COS 313-3 - A leaf-associated fungus alters leaf preferences of leafcutter bees and decreases the growth of bee pathogens

Abstract: Plant-insect interactions can be influenced by their biotic context, including microbes associated with either partner. Leafcutter bees (Megachile sp.) cut discs from living leaves and use them as nest lining, a behavior that brings developing larvae into close contact with both plant tissue and plant-associated microbes, which could affect nests either positively or negatively. In southern Arizona, leafcutter bees often cut leaves of roses (Rosa x hybrida), which harbor rich microbial communities on leaf surfaces. Previously, we found that fungi in Aspergillus sect. Nigri are more common on rose leaves cut by leafcutter bees than on non-cut leaves, and that leaves experimentally treated with Aspergillus receive more cuts than control leaves. Given that many Aspergillus strains produce secondary metabolites that inhibit growth of other fungi, we hypothesized that Aspergillus protects leafcutter bee larvae against entomopathogens. To test this hypothesis, we measured the degree to which fungi from rose leaves (Aspergillus or Alternaria alternata, which is abundant on rose leaves but has no effect on cutting) inhibited four entomopathogens in vitro (three strains of Ascosphaera spp., which are pathogens of bees, and Beauveria bassiana, a generalist pathogen). We predicted that entomopathogens would be inhibited more by Aspergillus than by Alternaria. Consistent with our prediction, growth of Ascosphaera strains in vitro was inhibited markedly by Aspergillus, while Alternaria inhibited Ascosphaera significantly less. However, we found that the generalist entomopathogen B. bassiana was inhibited minimally and similarly by both Aspergillus and Alternaria. Ascosphaera strains cause chalkbrood, which can be a significant source of mortality in bee nests. Therefore, choosing nest material that protects against this pathogen could be critical for bees’ fitness. While further research is needed to confirm that Aspergillus has a protective role in a more realistic nest setting, our results suggest that this common fungus may slow the growth of bee-associated pathogens. If consistent across leafcutter bee species, this result could have implications for the health of alfalfa leafcutter bees, important agricultural pollinators. More broadly, our work suggests that a common member of phylloplane fungal communities has the potential to mediate the outcome of a plant-insect interaction, influencing both which leaves and plants receive damage, and the risk of pathogen infection during a vulnerable life stage for bees.