Pollinators mediate floral microbial diversity and microbial network under agrochemical disturbance

Abstract

How pollinators mediate microbiome assembly in the anthosphere is a major unresolved question of theoretical and applied importance in the face of anthropogenic disturbance. We addressed this question by linking visitation of diverse pollinator functional groups (bees, wasps, flies, butterflies, beetles, true bugs and other taxa) to the key properties of the floral microbiome (microbial α‐ and β‐diversity and microbial network) under agrochemical disturbance, using a field experiment of bactericide and fungicide treatments on cultivated strawberries that differ in flower abundance. Structural equation modelling was used to link agrochemical disturbance and flower abundance to pollinator visitation to floral microbiome properties. Our results revealed that (i) pollinator visitation influenced the α‐ and β‐diversity and network centrality of the floral microbiome, with different pollinator functional groups affecting different microbiome properties; (ii) flower abundance influenced the floral microbiome both directly by governing the source pool of microbes and indirectly by enhancing pollinator visitation; and (iii) agrochemical disturbance affected the floral microbiome primarily directly by fungicide, and less so indirectly via pollinator visitation. These findings improve the mechanistic understanding of floral microbiome assembly, and may be generalizable to many other plants that are visited by diverse insect pollinators in natural and managed ecosystems.

Contrasting microbial communities on male and female flowers of a dioecious plant, Mallotus japonicus (Euphorbiaceae)

“…It has been reported that insect visitors play important roles in vectoring flower microbes in M . japonicus and many other plant species (Russell et al, 2019; Ushio et al, 2015; Wei et al, 2020), while the importance of dispersal by flower visitors may differ between male and female flowers or among microbes. Insect visitors may be important vectors of some bacteria, such as ASV02P1, ASV03M1, ASV04E1, and ASV09E2 abundant on male flowers.…”

“…Pollinators and herbivores carry microbes on their body surface, in their gut system, or on the surface of the pollen attached to their body (Herrera et al, 2009; Manirajan et al, 2018; Sasu et al, 2010; Ushio et al, 2015), though their effects may vary among visitor groups and individuals. A recent study (Wei et al, 2020) showed that different pollinator guilds had distinct effects on both the alpha and beta diversity of floral microbes on cultivated strawberries. Bees, which are extensive foragers, increased alpha diversity by enhancing colonization, while true bugs and flies contributed to microbial community differentiation and increased beta diversity.…”

“…This is partly because most of the studies on floral microbes have been performed in hermaphrodites or only examined microbes in floral nectar of a dioecious plant (Golonka & Vilgalys, 2013; Tsuji & Fukami, 2018). A limited study of whole flower microbial community reported significant difference in the microbial compositions and diversity between the sexes in dioecious strawberries, but the study did not examine detailed taxonomic differences below the phylum and their underlying mechanisms (Wei et al, 2020).…”

Flower colour and flowering phenology mediate plant–pollinator interaction assembly in a diverse co‐flowering community

“…The study was conducted in a diverse serpentine seep co‐flowering community at the McLaughlin Natural Reserve in northern California, USA (38°51′41.4″N, 122°23′54.8″W; banana slug site in Koski et al, 2015; Wei et al, 2021). This reserve is part of the University of California Natural Reserve System, which provided permission to conduct the study.…”

“…plant communities; Ashman et al, 2020; Götzenberger et al, 2012). This is mainly due to the difficulty of incorporating the intrinsic complexities of species‐rich communities and the interactions within them (Ashman et al, 2020; Götzenberger et al, 2012; Hegland et al, 2009; Wei et al, 2021). This gap in knowledge has in turn hindered our ability to gain a more complete understanding of the ecological processes and underlying mechanisms that shape natural communities (Ashman et al, 2020; Götzenberger et al, 2012; Wolowski et al, 2017).…”