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      An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: impacts on organisms and ecosystems

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          Abstract

          New information on the lethal and sublethal effects of neonicotinoids and fipronil on organisms is presented in this review, complementing the previous Worldwide Integrated Assessment (WIA) in 2015. The high toxicity of these systemic insecticides to invertebrates has been confirmed and expanded to include more species and compounds. Most of the recent research has focused on bees and the sublethal and ecological impacts these insecticides have on pollinators. Toxic effects on other invertebrate taxa also covered predatory and parasitoid natural enemies and aquatic arthropods. Little new information has been gathered on soil organisms. The impact on marine and coastal ecosystems is still largely uncharted. The chronic lethality of neonicotinoids to insects and crustaceans, and the strengthened evidence that these chemicals also impair the immune system and reproduction, highlights the dangers of this particular insecticidal class (neonicotinoids and fipronil), with the potential to greatly decrease populations of arthropods in both terrestrial and aquatic environments. Sublethal effects on fish, reptiles, frogs, birds, and mammals are also reported, showing a better understanding of the mechanisms of toxicity of these insecticides in vertebrates and their deleterious impacts on growth, reproduction, and neurobehaviour of most of the species tested. This review concludes with a summary of impacts on the ecosystem services and functioning, particularly on pollination, soil biota, and aquatic invertebrate communities, thus reinforcing the previous WIA conclusions (van der Sluijs et al. 2015).

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          High Levels of Miticides and Agrochemicals in North American Apiaries: Implications for Honey Bee Health

          Background Recent declines in honey bees for crop pollination threaten fruit, nut, vegetable and seed production in the United States. A broad survey of pesticide residues was conducted on samples from migratory and other beekeepers across 23 states, one Canadian province and several agricultural cropping systems during the 2007–08 growing seasons. Methodology/Principal Findings We have used LC/MS-MS and GC/MS to analyze bees and hive matrices for pesticide residues utilizing a modified QuEChERS method. We have found 121 different pesticides and metabolites within 887 wax, pollen, bee and associated hive samples. Almost 60% of the 259 wax and 350 pollen samples contained at least one systemic pesticide, and over 47% had both in-hive acaricides fluvalinate and coumaphos, and chlorothalonil, a widely-used fungicide. In bee pollen were found chlorothalonil at levels up to 99 ppm and the insecticides aldicarb, carbaryl, chlorpyrifos and imidacloprid, fungicides boscalid, captan and myclobutanil, and herbicide pendimethalin at 1 ppm levels. Almost all comb and foundation wax samples (98%) were contaminated with up to 204 and 94 ppm, respectively, of fluvalinate and coumaphos, and lower amounts of amitraz degradates and chlorothalonil, with an average of 6 pesticide detections per sample and a high of 39. There were fewer pesticides found in adults and brood except for those linked with bee kills by permethrin (20 ppm) and fipronil (3.1 ppm). Conclusions/Significance The 98 pesticides and metabolites detected in mixtures up to 214 ppm in bee pollen alone represents a remarkably high level for toxicants in the brood and adult food of this primary pollinator. This represents over half of the maximum individual pesticide incidences ever reported for apiaries. While exposure to many of these neurotoxicants elicits acute and sublethal reductions in honey bee fitness, the effects of these materials in combinations and their direct association with CCD or declining bee health remains to be determined.
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            Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites

            Since their discovery in the late 1980s, neonicotinoid pesticides have become the most widely used class of insecticides worldwide, with large-scale applications ranging from plant protection (crops, vegetables, fruits), veterinary products, and biocides to invertebrate pest control in fish farming. In this review, we address the phenyl-pyrazole fipronil together with neonicotinoids because of similarities in their toxicity, physicochemical profiles, and presence in the environment. Neonicotinoids and fipronil currently account for approximately one third of the world insecticide market; the annual world production of the archetype neonicotinoid, imidacloprid, was estimated to be ca. 20,000 tonnes active substance in 2010. There were several reasons for the initial success of neonicotinoids and fipronil: (1) there was no known pesticide resistance in target pests, mainly because of their recent development, (2) their physicochemical properties included many advantages over previous generations of insecticides (i.e., organophosphates, carbamates, pyrethroids, etc.), and (3) they shared an assumed reduced operator and consumer risk. Due to their systemic nature, they are taken up by the roots or leaves and translocated to all parts of the plant, which, in turn, makes them effectively toxic to herbivorous insects. The toxicity persists for a variable period of time—depending on the plant, its growth stage, and the amount of pesticide applied. A wide variety of applications are available, including the most common prophylactic non-Good Agricultural Practices (GAP) application by seed coating. As a result of their extensive use and physicochemical properties, these substances can be found in all environmental compartments including soil, water, and air. Neonicotinoids and fipronil operate by disrupting neural transmission in the central nervous system of invertebrates. Neonicotinoids mimic the action of neurotransmitters, while fipronil inhibits neuronal receptors. In doing so, they continuously stimulate neurons leading ultimately to death of target invertebrates. Like virtually all insecticides, they can also have lethal and sublethal impacts on non-target organisms, including insect predators and vertebrates. Furthermore, a range of synergistic effects with other stressors have been documented. Here, we review extensively their metabolic pathways, showing how they form both compound-specific and common metabolites which can themselves be toxic. These may result in prolonged toxicity. Considering their wide commercial expansion, mode of action, the systemic properties in plants, persistence and environmental fate, coupled with limited information about the toxicity profiles of these compounds and their metabolites, neonicotinoids and fipronil may entail significant risks to the environment. A global evaluation of the potential collateral effects of their use is therefore timely. The present paper and subsequent chapters in this review of the global literature explore these risks and show a growing body of evidence that persistent, low concentrations of these insecticides pose serious risks of undesirable environmental impacts.
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              Non-bee insects are important contributors to global crop pollination

              Wild and managed bees are well documented as effective pollinators of global crops of economic importance. However, the contributions by pollinators other than bees have been little explored despite their potential to contribute to crop production and stability in the face of environmental change. Non-bee pollinators include flies, beetles, moths, butterflies, wasps, ants, birds, and bats, among others. Here we focus on non-bee insects and synthesize 39 field studies from five continents that directly measured the crop pollination services provided by non-bees, honey bees, and other bees to compare the relative contributions of these taxa. Non-bees performed 25-50% of the total number of flower visits. Although non-bees were less effective pollinators than bees per flower visit, they made more visits; thus these two factors compensated for each other, resulting in pollination services rendered by non-bees that were similar to those provided by bees. In the subset of studies that measured fruit set, fruit set increased with non-bee insect visits independently of bee visitation rates, indicating that non-bee insects provide a unique benefit that is not provided by bees. We also show that non-bee insects are not as reliant as bees on the presence of remnant natural or seminatural habitat in the surrounding landscape. These results strongly suggest that non-bee insect pollinators play a significant role in global crop production and respond differently than bees to landscape structure, probably making their crop pollination services more robust to changes in land use. Non-bee insects provide a valuable service and provide potential insurance against bee population declines.
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                Author and article information

                Contributors
                bonmatin@cnrs-orleans.fr
                Journal
                Environ Sci Pollut Res Int
                Environ Sci Pollut Res Int
                Environmental Science and Pollution Research International
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                0944-1344
                1614-7499
                9 November 2017
                9 November 2017
                2021
                : 28
                : 10
                : 11749-11797
                Affiliations
                [1 ]GRID grid.5477.1, ISNI 0000000120346234, Utrecht University, ; Utrecht, The Netherlands
                [2 ]GRID grid.12082.39, ISNI 0000 0004 1936 7590, School of Life Sciences, , University of Sussex, ; Brighton, BN1 9QG UK
                [3 ]GRID grid.19188.39, ISNI 0000 0004 0546 0241, Department of Entomology, , National Taiwan University, ; Taipei, Taiwan
                [4 ]GRID grid.421630.2, ISNI 0000 0001 2110 3189, RSPB Centre for Conservation of Science, The Lodge, ; Sandy, Bedfordshire SG19 2DL UK
                [5 ]GRID grid.1013.3, ISNI 0000 0004 1936 834X, School of Life and Environmental Sciences, , The University of Sydney, ; 1 Central Avenue, Eveleigh, NSW 2015 Australia
                [6 ]GRID grid.10711.36, ISNI 0000 0001 2297 7718, Laboratory of Soil Biodiversity, , University of Neuchâtel, ; Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland
                [7 ]GRID grid.10711.36, ISNI 0000 0001 2297 7718, Anthropology Institute, , University of Neuchâtel, ; Rue Saint-Nicolas 4, 2000 Neuchâtel, Switzerland
                [8 ]GRID grid.7914.b, ISNI 0000 0004 1936 7443, Centre for the Study of the Sciences and the Humanities, , University of Bergen, ; Postboks 7805, 5020 Bergen, Norway
                [9 ]GRID grid.7914.b, ISNI 0000 0004 1936 7443, Department of Chemistry, , University of Bergen, ; Postboks 7805, 5020 Bergen, Norway
                [10 ]GRID grid.5477.1, ISNI 0000000120346234, Copernicus Institute of Sustainable Development, Environmental Sciences, , Utrecht University, ; Heidelberglaan 2, 3584 CS Utrecht, The Netherlands
                [11 ]GRID grid.146611.5, ISNI 0000 0001 0775 5922, Natural Resources Canada, , Canadian Forest Service, ; 1219 Queen St. East, Sault Ste. Marie, ON P6A 2E5 Canada
                [12 ]GRID grid.463881.0, ISNI 0000 0004 0385 962X, Aix Marseille Univ, CNRS, LCE, ; Marseille, France
                [13 ]GRID grid.261331.4, ISNI 0000 0001 2285 7943, Department of Entomology, , The Ohio State University, ; 1680 Madison Ave, Wooster, OH 44691 USA
                [14 ]GRID grid.1214.6, ISNI 0000 0000 8716 3312, Smithsonian Institution, ; 701 Seaway Drive Fort Pierce, Florida, 34949 USA
                [15 ]Task Force on Systemic Pesticides, Pertuis-du-Sault, 2000 Neuchâtel, Switzerland
                [16 ]GRID grid.417870.d, ISNI 0000 0004 0614 8532, Centre National de la Recherche Scientifique (CNRS), , Centre de Biophysique Moléculaire, ; Rue Charles Sadron, 45071 Orléans, France
                Author notes

                Responsible editor: Philippe Garrigues

                Author information
                http://orcid.org/0000-0003-1770-0460
                Article
                341
                10.1007/s11356-017-0341-3
                7921077
                29124633
                70a92219-c963-48bd-9b8c-da0aefd70691
                © The Author(s) 2017

                Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 25 July 2017
                : 25 September 2017
                Funding
                Funded by: Triodos Foundation (The Netherlands)
                Funded by: Act Beyond Trust (Japan)
                Funded by: Stichting Triodos Foundation (The Netherlands)
                Funded by: M.A.O.C. Gravin van Bylandt Stichting (The Netherlands)
                Funded by: Zukunft Stiftung Landwirtschaft (Germany)
                Funded by: Hartmut Spaeter Umweltstiftung (Germany)
                Funded by: Lune de Miel Foundation (France)
                Categories
                Worldwide Integrated Assessment of the Impact of Systemic Pesticides on Biodiversity and Ecosystems
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2021

                General environmental science
                systemic insecticides,neonicotinoids,fipronil,insects,pollinators,soil biota,aquatic organisms,vertebrates,ecosystem services,review

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