Legitimate visitors and nectar robbers of Aquilegia formosa have different effects on nectar bacterial communities

Abstract

Metacommunity structure is strongly influenced by dispersal between habitat patches. Dispersal mode (e.g., active or passively via vector, wind, or water) is recognized to influence metacommunity dynamics, but it is not well understood how within-mode heterogeneity impacts dispersal and community assembly, particularly for microbial communities. Microbes often rely on flower visitors for dispersal among short-lived floral nectar habitats, but it is unclear whether flower visitor guilds (e.g., legitimate visitors vs. larcenists) differentially influence nectar microbial diversity and community structure. We surveyed the community of legitimate nectar foragers and nectar robbers, which damage flowers to obtain floral rewards, of Aquilegia formosa. Then, we evaluated how manipulating access by legitimate nectar foragers, primary nectar robbers, and/or secondary nectar robbers influenced the diversity, species composition, and beta diversity of nectar bacteria within individual flowers. A taxonomically diverse insect community visited A. formosa, and visitors differentially influenced nectar bacterial community structure at within-flower (local) and among-flower (regional) scales. When legitimate nectar foragers were allowed to access A. formosa, we observed an increase in bacterial diversity and changes in bacterial species composition such that common nectar bacteria had higher relative abundances. In contrast, effects of natural and simulated robbing had little effect on bacterial alpha diversity, but simulated robbing decreased the relative abundance of common nectar bacteria, and natural nectar robbing events reduced beta diversity of nectar bacteria. This work highlights the importance of visitor identity on microbial diversity and species composition in flowers, and, more broadly, suggests that vectors can differentially influence metacommunity structure.

Movers and shakers: Bumble bee foraging behavior shapes the dispersal of microbes among and within flowers

“…), patterns of microbial community structure in nature are likely more diverse than our study implies, though they might still reflect the dominant pollinator foraging behavior (e.g., nectaring, scrabbling, buzzing; see also Zemenick et al. ). Additionally, while artificial flowers compared to live flowers likely differ in physical properties that affect microbial dispersal, in the present study dispersal patterns were qualitatively similar between live and artificial flowers.…”

“…We should note however that floral organ size likely shapes microbial receipt (larger flower organs received more microbes in our study) and that bumble bees foraging for nectar on artificial flowers deposited microbes equally among floral organs (though we could have found no effect due to low microbial dispersal by nectar foragers). Given that floral organ size varies among plant species and that pollinators may use multiple foraging behaviors on a single flower (Laverty 1980, Corbet et al 1988), patterns of microbial community structure in nature are likely more diverse than our study implies, though they might still reflect the dominant pollinator foraging behavior (e.g., nectaring, scrabbling, buzzing; see also Zemenick et al 2018). Additionally, while artificial flowers compared to live flowers likely differ in physical properties that affect microbial dispersal, in the present study dispersal patterns were qualitatively similar between live and artificial flowers.…”

“…Pollinators exhibit different foraging behaviors at flowers that could result in different patterns of microbial dispersal (Zemenick et al 2018). Pollinators such as bees must extract pollen and nectar from flowers, which necessitates use of highly distinct behaviors, even on the same flower (Free 1968, Corbet et al 1988, Westerkamp 1999.…”

Linked networks reveal dual roles of insect dispersal and species sorting for bacterial communities in flowers

“…However, poor vectors of pollen could be just as effective in vectoring microbes as pollinators. Previous work has shown that herbivores (Samuni-Blank et al 2014) and nectar robbers (Zemenick et al 2018) have distinct effects on microbial community composition. In the current study, a strong correlation between non-bee Hymenoptera and floral bacterial communities (Fig.…”

Towards a better understanding of the role of nectar-inhabiting yeasts in plant–animal interactions

“…to feed on nectar, seek shelter or use these as mating/nesting places), pollen can get attached to their body surfaces and subsequently be spread to new flowers [1,4]. Pollinators and non-pollinating visitors are not sterile but carry diverse microbial communities, particularly consisting of bacteria and fungi, that may disperse to nectar and the surface of other floral parts such as the corolla, stamens, and pistil when visiting flowers [5][6][7][8][9][10][11]. The dispersal of microbes from flower to flower by animal vectors is a dynamic process that keeps ongoing during the flower lifetime [6,9,10].…”