Medicinal value of sunflower pollen against bee pathogens

Abstract

Global declines in pollinators, including bees, can have major consequences for ecosystem services. Bees are dominant pollinators, making it imperative to mitigate declines. Pathogens are strongly implicated in the decline of native and honey bees. Diet affects bee immune responses, suggesting the potential for floral resources to provide natural resistance to pathogens. We discovered that sunflower (Helianthus annuus) pollen dramatically and consistently reduced a protozoan pathogen (Crithidia bombi) infection in bumble bees (Bombus impatiens) and also reduced a microsporidian pathogen (Nosema ceranae) of the European honey bee (Apis mellifera), indicating the potential for broad anti-parasitic effects. In a field survey, bumble bees from farms with more sunflower area had lower Crithidia infection rates. Given consistent effects of sunflower in reducing pathogens, planting sunflower in agroecosystems and native habitat may provide a simple solution to reduce disease and improve the health of economically and ecologically important pollinators.

Figure 1

(A) Effects of pollen diets on Crithidia infection in individual Bombus impatiens workers. Bees were inoculated with Crithidia and fed a monofloral pollen diet commonly grown in large monocultures in agroecosystems: sunflower (Helianthus annuus; Sun), buckwheat (Fagopyrum cymosum; Buck), rapeseed (Brassica campestris; Rape), or a mixed diet composed of equal weights of the three monofloral pollens (Mix). (B) Pollen diets did not significantly affect rate of worker death over the 7 d experiment shown in (A). Y-axis shows exponentiated hazard rates ±1 standard error. (C) Crithidia infection was allowed to build for one week post-inoculation before providing pollen treatments: sunflower (Sun), buckwheat (Buck), or a wildflower pollen mixture (WF Mix). (D) Inoculated bees were fed sunflower pollen from two sources, China (CN) or USA (USA), or a control wildflower pollen mixture (WF Mix). Bars and error bars indicate negative binomial model means ±1 standard error back-transformed (i.e., exponentiated) from the scale of the linear predictor. Crithidia counts represent raw counts of cells diluted in a gut homogenate. Error bars represent uncertainty in fixed effects portions of models only, and do not account for variability due to random effects. Different letters above each bar within panels indicate significant differences based on Tukey’s HSD tests.

Figure 2

Bombus impatiens microcolony performance. Microcolonies were fed either buckwheat (Buck) or sunflower (Sun) pollen diets and either inoculated with Crithidia (Infected) or a Crithidia-free control solution (Uninfected). Infection did not significantly affect responses in A-C and so responses were averaged across infection treatments for these panels. (A) Mean number of larvae produced, (B) mean total larval mass, (C) proportion of microcolonies that produced pupae during the experiment, and (D) mean number of eggs produced. Crithidia infection reduced egg production in microcolonies fed buckwheat pollen, but not sunflower pollen. For all panels, error bars indicate ±1 standard error. Error bars represent uncertainty in fixed effects portions of models only, and do not account for variability due to random effect.

Figure 3

Effects of pollen diet on Nosema infection in honey bees (Apis mellifera). (A) Sunflower pollen reduced Nosema infection in honey bees by an average of 29% compared to buckwheat pollen across the two time periods. Bars and error bars indicate negative binomial model means ±1 standard error back-transformed (i.e., exponentiated) from the scale of the linear predictor. Error bars represent uncertainty in fixed effects portions of models only, and do not account for variability due to random effect. (B) Exponentiated hazard rates ±1 standard error for mortality on different pollen diets. Sunflower-fed bees died at nearly four times the rate of buckwheat-fed bees and had equivalent survival to bees with no pollen. Lower-case letters indicate significant differences based on post hoc pairwise comparisons; in (A), comparisons are made within each time point (10 d and 15 d).

Figure 4

Negative relationship between the area of sunflower planted on farms and Crithidia infection intensity in Bombus impatiens workers. Line and shaded band indicate back-transformed mean Crithidia counts for area of sunflower planted ±1 standard error; points show counts for individual bees.