Dominant bee species and floral abundance drive parasite temporal dynamics in plant-pollinator communities

Abstract

Pollinator declines can leave communities less diverse and potentially at increased risk to infectious diseases. Species-rich plant and bee communities have high species turnover, making the study of disease dynamics challenging. To address how temporal dynamics shape parasite prevalence in plant and bee communities, we screened >5,000 bees and flowers through an entire growing season for five common bee microparasites ( Nosema ceranae , N. bombi , Crithidia bombi , C. expoeki and neogregarines). Over 110 bee species and 89 flower species were screened, revealing 42% of bee species (12.2% individual bees) and 70% of flower species (8.7% individual flowers) had at least one parasite in or on them, respectively. Some common flowers (e.g., Lychnis flos-cuculi ) harboured multiple parasite species, whilst others (e.g., Lythrum salicaria ) had few. Significant temporal variation of parasite prevalence in bees was linked to bee diversity, bee and flower abundance, and community composition. Specifically, we found that bee communities had the highest prevalence late in the season, when social bees ( Bombus spp. and Apis mellifera ) were dominant and bee diversity was lowest. Conversely, prevalence on flowers was lowest late in the season when floral abundance was the highest. Thus, turnover in the bee community impacted community-wide prevalence, and turnover in the plant community impacted when parasite transmission was likely to occur at flowers. These results imply that efforts to improve bee health will benefit from promoting high floral numbers to reduce transmission risk, maintaining bee diversity to dilute parasites, and monitoring the abundance of dominant competent hosts.

Metatranscriptome Analysis of Sympatric Bee Species Identifies Bee Virus Variants and a New Virus, Andrena-Associated Bee Virus-1

“…The observation that AnBV-1 infections were detected only in honey bees at the Luzit site, which had low floral diversity and high honey bee activity, indicates that AnBV-1 may also spread between co-foraging honey bees ( Supplementary Table S6). Whereas the relationships observed here are consistent with those expected under interspecific transmission through shared flowers, and similar to reported results from other studies that followed the temporal dynamics of different pollinator pathogen infections [161], our field data were obtained on a single sample date, and it is likely that AnBV-1 infection prevalence in honey bees, mining bees, and other bees and insects not screened in our study varies with time. Therefore, prevalence at a particular sampling date represents the status of the system on a particular sampling date (or point in time).…”

“…Indeed, AnBV-1 infections in honey bees were detected in sites with low floral diversity and were absent in honey bees in high floral diversity sites ( Figure 6C and Supplementary Table S6). These results suggest a strong effect of epidemiological dilution by flower species diversity [161,162,163,164]; in sites with high floral diversity, the generalist honey bees can forage on a wide range of floral species, and therefore their exposure to flowers that are visited by mining bees, which primarily forage on yellow mustard plants, is reduced. The correlation between low flower diversity and AnBV-1 infection in honey bees can also be explained by other, non-mutually-exclusive mechanisms.…”

“…This suggests, epidemiological dilution by flower abundance. Since flowers can serve as virus transmission hubs [161], the number of AnBV-1 contaminated flowers can be diluted by many non-contaminated flowers, reducing the probability of sharing the same individual flowers between an infected mining bee and an uninfected honey bee. At very high densities of AnBV-1-infected mining bees, the impact of shared flower abundance in sites with low floral diversity appears to reverse ( Figure 6B, red lines), perhaps because of honey bee recruitment to dominant floral resources [168].…”

Crithidia bombi can infect two solitary bee species while host survivorship depends on diet

“…Most bee species within a community can be exposed to numerous pathogens when foraging at flowers, including C. bombi (Figueroa et al ., 2020; Graystock et al ., 2020). Our results support a growing body of literature indicating the need to assess the host range of bee pathogens, including assessments of replication and impacts on survival (Bramke et al ., 2019; Müller et al ., 2019).…”

“…While C. bombi is known to infect multiple bumble bee species (Colla et al ., 2006; Cordes et al ., 2012; Ruiz-González et al ., 2012), honey bees are not a known host (Ruiz-González and Brown, 2006; Graystock et al ., 2015), even though both groups belong to the same family. It is largely unknown whether solitary bee species, which frequently test positive for C. bombi via PCR-based screenings (Figueroa et al ., 2020; Graystock et al ., 2020), are actually infected by this pathogen (Ravoet et al ., 2014). The solitary bees Osmia lignaria and M. rotundata are cavity-nesting species that provide important pollination services for fruits and vegetables in North America and Europe (Velthuis and van Doorn, 2006; Pitts-Singer and Cane, 2011; Brittain et al ., 2013) and can serve as model organisms for experimentally evaluating epidemiological questions due to their commercial availability.…”