Contrasting effects of fungicide and herbicide active ingredients and their formulations on bumblebee learning and behaviour

Abstract

ABSTRACT Fungicides and herbicides are two of the most heavily applied pesticide classes in the world, but receive little research attention with regards to their potential impacts on bees. As they are not designed to target insects, the mechanisms behind potential impacts of these pesticides are unclear. It is therefore important to understand their influence at a range of levels, including sublethal impacts on behaviours such as learning. We used the proboscis extension reflex (PER) paradigm to assess how the herbicide glyphosate and the fungicide prothioconazole affect bumblebee olfactory learning. We also assessed responsiveness, and compared the impacts of these active ingredients and their respective commercial formulations (Roundup Biactive and Proline). We found that learning was not impaired by either formulation but, of the bees that displayed evidence of learning, exposure to prothioconazole active ingredient increased learning level in some situations, while exposure to glyphosate active ingredient resulted in bumblebees being less likely to respond to antennal stimulation with sucrose. Our data suggest that fungicides and herbicides may not negatively impact olfactory learning ability when bumblebees are exposed orally to field-realistic doses in a lab setting, but that glyphosate has the potential to cause changes in responsiveness in bees. As we found impacts of active ingredients and not commercial formulations, this suggests that co-formulants may modify impacts of active ingredients in the products tested on olfactory learning without being toxic themselves. More research is needed to understand the mechanisms behind potential impacts of fungicides and herbicides on bees, and to evaluate the implications of behavioural changes caused by glyphosate and prothioconazole for bumblebee fitness.