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      Oral or Topical Exposure to Glyphosate in Herbicide Formulation Impacts the Gut Microbiota and Survival Rates of Honey Bees

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          Abstract

          The honey bee gut microbial community plays a vital role in immune response and defense against opportunistic pathogens. Environmental stressors, such as the herbicide glyphosate, may affect the gut microbiota, with negative consequences for bee health. Glyphosate is usually sprayed in the field mixed with adjuvants, which enhance herbicidal activity. These adjuvants may also enhance undesired effects in nontargeted organisms. This seems to be the case for glyphosate-based herbicide on honey bees. As we show in this study, oral exposure to either pure glyphosate or glyphosate in a commercial herbicide formulation perturbs the gut microbiota of honey bees, and topical exposure to the formulation also has a direct effect on honey bee health, increasing mortality in a dose-dependent way and leaving surviving bees with a perturbed microbiota. Understanding the effects of herbicide formulations on honey bees may help to protect these important agricultural pollinators.

          ABSTRACT

          Honey bees are important agricultural pollinators that rely on a specific gut microbiota for the regulation of their immune system and defense against pathogens. Environmental stressors that affect the bee gut microbial community, such as antibiotics and glyphosate, can indirectly compromise bee health. Most of the experiments demonstrating these effects have been done under laboratory conditions with pure chemicals. Here, we investigated the oral and topical effects of various concentrations of glyphosate in a herbicide formulation on the honey bee gut microbiota and health under laboratory and field conditions. Under all of these conditions, the formulation, dissolved in sucrose syrup or water, affected the abundance of beneficial bacteria in the bee gut in a dose-dependent way. Mark-recapture experiments also demonstrated that bees exposed to the formulation were more likely to disappear from the colony, once reintroduced after exposure. Although no visible effects were observed for hives exposed to the formulation in field experiments, challenge trials with the pathogen Serratia marcescens, performed under laboratory conditions, revealed that bees from hives exposed to the formulation exhibited increased mortality compared with bees from control hives. In the field experiments, glyphosate was detected in honey collected from exposed hives, showing that worker bees transfer xenobiotics to the hive, thereby extending exposure and increasing the chances of exposure to recently emerged bees. These findings show that different routes of exposure to glyphosate-based herbicide can affect honey bees and their gut microbiota.

          IMPORTANCE The honey bee gut microbial community plays a vital role in immune response and defense against opportunistic pathogens. Environmental stressors, such as the herbicide glyphosate, may affect the gut microbiota, with negative consequences for bee health. Glyphosate is usually sprayed in the field mixed with adjuvants, which enhance herbicidal activity. These adjuvants may also enhance undesired effects in nontargeted organisms. This seems to be the case for glyphosate-based herbicide on honey bees. As we show in this study, oral exposure to either pure glyphosate or glyphosate in a commercial herbicide formulation perturbs the gut microbiota of honey bees, and topical exposure to the formulation also has a direct effect on honey bee health, increasing mortality in a dose-dependent way and leaving surviving bees with a perturbed microbiota. Understanding the effects of herbicide formulations on honey bees may help to protect these important agricultural pollinators.

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          Pollen nutritional content and digestibility for animals

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            Environmental and health effects of the herbicide glyphosate

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              Glyphosate perturbs the gut microbiota of honey bees

              Significance Increased mortality of honey bee colonies has been attributed to several factors but is not fully understood. The herbicide glyphosate is expected to be innocuous to animals, including bees, because it targets an enzyme only found in plants and microorganisms. However, bees rely on a specialized gut microbiota that benefits growth and provides defense against pathogens. Most bee gut bacteria contain the enzyme targeted by glyphosate, but vary in whether they possess susceptible versions and, correspondingly, in tolerance to glyphosate. Exposing bees to glyphosate alters the bee gut community and increases susceptibility to infection by opportunistic pathogens. Understanding how glyphosate impacts bee gut symbionts and bee health will help elucidate a possible role of this chemical in colony decline.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                Appl Environ Microbiol
                Appl. Environ. Microbiol
                aem
                aem
                AEM
                Applied and Environmental Microbiology
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                0099-2240
                1098-5336
                10 July 2020
                1 September 2020
                September 2020
                1 September 2020
                : 86
                : 18
                : e01150-20
                Affiliations
                [a ]Department of Integrative Biology, University of Texas at Austin, Austin, Texas, USA
                [b ]Mass Spectrometry Facility, Department of Chemistry, University of Texas at Austin, Austin, Texas, USA
                University of Illinois at Chicago
                Author notes
                Address correspondence to Erick V. S. Motta, erickvsm@ 123456utexas.edu , or Nancy A. Moran, nancy.moran@ 123456austin.utexas.edu .

                Citation Motta EVS, Mak M, De Jong TK, Powell JE, O’Donnell A, Suhr KJ, Riddington IM, Moran NA. 2020. Oral or topical exposure to glyphosate in herbicide formulation impacts the gut microbiota and survival rates of honey bees. Appl Environ Microbiol 86:e01150-20. https://doi.org/10.1128/AEM.01150-20.

                Author information
                https://orcid.org/0000-0001-9360-4353
                https://orcid.org/0000-0003-2983-9769
                Article
                01150-20
                10.1128/AEM.01150-20
                7480383
                32651208
                c183ba97-d031-4d03-8ffc-bfcb0e3f9e2f
                Copyright © 2020 Motta et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 14 May 2020
                : 6 July 2020
                Page count
                supplementary-material: 1, Figures: 7, Tables: 0, Equations: 0, References: 88, Pages: 21, Words: 14806
                Funding
                Funded by: USDA | National Institute of Food and Agriculture (NIFA), https://doi.org/10.13039/100005825;
                Award ID: 2018-67013-27540
                Award Recipient :
                Funded by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), https://doi.org/10.13039/501100002322;
                Award ID: 13578-13-8
                Award Recipient : Erick V. S. Motta
                Categories
                Microbial Ecology
                Spotlight
                Custom metadata
                September 2020

                Microbiology & Virology
                apis mellifera,gut microbiome,herbicide,glyphosate
                Microbiology & Virology
                apis mellifera, gut microbiome, herbicide, glyphosate

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