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      Supplemental forage ameliorates the negative impact of insecticides on bumblebees in a pollinator-dependent crop

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          Abstract

          Insecticide use and insufficient forage are two of the leading stressors to pollinators in agroecosystems. While these factors have been well studied individually, the experimental designs do not reflect real-world conditions where insecticide exposure and lack of forage occur simultaneously and could interactively suppress pollinator health. Using outdoor enclosures, we tested the effects of insecticides (imidacloprid + lambda-cyhalothrin) and non-crop forage (clover) in a factorial design, measuring the survival, behaviour and performance of bumblebees ( Bombus impatiens), as well as pollination of the focal crop, watermelon. Colony survival was synergistically reduced to 17% in watermelon alone + insecticides (survival was 100% in all other treatments). However, behavioural shifts in foraging were mainly owing to insecticides (e.g. 95% reduced visitation rate to watermelon flowers), while impacts on hive performance were primarily driven by clover presence (e.g. 374% increase in the number of live eggs). Insecticide-mediated reductions in foraging decreased crop pollination (fruit set) by 32%. Altogether, these data indicate that both insecticides and non-crop forage play integral roles in shaping pollinator health in agricultural landscapes, but the relative importance and interaction of these two factors depend on which aspect of ‘health’ is being considered.

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          Most cited references55

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          Bee declines driven by combined stress from parasites, pesticides, and lack of flowers.

          Bees are subject to numerous pressures in the modern world. The abundance and diversity of flowers has declined; bees are chronically exposed to cocktails of agrochemicals, and they are simultaneously exposed to novel parasites accidentally spread by humans. Climate change is likely to exacerbate these problems in the future. Stressors do not act in isolation; for example, pesticide exposure can impair both detoxification mechanisms and immune responses, rendering bees more susceptible to parasites. It seems certain that chronic exposure to multiple interacting stressors is driving honey bee colony losses and declines of wild pollinators, but such interactions are not addressed by current regulatory procedures, and studying these interactions experimentally poses a major challenge. In the meantime, taking steps to reduce stress on bees would seem prudent; incorporating flower-rich habitat into farmland, reducing pesticide use through adopting more sustainable farming methods, and enforcing effective quarantine measures on bee movements are all practical measures that should be adopted. Effective monitoring of wild pollinator populations is urgently needed to inform management strategies into the future.
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            Crop pollination from native bees at risk from agricultural intensification.

            Ecosystem services are critical to human survival; in selected cases, maintaining these services provides a powerful argument for conserving biodiversity. Yet, the ecological and economic underpinnings of most services are poorly understood, impeding their conservation and management. For centuries, farmers have imported colonies of European honey bees (Apis mellifera) to fields and orchards for pollination services. These colonies are becoming increasingly scarce, however, because of diseases, pesticides, and other impacts. Native bee communities also provide pollination services, but the amount they provide and how this varies with land management practices are unknown. Here, we document the individual species and aggregate community contributions of native bees to crop pollination, on farms that varied both in their proximity to natural habitat and management type (organic versus conventional). On organic farms near natural habitat, we found that native bee communities could provide full pollination services even for a crop with heavy pollination requirements (e.g., watermelon, Citrullus lanatus), without the intervention of managed honey bees. All other farms, however, experienced greatly reduced diversity and abundance of native bees, resulting in insufficient pollination services from native bees alone. We found that diversity was essential for sustaining the service, because of year-to-year variation in community composition. Continued degradation of the agro-natural landscape will destroy this "free" service, but conservation and restoration of bee habitat are potentially viable economic alternatives for reducing dependence on managed honey bees.
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              REVIEW: An overview of the environmental risks posed by neonicotinoid insecticides

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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: Project administrationRole: Writing-original draftRole: Writing-review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: VisualizationRole: Writing-original draftRole: Writing-review & editing
                Role: InvestigationRole: Methodology
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: SupervisionRole: VisualizationRole: Writing-original draftRole: Writing-review & editing
                Journal
                Proc Biol Sci
                Proc Biol Sci
                RSPB
                royprsb
                Proceedings of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8452
                1471-2954
                June 30, 2021
                June 30, 2021
                June 30, 2021
                : 288
                : 1953
                : 20210785
                Affiliations
                [ 1 ]Department of Entomology, Purdue University, , 901 West State Street, West Lafayette, IN, USA
                [ 2 ]Department of Entomology and Nematology, University of Florida, , 1881 Natural Area Drive, Gainesville, FL, USA
                Author notes
                [†]

                These authors contributed equally to this study.

                Electronic supplementary material is available online https://doi.org/10.6084/m9.figshare.c.5469506.

                Author information
                http://orcid.org/0000-0003-4469-2750
                Article
                rspb20210785
                10.1098/rspb.2021.0785
                8242826
                34187195
                649a7b3f-46af-497d-b6f9-40b4b17ba9dc
                © 2021 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : April 25, 2021
                : June 4, 2021
                Funding
                Funded by: National Institute of Food and Agriculture, http://dx.doi.org/10.13039/100005825;
                Award ID: 2016-51181-25410
                Categories
                1001
                69
                60
                Ecology
                Research Articles
                Custom metadata
                June 30, 2021

                Life sciences
                agroecosystem,bombus impatiens,crop pollination,herbicide,insecticide,pollinator health
                Life sciences
                agroecosystem, bombus impatiens, crop pollination, herbicide, insecticide, pollinator health

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