Effect of acute pesticide exposure on bee spatial working memory using an analogue of the radial-arm maze

Samuelson, Ash E.; Chen-Wishart, Z.; Gill, Richard J.; Leadbeater, Ellouise

doi:10.1038/srep38957

Cited by 97 publications

(94 citation statements)

References 60 publications

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“…Intriguingly, a previous study showed that neonicotinoid-induced impairment to spatial learning behavior in bumblebees appeared to be exhibited more highly in the largest colony workers (Samuelson, Chen-Wishart, Gill, & Leadbeater, 2016). Intriguingly, a previous study showed that neonicotinoid-induced impairment to spatial learning behavior in bumblebees appeared to be exhibited more highly in the largest colony workers (Samuelson, Chen-Wishart, Gill, & Leadbeater, 2016).…”

Section: Discussionmentioning

confidence: 96%

Pesticide exposure affects flight dynamics and reduces flight endurance in bumblebees

Kenna

Cooley

Pretelli

et al. 2019

Ecology and Evolution

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The emergence of agricultural land use change creates a number of challenges that insect pollinators, such as eusocial bees, must overcome. Resultant fragmentation and loss of suitable foraging habitats, combined with pesticide exposure, may increase demands on foraging, specifically the ability to collect or reach sufficient resources under such stress. Understanding effects that pesticides have on flight performance is therefore vital if we are to assess colony success in these changing landscapes. Neonicotinoids are one of the most widely used classes of pesticide across the globe, and exposure to bees has been associated with reduced foraging efficiency and homing ability. One explanation for these effects could be that elements of flight are being affected, but apart from a couple of studies on the honeybee (Apis mellifera), this has scarcely been tested. Here, we used flight mills to investigate how exposure to a field realistic (10 ppb) acute dose of imidacloprid affected flight performance of a wild insect pollinator—the bumblebee, Bombus terrestris audax. Intriguingly, observations showed exposed workers flew at a significantly higher velocity over the first ¾ km of flight. This apparent hyperactivity, however, may have a cost because exposed workers showed reduced flight distance and duration to around a third of what control workers were capable of achieving. Given that bumblebees are central place foragers, impairment to flight endurance could translate to a decline in potential forage area, decreasing the abundance, diversity, and nutritional quality of available food, while potentially diminishing pollination service capabilities.

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Section: Discussionmentioning

confidence: 96%

Pesticide exposure affects flight dynamics and reduces flight endurance in bumblebees

Kenna

Cooley

Pretelli

et al. 2019

Ecology and Evolution

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“…It is too early to draw conclusions about species differences in the impact of pesticides on bee cognitive abilities, and this knowledge gap is important given that wild bee flower visits can enhance the fruit set of crops regardless of the presence of honeybees (Garibaldi et al., ), and are thought to offer an important buffer in the case of a domesticated honeybee collapse (Greenleaf & Kremen, ). Research on non‐ Apis species, such as bumblebees (including species other than Bombus terrestris ) and solitary bees, is sorely needed, and the development of non PER‐based paradigms for testing the effects of pesticides on cognition is welcome in this respect (Samuelson et al., ; Tan et al., ).…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, pesticide exposure has been shown to influence olfactory processing (Andrione, Vallortigara, Antolini, & Haase, ) suggesting that exploration of alternative visual and/or spatial modalities will be critical if researchers are specifically interested in how pesticides influence bee learning and memory at the level of neural processing, rather than stimulus perception. Initial exploration of these methodologies has provided evidence for cognitive effects of pesticides outside of olfactory paradigms, and should be further explored (Samuelson et al., ).…”

Section: Discussionmentioning

confidence: 99%

“…Typically, PER‐based experiments that relate to pesticides use an absolute conditioning paradigm (where bees learn to associate only one scent with sucrose) rather than differential conditioning (where one scent is rewarded and an alternative is not; Stanley, Smith, & Raine, ). Although other paradigms to test learning and memory (e.g., free‐flying association, spatial learning, aversive learning, or tactile learning [Bernadou, Démares, Couret‐Fauvel, Sandoz, & Gauthier, ; Tan et al., ; Samuelson, Chen‐Wishart, Gill, & Leadbeater, ; Zhang & Nieh, ]) are available and widely used in the cognitive literature, only a very small number of studies have used such methods to assay how pesticides influence performance (see Section ; Bernadou et al., ; Samuelson et al., ; Zhang & Nieh, ). In contrast, the PER paradigm is the most commonly used methodology to assess bee learning and memory and thus provides an obvious target for our study.…”

Section: Methodsmentioning

confidence: 99%

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Quantifying the impact of pesticides on learning and memory in bees

Siviter

Koricheva

Brown

et al. 2018

Journal of Applied Ecology

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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.

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“…Neonicotinoids target nicotinic acetylcholine receptors (nAChRs) which they bind to and thus excite; this can result in paralysis, convulsions and death (Matsuda et al, 2001). Controlled exposure experiments using honeybees and bumblebees have shown that exposure at comparable concentrations to those found in nectar and pollen can have sublethal effects on learning and memory (Siviter, Koricheva, Brown, & Leadbeater, 2018;Stanley, Smith, & Raine, 2015), cognition and problem solving (Baracchi, Marples, Jenkins, Leitch, & Chittka, 2017;Samuelson, Chen-Wishart, Gill, & Leadbeater, 2016;Williamson & Wright, 2013), motor function (Drummond, Williamson, Fitchett, Wright, & Judge, 2016;Williamson, Willis, & Wright, 2014), foraging performance (Gill & Raine, 2014;Henry et al, 2012;Stanley, Russell, Morrison, Rogers, & Raine, 2016), navigation abilities (Fischer et al, 2014) and the immune system (Brandt, Gorenflo, Siede, Meixner, & Büchler, 2016;Brandt et al, 2017;Di Prisco et al, 2013). Despite the growing interest in the link between neonicotinoid exposure and toxicity to bees, we know little about the molecules and genes through which neonicotinoid action is mediated, or whether neonicotinoids may also affect "off-target" processes that are not mediated by nAChRs.…”

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confidence: 99%

Caste‐ and pesticide‐specific effects of neonicotinoid pesticide exposure on gene expression in bumblebees

et al. 2019

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Social bees are important insect pollinators of wildflowers and agricultural crops, making their reported declines a global concern. A major factor implicated in these declines is the widespread use of neonicotinoid pesticides. Indeed, recent research has demonstrated that exposure to low doses of these neurotoxic pesticides impairs bee behaviours important for colony function and survival. However, our understanding of the molecular‐genetic pathways that lead to such effects is limited, as is our knowledge of how effects may differ between colony members. To understand what genes and pathways are affected by exposure of bumblebee workers and queens to neonicotinoid pesticides, we implemented a transcriptome‐wide gene expression study. We chronically exposed Bombus terrestris colonies to either clothianidin or imidacloprid at field‐realistic concentrations while controlling for factors including colony social environment and worker age. We reveal that genes involved in important biological processes including mitochondrial function are differentially expressed in response to neonicotinoid exposure. Additionally, clothianidin exposure had stronger effects on gene expression amplitude and alternative splicing than imidacloprid. Finally, exposure affected workers more strongly than queens. Our work demonstrates how RNA‐Seq transcriptome profiling can provide detailed novel insight on the mechanisms mediating pesticide toxicity to a key insect pollinator.

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Effect of acute pesticide exposure on bee spatial working memory using an analogue of the radial-arm maze

Cited by 97 publications

References 60 publications

Pesticide exposure affects flight dynamics and reduces flight endurance in bumblebees

Pesticide exposure affects flight dynamics and reduces flight endurance in bumblebees

Quantifying the impact of pesticides on learning and memory in bees

Caste‐ and pesticide‐specific effects of neonicotinoid pesticide exposure on gene expression in bumblebees

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