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Does exposing bees to glyphosate alter the bee gut microbiota and increase susceptibility to infection by opportunistic pathogens? A study by Erick V. S. Motta, Kasie Raymann, and Nancy A. Moran demonstrated that the relative and absolute abundances of dominant gut microbiota species are decreased in bees exposed to glyphosate at concentrations documented in the environment. Glyphosate exposure of young workers increased mortality of bees subsequently exposed to the opportunistic pathogen Serratia marcescens. Members of the bee gut microbiota varied in susceptibility to glyphosate, largely corresponding to whether they possessed an EPSPS of class I (sensitive to glyphosate) or class II (insensitive to glyphosate). This basis for differences in sensitivity was confirmed using in vitro experiments in which the EPSPS gene from bee gut bacteria was cloned into Escherichia coli. All strains of the core bee gut species, Snodgrassella alvi, encode a sensitive class I EPSPS, and reduction in S. alvi levels was a consistent experimental result.

Submitted by: Sasha


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Expert response from Steven L. Levine, Ph.D.

Global Lead- Ecotoxicology and Environmental Risk Assessment, Monsanto Company

Tuesday, 10/30/2018 12:21

Motta et al. (2018) is a complicated study, that tests a hypothesis that inhibition of EPSPS in the gut microbiome can result in increased susceptibility to opportunistic pathogens, but some of the experimental conditions make interpretation equivocal. Results from laboratory studies that assess toxicity to individual honey bees are not automatically indicative of effects to honey bee colonies. The reason for this is that honeybees often respond differently when they are exposed as part of a colony. To address this difference, EPA’s scheme for testing effects to honey bee’s progresses from highly conservative studies, where individual bees are tested in highly artificial metal or plastic containers in the laboratory, to more realistic whole-hive studies (EPA, 2015).

The principal laboratory experiment performed by Motta et al., examined the effects of five days of glyphosate pre-exposure to adult honey bees that were challenged with a high level of bacterial infection. The conclusions from the experiment were that pre-exposing honey bees to glyphosate altered the composition of gut microbiota and increased susceptibility to infection by pathogens. First, it is important to point out that the duration and magnitude of glyphosate exposure in this experiment was unrealistically high and does not replicate exposures of bees in agricultural settings where honey bees consume a diet containing nectar and pollen, which contains proteins and aromatic amino acids (Taha et al. 2017). Second, microbiomes are complex and variable and the composition of the honey bee gut microbiome differs with age and task in the colony (ARS, 2018). Based on these results, it becomes important to examine potential effects of glyphosate in a colony feeding study.                                                      

Glyphosate and Roundup agricultural herbicides have been extensively tested in colony level feeding studies (Ferguson, 1987; Burgett and Fisher, 1990; Thompson et al, 2014). The first colony feeding was performed in Australia and found no significant effects to larval and adult honey bees after six consecutive days of whole-hive exposure to 5 mg glyphosate/kg sucrose solution (Ferguson, 1987; Ferguson, 1988). Motta et al. also tested glyphosate at 5 mg/L in a feeding study and reported a change in composition but not abundance of bacteria in the gut microbiome. Interestingly, this change in composition was not observed at 10 mg/L by Motta et al., and this inconsistency questions the biological relevance of the change in composition reported at 5 mg/L. Ferguson concluded from her study that glyphosate could be safely used around honey bee hives. Further, Ferguson reported that levels for a range of pesticides rapidly decline in nectar and pollen, with >90 percent dissipation in three to four days after spraying. Similar results, showing a rapid decline of glyphosate residues in nectar and pollen, were also reported by Thompson et al. (2014). This rapid decline of glyphosate residues in nectar and pollen greatly limits exposure of honey bee colonies to glyphosate.

These original findings by Ferguson were supported by colony feeding trials conducted by two well-established apicultural experts, Burgett and Fisher, from Oregon State University (Burgett and Fisher, 1990). In their first honey bee colony feeding study, colonies were fed Roundup in sucrose solution at a concentration that was 100 to 1000 times above worst-case glyphosate exposure levels reported by Thompson et al. (2014). No significant effects were observed to honey bee adults or brood production after 42 days of observation, which is an indicator of no effects to egg production, egg laying and brood maintenance. In their second whole-hive study, blooming bee-attractive vegetation adjacent to the hives were treated at 6.8 kg a.s./ha (6.1 lb/A). This is a high application rate for Roundup and is six times a typical glyphosate application rate for agricultural uses. As with the colony feeding study, there were no effects to adult honey bee or brood production over the 42-day post-application period.

These initial findings are supported by a more recently published colony feeding study (Thompson et al, 2014). The glyphosate studies performed by Thompson et al., followed international guidance for honey bee testing (OECD guidance document 75). Thompson et al. demonstrated no effect to larval development, growth and survival and adult survival at glyphosate concentrations of 75, 150 and 300 mg/L. These glyphosate concentrations exceed worst-case field exposure the and greatly exceed the levels tested by Motta et al. In addition to these colony level feeding studies, lifecycle studies with beneficial invertebrates have shown no significant effects to growth, survival and reproduction at levels that greatly exceed environmentally realistic glyphosate concentrations (von Mérey et al, 2016).

Currently, there are no reported glyphosate concentrations for beehives, however, measured levels of glyphosate in honey (an important hive product) have been shown to be exceedingly low. A recent FDA residue study demonstrated that in 19 commercial honey samples, over half of the samples were below the analytical limit of detection of 16 ng/g or 0.016 ppm. The glyphosate levels in the samples with detections only ranged from 0.017 to 0.121 ppm, with an average of 0.039 ppm (Chamkasem, 2016).

As you noticed, the study by Motta et al. is complex and thought provoking, but it does not model real world feeding ecology or exposures and controlled hive studies more closely replicate the conditions in the field.  Furthermore, the weight of evidence from colony-level feeding studies demonstrates that honey bees will not be adversely affected by glyphosate at environmentally realistic exposure levels. 

References:

ARS, 2018: Species shifts in the honey bee microbiome differ with age and hive role (2018, July 3) retrieved 26 September 2018 from https://phys.org/news/2018-07-species-shifts-honey-bee-microbiome.html.

Burgett, M. and Fisher, G. 1990. A review of the Belizean honey bee industry: Final report prepared at the request of The Belize Honey Producers Federation. Department of Entomology, Oregon State University, Corvallis, Oregon.

Chamkasem, N. 2016. Method development/validation of the direct determination of glyphosate, glufosinate, and AMPA in Food by LC/MS. Southeast Regional Laboratory, U.S. Food and Drug Administration, Atlanta, GA. https://www.nacrw.org/2016/presentations/O-27.pdf.

EPA, 2015. Guidance for Assessing Pesticide Risks to Bees. Office of Pesticide Programs

United States Environmental Protection Agency Washington, D.C. 20460; Health Canada Pest Management Regulatory Agency; Ottawa, ON, Canada; California Department of Pesticide Regulation, Sacramento, CA. https://www.epa.gov/sites/...06/.../pollinator_risk_assessment_guidance_06_19_14.pdf

Ferguson, F. 1987. Interim report. Long term effects of systemic pesticides on honey bees. The Australian Beekeeper. Pages: 49-53 (September issue).

Ferguson, F. 1988. Long term effects of systemic pesticides on honey bees. Bee keeping in the year 2000: Second Australian and International Beekeeping Congress, Surfers Paradise, Gold Coast, Queensland, Australia, July 21-26, 1988. Editor: John W. Rhodes. Pages: 137-141.

Taka EKA, Kahtani SA, R Taha. 2017. Protein content and amino acids composition of bee-pollens from major floral sources in Al-Ahsa, eastern Saudi Arabia. Saudi Journal of Biological Sciences. In press. https://www.sciencedirect.com/science/article/pii/S1319562X17301523

Thompson HM, Levine SL, Doering J, Norman S, Manson P, Sutton P, von Mérey G. 2014. Evaluating exposure and potential effects on honeybee brood (Apis mellifera) development using glyphosate as an example. Integr Environ Assess Manag. 10(3):463-70. doi: 10.1002/ieam.1529.

von Mérey G, Mehrsheikh A, Manson P, Sutton P, Levine SL. 2016. Glyphosate and AMPA chronic risk assessment for soil biota. Environ Toxicol Chem. 35:2742-2752. doi: 10.1002/etc.3438

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