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      The Effects of Exposure to Flupyradifurone on Survival, Development, and Foraging Activity of Honey Bees ( Apis mellifera L.) under Field Conditions

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          Abstract

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          Honey bees play an invaluable role in ecosystem stability and global food security. Recently, much attention has been directed toward the safety of pesticides to bees. Flupyradifurone (FPF) is a new butenolide insecticide and is considered friendly to honey bee fitness according to risk assessment procedures. Although no significant side-effects on bee colony strength parameters at FPF field-realistic concentration, laboratory experiments have demonstrated that FPF has multiple negative effects on the behavior of individual honey bees. The information suggested that FPF is posing potential risks to honey bees. In this study, we found that the survival rate of bees exposed to FPF was statistically significantly reduced, whereas there were no negative effects on larvae development nor foraging activity. In addition, immune- and detoxification-related genes were upregulated in exposed foragers and newly emerged bees, suggesting that more important synergistic and behavioral effects that can affect colony fitness should be explored in the future.

          Abstract

          Flupyradifurone (FPF) is a novel systemic nAChR agonist that interferes with signal transduction in the central nervous system of sucking pests. Despite claims that FPF is potentially “bee-safe” by risk assessments, laboratory data have suggested that FPF has multiple sub-lethal effects on individual honey bees. Our study aimed to expand the studies to the effects of field-realistic concentration of FPF. We found a statistically significant decrease in the survival rate of honey bees exposed to FPF, whereas there were no significantly negative effects on larvae development durations nor foraging activity. In addition, we found that the exposed foragers showed significantly higher expression of ApidNT, CYP9Q2, CYP9Q3, and AmInR-2 compared to the CK group (control group), but no alteration in the gene expression was observed in larvae. The exposed newly emerged bees showed significantly higher expression of Defensin and ApidNT. These results indicate that the chronic exposure to the field-realistic concentration of FPF has negligible effects, but more important synergistic and behavioral effects that can affect colony fitness should be explored in the future, considering the wide use of FPF on crops pollinated and visited by honey bees.

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          Most cited references50

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          Global pollinator declines: trends, impacts and drivers.

          Pollinators are a key component of global biodiversity, providing vital ecosystem services to crops and wild plants. There is clear evidence of recent declines in both wild and domesticated pollinators, and parallel declines in the plants that rely upon them. Here we describe the nature and extent of reported declines, and review the potential drivers of pollinator loss, including habitat loss and fragmentation, agrochemicals, pathogens, alien species, climate change and the interactions between them. Pollinator declines can result in loss of pollination services which have important negative ecological and economic impacts that could significantly affect the maintenance of wild plant diversity, wider ecosystem stability, crop production, food security and human welfare. Copyright (c) 2010 Elsevier Ltd. All rights reserved.
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            A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee

            The honeybee genome has substantially fewer protein coding genes (≈ 11 000 genes) than Drosophila melanogaster (≈ 13 500) and Anopheles gambiae (≈ 14 000). Some of the most marked differences occur in three superfamilies encoding xenobiotic detoxifying enzymes. Specifically there are only about half as many glutathione-S-transferases (GSTs), cytochrome P450 monooxygenases (P450s) and carboxyl/cholinesterases (CCEs) in the honeybee. This includes 10-fold or greater shortfalls in the numbers of Delta and Epsilon GSTs and CYP4 P450s, members of which clades have been recurrently associated with insecticide resistance in other species. These shortfalls may contribute to the sensitivity of the honeybee to insecticides. On the other hand there are some recent radiations in CYP6, CYP9 and certain CCE clades in A. mellifera that could be associated with the evolution of the hormonal and chemosensory processes underpinning its highly organized eusociality.
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              Threats to an ecosystem service: pressures on pollinators

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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                Insects
                Insects
                insects
                Insects
                MDPI
                2075-4450
                16 April 2021
                April 2021
                : 12
                : 4
                : 357
                Affiliations
                [1 ]Key Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Ministry of Agriculture, Beijing 100093, China; guoyi63671@ 123456163.com (Y.G.); dqyapis@ 123456163.com (Q.-Y.D.); daipingli@ 123456caas.cn (P.-L.D.); wangqiang@ 123456caas.cn (Q.W.); houchunsheng@ 123456caas.cn (C.-S.H.); liuyongjun@ 123456caas.cn (Y.-J.L.); zhangli3393@ 123456126.com (L.Z.)
                [2 ]Bureau of Landscape and Forestry, Miyun District, Beijing 101500, China; luoqihua0825@ 123456163.com
                Author notes
                [* ]Correspondence: wuyanyan@ 123456caas.cn (Y.-Y.W.); gaojing@ 123456caas.cn (J.G.); Tel.: +86-10-6259-1738 (J.G.)
                [†]

                These authors have contributed equally to this study.

                Author information
                https://orcid.org/0000-0002-8297-652X
                https://orcid.org/0000-0003-0146-7668
                Article
                insects-12-00357
                10.3390/insects12040357
                8074100
                33923512
                50ae32a7-89fc-45f2-8cb0-29ee0b9695b2
                © 2021 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( https://creativecommons.org/licenses/by/4.0/).

                History
                : 19 March 2021
                : 13 April 2021
                Categories
                Article

                flupyradifurone,honey bee,pesticide,development,foraging activity

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