Herbivory and Time Since Flowering Shape Floral Rewards and Pollinator-Pathogen Interactions.

Herbivory can induce chemical changes throughout plant tissues including flowers, which could affect pollinator-pathogen interactions. Pollen is highly defended compared to nectar, but no study has examined whether herbivory affects pollen chemistry. We assessed the effects of leaf herbivory on nectar and pollen alkaloids in Nicotiana tabacum, and how herbivory-induced changes in nectar and pollen affect pollinator-pathogen interactions. We damaged leaves of Nicotiana tabacum using the specialist herbivore Manduca sexta and compared nicotine and anabasine concentrations in nectar and pollen. We then pooled nectar and pollen by collection periods (within and after one month of flowering), fed them in separate experiments to bumble bees (Bombus impatiens) infected with the gut pathogen Crithidia bombi, and assessed infections after seven days. We did not detect alkaloids in nectar, and leaf damage did not alter the effect of nectar on Crithidia counts. In pollen, herbivory induced higher concentrations of anabasine but not nicotine, and alkaloid concentrations rose and then fell as a function of days since flowering. Bees fed pollen from damaged plants had Crithidia counts 15 times higher than bees fed pollen from undamaged plants, but only when pollen was collected after one month of flowering, indicating that both damage and time since flowering affected interaction outcomes. Within undamaged treatments, bees fed late-collected pollen had Crithidia counts 10 times lower than bees fed early-collected pollen, also indicating the importance of time since flowering. Our results emphasize the role of herbivores in shaping pollen chemistry, with consequences for interactions between pollinators and their pathogens.

From plant fungi to bee parasites: mycorrhizae and soil nutrients shape floral chemistry and bee pathogens.

Bee populations have experienced declines in recent years, due in part to increased disease incidence. Multiple factors influence bee-pathogen interactions, including nectar and pollen quality and secondary metabolites. However, we lack an understanding of how plant interactions with their environment shape bee diet quality. We examined how plant interactions with the belowground environment alter floral rewards and, in turn, bee-pathogen interactions. Soil-dwelling mycorrhizal fungi are considered plant mutualists, although the outcome of the relationship depends on environmental conditions such as nutrients. In a 2 × 2 factorial design, we asked whether mycorrhizal fungi and nutrients affect concentrations of nectar and pollen alkaloids (anabasine and nicotine) previously shown to reduce infection by the gut pathogen Crithidia in the native bumble bee Bombus impatiens. To ask how plant interactions affect this common bee pathogen, we fed pollen and nectar from our treatment plants, and from a wildflower pollen control with artificial nectar, to bees infected with Crithidia. Mycorrhizal fungi and fertilizer both influenced flowering phenology and floral chemistry. While we found no anabasine or nicotine in nectar, high fertilizer increased anabasine and nicotine in pollen. Arbuscular mycorrhizal fungi (AMF) decreased nicotine concentrations, but the reduction due to AMF was stronger in high than low-nutrient conditions. AMF and nutrients also had interactive effects on bee pathogens via changes in nectar and pollen. High fertilizer reduced Crithidia cell counts relative to low fertilizer in AMF plants, but increased Crithidia in non-AMF plants. These results did not correspond with effects of fertilizer and AMF on pollen alkaloid concentrations, suggesting that other components of pollen or nectar were affected by treatments and shaped pathogen counts. Our results indicate that soil biotic and abiotic environment can alter bee-pathogen interactions via changes in floral rewards, and underscore the importance of integrative studies to predict disease dynamics and ecological outcomes.