A worldwide survey of neonicotinoids in honey

Mitchell, Edward A. D.; Mulhauser, Blaise; Mulot, Matthieu; Mutabazi, Aline; Glauser, Gaëtan; Aebi, Alexandre

doi:10.1126/science.aan3684

Cited by 398 publications

(285 citation statements)

References 79 publications

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“…Chronic pesticide exposure is increasingly likely to occur in the field as water‐soluble systemic pesticides have been found to occur in wild flowers on field margins (Botias et al., ), and in flowers sold in garden centres (Lentola et al., ), while pesticide products are freely available for gardeners to purchase, and bees preferentially feed on sucrose solutions that have been treated with pesticides (Kessler et al., ). Our results draw together a body of evidence that in combination suggests the rising prevalence of pesticides in the environment (Mitchell et al., ) is increasingly likely to influence the cognitive abilities of bees.…”

Section: Discussionmentioning

confidence: 99%

Quantifying the impact of pesticides on learning and memory in bees

Siviter

Koricheva

Brown

et al. 2018

Journal of Applied Ecology

151

127

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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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Section: Discussionmentioning

confidence: 99%

Quantifying the impact of pesticides on learning and memory in bees

Siviter

Koricheva

Brown

et al. 2018

Journal of Applied Ecology

151

127

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“…However, neonicotinoids have been implicated as a threat to eusocial bees (Gill et al, 2012;Goulson, 2013;Lundin, Rundlöf, Smith, Fries, & Bommarco, 2015;Tsvetkov et al, 2017;Whitehorn, O'Connor, Wackers, & Goulson, 2012;Woodcock et al, 2017). Foraging eusocial bees are frequently exposed to neonicotinoids in treated landscapes (Botías, David, Hill, & Goulson, 2017;Botías et al, 2015;David et al, 2016;Mitchell et al, 2017;Rolke, Persigehl, Peters, Sterk, & Blenau, 2016), and controlled exposure experiments have demonstrated impaired homing ability (Fischer et al, 2014) and foraging efficiency of workers, including longer foraging trips and reduced rate of pollen collection (Feltham, Park, & Goulson, 2014;Gill & Raine, 2014;Stanley & Raine, 2016). A possible explanation for these reported impairments is that certain aspects of foraging flight dynamics, such as endurance and speed, are affected by neonicotinoid exposure.…”

Section: Introductionmentioning

confidence: 99%

“…For this study, we exposed individual workers to the neonicotinoid imidacloprid at a concentration of 10 ppb as it is: (a) a widely used insecticide across the globe with a growing market in many regions (Auteri et al, 2017;Casida, 2018;Cressey, 2017;Mitchell et al, 2017;Zhang, 2018); (b) a concentration that can be found inside social bee colonies, on return foraging workers, and in the pollen and nectar of individual flowers (Blacquière, Smagghe, van Gestel, & Mommaerts, 2012;Cresswell, 2011;Dively & Kamel, 2012;Goulson, 2013;Hladik, Vandever, & Smalling, 2016);…”

Section: Introductionmentioning

confidence: 99%

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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“…Thiamethoxam (THI) is a widely prevalent neonicotinoid in nectar, honey, and pollen from both agricultural crops as well as non‐target species at median doses in seed‐treated oilseed rape nectar from 0.65 to 2.4 μg kg –1 , at mean doses in honey from 0.29 to 6.4 μg kg –1 , to as high as 17.2 μg kg –1 , and at mean doses in pollen from 0.15 to 28.9 μg kg –1 . In semi‐field studies, chronic exposure to environmental doses of THI, as well as its metabolite clothianidin (CLO), another neonicotinoid insecticide, have been linked to deleterious, sublethal effects on honey bees, including decreased queen fecundity (at doses of 4 μg kg –1 THI and 1 μg kg –1 CLO) and decreased colony honey production (at doses of 20 μg kg –1 CLO), but field studies often find no effect of environmental THI or CLO exposure on honey bee colonies …”

Section: Introductionmentioning

confidence: 99%

Effects of chronic dietary thiamethoxam and prothioconazole exposure onApis melliferaworker adults and brood

Wood

Mattos

Kozii

et al. 2019

Pest Management Science

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BACKGROUND Chronic exposure of honey bees (Apis mellifera Linnaeus) to the neonicotinoid thiamethoxam and the fungicide prothioconazole is common during foraging in agricultural landscapes. We evaluated the survival and hypopharyngeal gland development of adult worker honey bees, and the survival of the worker brood when chronically exposed to thiamethoxam or thiamethoxam and prothioconazole in combination. RESULTS We found that 30 days of exposure to 40 μg kg–1 of thiamethoxam significantly (P < 0.001) increased the frequency of death in worker adults by four times relative to solvent control. The worker brood required 23 times higher doses of thiamethoxam (1 mg L–1 or 909 μg kg–1) before a significant (P = 0.04), 3.9 times increase in frequency of death was observed relative to solvent control. No additive effects of simultaneous exposure of worker adults or brood to thiamethoxam and prothioconazole were observed. At day 8 and day 12, the hypopharyngeal gland acinar diameter was not significantly different (P > 0.05) between controls and adult workers exposed to thiamethoxam and/or prothioconazole. CONCLUSION These results indicate that chronic exposure to field‐realistic doses of thiamethoxam and/or prothioconazole are unlikely to affect the survival of adult workers and brood. © 2019 Society of Chemical Industry

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A worldwide survey of neonicotinoids in honey

Cited by 398 publications

References 79 publications

Quantifying the impact of pesticides on learning and memory in bees

Quantifying the impact of pesticides on learning and memory in bees

Pesticide exposure affects flight dynamics and reduces flight endurance in bumblebees

Effects of chronic dietary thiamethoxam and prothioconazole exposure onApis melliferaworker adults and brood

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