Direct and indirect effects of land use on microbiomes of trap-nesting solitary bee larvae and nests

Abstract

Introduction: The global decline in biodiversity and insect populations highlights the urgent need to conserve ecosystem functions, such as plant pollination by solitary bees. Human activities, particularly agricultural intensification, pose significant threats to these essential services. Changes in land use alter resource and nest site availability, pesticide exposure and other factors impacting the richness, diversity, and health of solitary bee species. In this study, we investigated yet another facet currently less well investigated in such context: Microbial communities associated with wild bees play crucial roles in larval development, metabolism, immunity and overall bee health. However, the drivers and dynamics of healthy microbiome in solitary bees are still poorly understood, especially regarding the direct and indirect effects of land use on the diversity and composition of these microbial communities.

Methods: We examined bacterial communities in the offspring and nest materials of the Megachilid trap-nesting solitary bee, Osmia bicornis, along a gradient of land use intensification by 16S rRNA gene metabarcoding. Given that landscape composition, climatic conditions, and food resources are known to influence microbial compositions in solitary bee species, we hypothesized that land use changes would alter resources available for food and nest material collection and thereby affecting the microbiomes in offspring and their nest environments. We anticipated reduced microbial diversity and altered composition with increased land use intensification, which is known to decrease the number and diversity of resources, including the pool of floral and soil bacteria in the surrounding environment.

Results: As expected, we observed significant shifts in the bacterial composition and diversity of bees and their nests across varying degrees of land use intensity, differing in management types and the availability of flowers. The Shannon diversity of bacteria in nest materials (larval pollen provision, soil nest enclosure) and larval guts decreased with increasing land use intensity. However, the pupae microbiome remained unaffected, indicating a reorganization of the microbiome during metamorphosis, which is not significantly influenced by land use and available resources.

Discussion: Our findings provide new insights into the factors shaping environmental transmission and changes in solitary bee microbiomes. This understanding is crucial for comprehending the impacts of intensive land use on wild bee health and developing strategies to mitigate these effects.

Keywords: Biodiversity Exploratories; Osmia bicornis; grasslands; metabarcoding; pollination; solitary bee microbiome.

Figure 1

(A) Differences in bacterial compositions of O. bicornis sample types (larval pollen provisions, soil nest enclosures, bee larvae & bee pupae) (represented by different colors) by non-metrical multi-dimensional scaling (NMDS, stress = 0.102) based on Bray-Curtis distances using transformed relative abundances data of ASV (amplicon sequent variants). ASVs were plotted for all bee nest specimens for all 27 plots. Each dot represents one sample of one nest (n = 144) (A). Variabilities in community structures of different bee species and specimen types. (B) The analysis of Bray-Curtis distances as distances to group centroids of each community. Differences between sample types were assessed by multivariate analysis of group dispersions (betadisper/adonis).

Figure 2

Effects of land use intensity (LUI) on (A) the Shannon plant diversity of plot vegetation and (B) pollen larval provisions, as well as Shannon bacterial diversity of (C) larvae, (D) pupae, (E) pollen larval provisions and (F) soil nest closings of Osmia bicornis sampled from trap nests installed at plots differing in land use intensity (LUI) in three biogeographical regions in Germany (Exploratories: Swabian Alb, Hainich-Dün and Schorfheide-Chorin). Shannon diversity is based on revealed ASVs (Amplicon sequent variants) per bee nest. Data for (A,B) was obtained through Peters et al. (2022) for comparison.

Figure 3

Variabilities in community structures of different land-use intensities (LUI categories: low-high) and O. bicornis bacterial microbiomes. The analysis of Bray-Curtis distances represents the beta-diversity as distances to group centroids of each community. Differences between land-use categories within a specimen group (A–D) were assessed by multivariate analysis of group dispersions (betadisper/adonis).

Figure 4

Schematic overview about the influence of land use intensity on bacterial microbiome diversity of different bee nest components, especially bee larvae.