourcade, Muenz, Sandoz, Rossler, & Devaud, 2010), and there is strong evidence that mushroom body development and function can be directly impaired through chronic or acute exposure to NAChR agonists respectively (Palmer et al, 2013; Peng & Yang, 2016). Effects of pesticides on bee cognition may vary across classes of pesticides, reflecting different modes of action (Klein et al, 2017) Such variation is important as certain neonicotinoids (imidacloprid, clothianidin, and thiamethoxam) are under a total ban in the EU with respect to agricultural use outside of permanent greenhouse structures (to be implemented by December 2018) (European Commission 2018), which is likely to create market demand for other pesticides as replacements (Brown et al, 2016; Campbell, 2013).
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