The effects of urban land use gradients on wild bee microbiomes

Abstract

Bees and their microbes interact in complex networks in which bees form symbiotic relationships with their bacteria and fungi. Microbial composition and abundance affect bee health through nutrition, immunity, and fitness. In ever-expanding urban landscapes, land use development changes bee habitats and floral resource availability, thus altering the sources of microbes that wild bees need to establish their microbiome. Here, we implement metabarcoding of the bacterial 16S and fungal ITS regions to characterize the diversity and composition of the microbiome in 58 small carpenter bees, Ceratina calcarata, across urban land use gradients (study area 6,425 km2). By categorizing land use development, green space, precipitation, and temperature variables as indicators of habitat across the city, we found that land use variables can predict microbial diversity. Microbial composition was also found to vary across urban land use gradients, with certain microbes such as Acinetobacter and Apilactobacillus overrepresented in less urban locations and Penicillium more abundant in developed areas. Environmental features may also lead to differences in microbe interactions, as co-occurrences between bacteria and fungi varied across percent land use development, exemplified by the correlation between Methylobacterium and Sphingomonas being more prevalent in areas of higher urban development. Surrounding landscapes change the microbial landscape in wild bees and alter the relationships they have with their microbiome. As such, urban centres should consider the impact of growing cities on their pollinators’ health and protect wild bees from the effects of anthropogenic activities.

Microbiome and floral associations of a wild bee using biodiversity survey collections

“…The diverse array of bacterial communities in Ontario included Acinetobacter and Enterobacter, but notably lacked Apilactobacillus (Figure 5A). This is consistent with patterns noted in the small carpenter bee Ceratina calcarata, where the normally ubiquitous Apilactobacillus was present in low relative abundances in Ontario (Nguyen & Rehan, 2022b), despite being previously characterised as a core bacterium and being found in almost all other bees (Graystock et al, 2017;Martinson et al, 2011;Nguyen & Rehan, 2022b, 2023aShell & Rehan, 2022). Martinson et al (2011) similarly found the absence of the bacterial phylotypes associated with the genus Lactobacillus.…”

“…Across all samples, we did not expect any potential impact of ethanol storage or washing on microbiome composition, as Hammer et al (2015) discovered that there were limited effects of surface sterilisation on microbiome characterisations and storage in 95% ethanol when compared to other storage methods. However, Apilactobacillus are found in practically all studied bees (Kwong & Moran, 2016;Martinson et al, 2011;Nguyen & Rehan, 2023a;Shell & Rehan, 2022), playing important roles in building immunity (Daisley et al, 2017; and aiding in host learning and memory behaviour (Zhang et al, 2022). Although potentially correlated to patterns of low relative abundances of Apilactobacillus in urban Ontario (Nguyen & Rehan, 2022b) and in agreement with Martinson et al (2011), which found the absence of Firm-4 and Firm-5 bacterial phylotypes in A. virescens, considerations should be made regarding the effectiveness of certain T A B L E 1 The core microbiome of Agapostemon virescens found at a frequency of at least 1% and detected in at least 50% of the samples, across all provinces and collection methods.…”

“…In comparison, solitary and facultatively social bees gain more of their microbiomes from their environment (Cohen et al, 2022;Dew et al, 2020;Graystock et al, 2017;Keller et al, 2021;McFrederick et al, 2012McFrederick et al, , 2017, bolstering more variable microbiota (Dew et al, 2020;McFrederick et al, 2017;Sookhan et al, 2021). Studies focusing on wild bee microbiomes are currently limited yet remain ongoing (Chau et al, 2023;Cohen et al, 2020;Handy et al, 2022;Kapheim et al, 2021;Nguyen & Rehan, 2023a;Shell & Rehan, 2022). Therefore, characterising the microbial ecology of additional bee species is necessary to compare differences in symbioses underpinning bee health.…”

Integrative population genetics and metagenomics reveals urbanization increases pathogen loads and decreases connectivity in a wild bee

“…For instance, we found that overall bacterial diversity was highest in urban areas which corroborates the findings of a recent study that also found bacterial richness in C. calcarata increased as urbanization increased (Nguyen & Rehan, 2022a). The authors also found that certain core microbiota differed in their abundance depending on urbanization level, such as Apilactobacillus and Acinetobacter core bacteria overabundant in rural sites, but the fungi Penicillium , which plays a role in bee immunity (Yoder et al, 2013), was abundant in urban areas (Nguyen & Rehan, 2022b). Likewise, we also found the change in metagenomic diversity revealed interesting patterns of abundance for core microbiota, such as the core family Lactobacillaceae, which was abundant in sites with high development.…”

Warming up through buildings and roads: what we know and should know about the urban heat island effect on bees

“…Some bee symbionts can survive at temperatures up to 52°C, whereas others are not able to grow below a certain thermal limit (29°C). On the other hand, functionally important bacteria, such as Apilactobacillus, are overrepresented in areas with lower annual temperatures (Nguyen and Rehan, 2022). Moreover, in honeybees there is a seasonal dominance of the non-core bacteria Bartonella, which is associated to dietary shifts caused by low temperatures in winter (Li et al, 2022a).…”