Poison or Potion: Effects of Sunflower Phenolamides on Bumble Bees and Their Gut Parasite

SIMPLE SUMMARY: Bee declines have been reported worldwide, partly due to parasite spread induced by human activities. However, bees may forage on specific floral resources to face parasite infection. Such natural resources are comparable to ‘natural pharmacies’ and may be favoured in bee conservation strategies. Consumption of sunflower pollen, despite being detrimental for larval development, has been recently shown to reduce the load of a widespread bumble bee gut parasite in the common eastern bumble bee. Although the underlying mechanisms remain unknown, it has been suggested that sunflower phenolamides—a family of molecules found in most flowering plants—may be responsible for such a reduction in parasite load. Here, we tested the impacts of sunflower phenolamides on healthy and infected buff-tailed bumble bees. Expectedly, sunflower pollen had harmful consequences on bumble bee development but surprisingly, it did not alter parasite load. By contrast, sunflower phenolamides had milder effects on bumble bee development but unexpectedly increased parasite load. Phenolamide effects may stem from the physiological stress they induced or the gut microbial community alteration they may have triggered. Since biological models and experimental framework differ greatly in related studies tackling plant–bee–parasite interplays, we challenged the definition of medicinal effects and questioned the way to assess them in controlled conditions. ABSTRACT: Specific floral resources may help bees to face environmental challenges such as parasite infection, as recently shown for sunflower pollen. Whereas this pollen diet is known to be unsuitable for the larval development of bumble bees, it has been shown to reduce the load of a trypanosomatid parasite (Crithidia bombi) in the bumble bee gut. Recent studies suggested it could be due to phenolamides, a group of compounds commonly found in flowering plants. We, therefore, decided to assess separately the impacts of sunflower pollen and its phenolamides on a bumble bee and its gut parasite. We fed Crithidia-infected and -uninfected microcolonies of Bombus terrestris either with a diet of willow pollen (control), a diet of sunflower pollen (natural diet) or a diet of willow pollen supplemented with sunflower phenolamides (supplemented diet). We measured several parameters at both microcolony (i.e., food collection, parasite load, brood development and stress responses) and individual (i.e., fat body content and phenotypic variation) levels. As expected, the natural diet had detrimental effects on bumble bees but surprisingly, we did not observe any reduction in parasite load, probably because of bee species-specific outcomes. The supplemented diet also induced detrimental effects but by contrast to our a priori hypothesis, it led to an increase in parasite load in infected microcolonies. We hypothesised that it could be due to physiological distress or gut microbiota alteration induced by phenolamide bioactivities. We further challenged the definition of medicinal effects and questioned the way to assess them in controlled conditions, underlining the necessity to clearly define the experimental framework in this research field.