Author contributions. LSA, REI and PCS conceived of and designed the study. PCS and IWF conducted chemical analysis of pollen and synthesized spermidines. AEF, RLM, PRA, LMC, PMD, and SL carried out bioassay experiments. AEF analyzed data and prepared figures. LSA wrote the manuscript with substantial contributions from PCS. All co-authors read and provided feedback on the manuscript.

1. Social insect castes and sexes differ in many ways, including morphology, behavior, and sometimes ploidy level. Recent studies have found that consuming sunflower pollen reduces the gut pathogen Crithidia bombi in workers of the common eastern bumble bee (Bombus impatiens). Here, this work is extended to the reproductive individuals that represent colony fitness-males and queens-to assess if the medicinal effects of sunflower pollen vary with bee caste and sex. 2. This study examined the effect of sunflower pollen compared to a diverse wildflower pollen mix on infection in worker, male, and daughter queen commercial B. impatiens. Bees were infected, fed either sunflower pollen or wildflower pollen for 7 days, and then infection levels were assessed. 3. Compared to wildflower pollen, sunflower pollen dramatically reduced Crithidia infection in workers and daughter queens, but not males. Infection levels were very low for both diets in males; this could be due to low pollen consumption or other mechanisms. 4. Reducing Crithidia infection in young queens before they undergo hibernation is important for population dynamics since infected queens are less likely to survive hibernation, and those that do are less likely to successfully establish a nest the following spring. Because sunflowers bloom in late summer when new queens are emerging, sunflowers could provide an important dietary component for queens during this critical life stage. Deepening our understanding of how diet impacts pathogens in reproductive bees, as well as workers, is crucial to maintain healthy pollinator populations.

Because carnivorous plants rely on arthropods as pollinators and prey, they risk consuming would-be mutualists. We examined this potential conflict in the Venus flytrap (Dionaea muscipula), whose pollinators were previously unknown. Diverse arthropods from two classes and nine orders visited flowers; 56% of visitors carried D. muscipula pollen, often mixed with pollen of coflowering species. Within this diverse, generalized community, certain bee and beetle species appear to be the most important pollinators, on the basis of their abundance, pollen load size, and pollen fidelity. Dionaea muscipula prey spanned four invertebrate classes and 11 orders; spiders, beetles, and ants were most common. At the family and species levels, few taxa were shared between traps and flowers, yielding a near-zero value of niche overlap for these potentially competing structures. Spatial separation of traps and flowers may contribute to partitioning the invertebrate community between nutritional and reproductive functions in D. muscipula.

Commercial bumblebees have become popular models to understand stressors and solutions for pollinator health, but few studies test whether results translate to other pollinators. Consuming sunflower pollen dramatically reduces infection by the gut parasite Crithidia bombi in commercially reared Bombus impatiens . We assessed the effect of sunflower pollen on infection in wild B. impatiens , Bombus griseocollis, Bombus bimaculatus and Bombus vagans . We also asked how pollen diet (50% sunflower pollen versus wildflower pollen) and infection (yes/no) affected performance in wild B. impatiens microcolonies. Compared to controls, sunflower pollen dramatically reduced Crithidia infection in commercial and wild B. impatiens, had similar but less dramatic effects in B. bimaculatus and B. vagans , and no effect in B. griseocollis . Bombus impatiens, B. bimaculatus and B. vagans are in the same subgenus, suggesting that responses to sunflower pollen may be phylogenetically conserved. In microcolonies, 50% sunflower pollen reduced infection compared to wildflower pollen, but also reduced reproduction. Sunflower pollen could control Crithidia infections in B. impatiens and potentially close relatives, but may hinder reproduction if other resources are scarce. We caution that research using managed bee species, such as B. impatiens , be interpreted carefully as findings may not relate to all bee species.

Parasites are linked to the decline of some bee populations; thus, understanding defense mechanisms has important implications for bee health. Recent advances have improved our understanding of factors mediating bee health ranging from molecular to landscape scales, but often as disparate literatures. Here, we bring together these fields and summarize our current understanding of bee defense mechanisms including immunity, immunization, and transgenerational immune priming in social and solitary species. Additionally, the characterization of microbial diversity and function in some bee taxa has shed light on the importance of microbes for bee health, but we lack information that links microbial communities to parasite infection in most bee species. Studies are beginning to identify how bee defense mechanisms are affected by stressors such as poor-quality diets and pesticides, but further research on this topic is needed. We discuss how integrating research on host traits, microbial partners, and nutrition, as well as improving our knowledge base on wild and semi-social bees, will help inform future research, conservation efforts, and management.

Certain diets can benefit bee health by reducing pathogens, but the mechanism(s) driving these medicinal effects are largely unexplored. Recent research found that sunflower ( Helianthus annuus ) pollen reduces the gut pathogen Crithidia bombi in the common eastern bumblebee ( Bombus impatiens ). Here, we tested the effects of sunflower pollen and infection on two bee immune metrics to determine whether sunflower pollen diet drives changes in host immunity that can explain this medicinal effect. Bees were infected with C. bombi or not and given either sunflower or wildflower pollen. Subsequently, bees received a benign immune challenge or were left naive to test the induced and constitutive immune responses, respectively. We measured haemolymph phenoloxidase activity, involved in the melanization cascade, and antibacterial activity. Sunflower pollen reduced C. bombi infection, but we found no significant pollen diet effect on either immune measure. Phenoloxidase activity was also not affected by C. bombi infection status; however, uninfected bees were more likely to have measurable constitutive antibacterial activity, while infected bees had higher induced antibacterial activity. Overall, we found that sunflower pollen does not significantly affect the immune responses we measured, suggesting that the mechanisms underlying its medicinal effect do not involve these bee immune parameters. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.

Plants have unique chemical and physical traits that can reduce infections in animals ranging from primates to caterpillars. Sunflowers (Helianthus annuus; Asteraceae) are one striking example, with pollen that suppresses infections by the trypanosomatid gut pathogen Crithidia bombi in the common eastern bumble bee (Bombus impatiens). However, the mechanism underlying this effect has remained elusive, and we do not know whether pollens from other Asteraceae species have similar effects. We evaluated whether mechanisms mediating sunflower pollen's antipathogenic effects are physical (due to its spiny exine), chemical (due to metabolites) or both. We also evaluated the degree to which pollen from seven other Asteraceae species reduced C. bombi infection relative to pollen from sunflower and two non‐Asteraceae species, and whether pollen spine length predicted pathogen suppression. We found that sunflower exines alone reduced infection as effectively as whole sunflower pollen, while sunflower pollen metabolites did not. Furthermore, bees fed pollen from four of seven other Asteraceae had 62%–92% lower C. bombi infections than those fed non‐Asteraceae pollen. Spine length, however, did not explain variation in bumble bee infection. Our study indicates that sunflower pollen's capacity to suppress C. bombi is driven by its spiny exine, and that this phenomenon extends to several other Asteraceae species. Our results indicate that sunflower pollen exines are as effective as whole pollen in reducing infection, suggesting that future studies should expand to assess the effects of other species with spiny pollen on pollinator–pathogen dynamics. Read the free Plain Language Summary for this article on the Journal blog.

No abstract