Abstract
Agricultural and apicultural practices expose honeybees to a range of pesticides that have the potential to negatively affect their physiology, neurobiology, and behavior. Accumulating evidence suggests that these effects extend to the honeybee gut microbiome, which serves important functions for honeybee health. Here we test the potential effects of the pesticides thiacloprid, acetamiprid, and oxalic acid on the gut microbiota of honeybees, first in direct in vitro inhibition assays and secondly in an in vivo caged bee experiment to test if exposure leads to gut microbiota community changes. We found that thiacloprid did not inhibit the honeybee core gut bacteria in vitro, nor did it affect overall community composition or richness in vivo. Acetamiprid did also not inhibit bacterial growth in vitro, but it did affect community structure within bees. The eight bacterial genera tested showed variable levels of susceptibility to oxalic acid in vitro. In vivo, treatment with this pesticide reduced amplicon sequence variant (ASV) richness and affected gut microbiome composition, with most marked impact on the common crop bacteria Lactobacillus kunkeei and the genus Bombella. We conducted network analyses which captured known associations between bacterial members and illustrated the sensitivity of the microbiome to environmental stressors. Our findings point to risks of honeybee exposure to oxalic acid, which has been deemed safe for use in treatment against Varroa mites in honeybee colonies, and we advocate for more extensive assessment of the long-term effects that it may have on honeybee health.
Highlights
The deleterious effects of pesticides on non-target organisms have been a critical area of study in the last decades (Mancini et al, 2019)
We address the potential effects of the pesticides acetamiprid, thiacloprid, and oxalic acid on the gut microbiota associated with honeybees
We evaluated the proportion of plates with honeybee gut bacteria that were inhibited across the specified concentrations of three pesticides and found that all strains were resistant to acetamiprid and thiacloprid, but sensitive to oxalic acid (Figure 2)
Summary
The deleterious effects of pesticides on non-target organisms have been a critical area of study in the last decades (Mancini et al, 2019). The vital ecosystem services pollinators provide prioritize assessment of pesticide toxicity in this group, and evidence of pesticide harm to honeybees continues to accumulate (Decourtye et al, 2004a; Gill et al, 2012; Goulson et al, 2015). Pesticide Effects on Honeybee Microbiome (Hung et al, 2018). Honeybees play a keystone role in pollination of natural ecosystems and agricultural crops (Goulson et al, 2015; Hristov et al, 2020). A combination of anthropogenic stressors appears to drive honeybee declines (Meeus et al, 2018), including reduced habitats (Naug, 2009; Breeze et al, 2014), reduced genetic diversity (Espregueira Themudo et al, 2020), use of antimicrobials in apiculture (Tian et al, 2012; Li et al, 2017; Raymann et al, 2017), and pesticide application (Boncristiani et al, 2012; Williamson et al, 2014; Johnson, 2015)
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