Pathogens are one of the factors driving pollinator declines. Diet can play an important role in mediating pollinator health and resistance to pathogens. Sunflower pollen ( Helianthus annuus ) dramatically reduced a gut pathogen ( Crithidia bombi ) of Bombus impatiens previously, but the breadth of this effect was unknown. We tested whether pollen from nine H. annuus cultivars, four wild H. annuus populations, H. petiolarus, H. argophyllus and two Solidago spp., reduced Crithidia in B. impatiens compared to mixed wildflower pollen and buckwheat pollen ( Fagopyrum esculentum ) as controls. We also compared hand- and honeybee-collected pollen (which contains nectar) to assess whether diet effects on pathogens were due to pollen or nectar. All Helianthus and Solidago pollen reduced Crithidia by 20–40-fold compared to buckwheat pollen, and all but three taxa reduced Crithidia compared to wildflower pollen. We found no consistent differences between hand- and bee-collected pollen, suggesting that pollen alone can reduce Crithidia infection. Our results indicate an important role of pollen diet for bee health and potentially broad options within the Asteraceae for pollinator plantings to manage bee disease.

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 9 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.

Young for help with data collection and feedback, the UMass Amherst Quantitative Statistics Group for feedback on statistical analyses, Biobest (Ontario, Canada) for donating bumblebee colonies, and J. van Wyk and R. Malfi for providing constructive comments on the manuscript.

Little is known about how simultaneous antagonistic interactions on plants and pollinators affect pollination services, even though herbivory can alter floral traits and parasites can change pollinator learning, perception, or behavior. We investigated how a common herbivore and bumble bee (Bombus spp.) parasite impact pollination in tomatoes (Solanum lycopersicum L.) (Solanales: Solanaceae). We exposed half the plants to low-intensity herbivory by the specialist Manduca sexta L. (Lepidoptera: Sphigidae), and observed bumble bee visits and time spent on flowers of damaged and control plants. Following observations, we caught the foraging bees and assessed infection by the common gut parasite, Crithidia bombi Lipa & Triggiani (Trypanosomatida: Trypanosomatidae). Interestingly, we found an interactive effect between herbivory and Crithidia infection; bees with higher parasite loads spent less time foraging on damaged plants compared to control plants. However, bees did not visit higher proportions of flowers on damaged or control plants, regardless of infection status. Our study demonstrates that multiple antagonists can have synergistic negative effects on the duration of pollinator visits, such that the consequences of herbivory may depend on the infection status of pollinators. If pollinator parasites indeed exacerbate the negative effects of herbivory on pollination services, this suggests the importance of incorporating bee health management practices to maximize crop production.