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Host-microbe interactions underlie the development and fitness of many macroorganisms, including bees. Whereas many social bees benefit from vertically transmitted gut bacteria, current data suggests that solitary bees, which comprise the vast majority of species diversity within bees, lack a highly specialized gut microbiome. Here, we examine the composition and abundance of bacteria and fungi throughout the complete life cycle of the ground-nesting solitary bee Anthophora bomboides standfordiana. In contrast to expectations, immature bee stages maintain a distinct core microbiome consisting of Actinobacterial genera (Streptomyces, Nocardiodes) and the fungus Moniliella spathulata. Dormant (diapausing) larval bees hosted the most abundant and distinctive bacteria and fungi, attaining 33 and 52 times their initial copy number, respectively. We tested two adaptive hypotheses regarding microbial functions for diapausing bees. First, using isolated bacteria and fungi, we found that Streptomyces from brood cells inhibited the growth of multiple pathogenic filamentous fungi, suggesting a role in pathogen protection during overwintering, when bees face high pathogen pressure. Second, sugar alcohol composition changed in tandem with major changes in fungal abundance, suggesting links with bee cold tolerance or overwintering biology. We find that A. bomboides hosts a conserved core microbiome that may provide key fitness advantages through larval development and diapause, which raises the question of how this microbiome is maintained and faithfully transmitted between generations. Our results suggest that focus on microbiomes of mature or active insect developmental stages may overlook stage-specific symbionts and microbial fitness contributions during host dormancy.

Abstract: Effectively promoting the stability and quality of ecosystem services involves the successful management of domesticated species and the control of introduced species. In the pollinator literature, interest and concern regarding pollinator species and pollinator health dramatically increased in recent years. Concurrently, the use of loaded terms when discussing domesticated and non-native species may have increased. As a result, pollinator ecology has inherited both the confusion associated with invasion biology’s lack of a standardized terminology to describe native, managed, or introduced species as well as loaded terms with very strong positive or negative connotations. The recent explosion of research on native bees and alternative pollinators, coupled with the use of loaded language, has led to a perceived divide between native bee and managed bee researchers. In comparison, the bird literature discusses the study of managed (poultry) and non-managed (all other birds) species without an apparent conflict with regard to the use of terms with strong connotations or sentiment. Here, we analyze word usage when discussing non-managed and managed bee and bird species in 3614 ecological and evolutionary biology papers published between 1990 and 2019. Using time series analyses, we demonstrate how the use of specific descriptor terms (such as wild, introduced, and exotic) changed over time. We then conducted co-citation network analyses to determine whether papers that share references have similar terminology and sentiment. We predicted a negative language bias towards introduced species and positive language bias towards native species. We found an association between the term invasive and bumble bees and we observed significant increases in the usage of more ambiguous terms to describe non-managed species, such as wild. We detected a negative sentiment associated with the research area of pathogen spillover in bumble bees, which corroborates the subjectivity that language carries. We recommend using terms that acknowledge the role of human activities on pathogen spillover and biological invasions. Avoiding the usage of loaded terms when discussing managed and non-managed species will advance our understanding and promote effective and productive communication across scientists, general public, policy makers and other stake holders in our society.

Pathogens and parasites of solitary bees have been studied for decades, but the microbiome as a whole is poorly understood for most taxa. Comparative analyses of microbiome features such as composition, abundance, and specificity, can shed light on bee ecology and the evolution of host-microbe interactions. Here we study microbiomes of ground-nesting cellophane bees (Colletidae: Diphaglossinae). From a microbial point of view, the diphaglossine genus Ptiloglossa is particularly remarkable: their larval provisions are liquid and smell consistently of fermentation. We sampled larval provisions and various life stages from wild nests of Ptiloglossa arizonensis and two species of closely related genera: Caupolicana yarrowi and Crawfordapis luctuosa. We also sampled nectar collected by P. arizonensis. Using 16S rRNA gene sequencing, we find that larval provisions of all three bee species are near-monocultures of lactobacilli. Nectar communities are more diverse, suggesting ecological filtering. Shotgun metagenomic and phylogenetic data indicate that Ptiloglossa culture multiple species and strains of Apilactobacillus, which circulate among bees and flowers. Larval lactobacilli disappear before pupation, and hence are likely not vertically transmitted, but rather reacquired from flowers as adults. Thus, brood cell microbiomes are qualitatively similar between diphaglossine bees and other solitary bees: lactobacilli-dominated, environmentally acquired, and non-species-specific. However, shotgun metagenomes provide evidence of a shift in bacterial abundance. As compared with several other bee species, Ptiloglossa have much higher ratios of bacterial to plant biomass in larval provisions, matching the unusually fermentative smell of their brood cells. Overall, Ptiloglossa illustrate a path by which hosts can evolve quantitatively novel symbioses: not by acquiring or domesticating novel symbionts, but by altering the microenvironment to favor growth of already widespread and generalist microbes.

Urbanization is associated with increases in impervious land cover, which alters the distribution of resources available to wildlife and concentrates activity in unbuilt spaces such as parks and gardens. How resource shifts alter the dynamics of parasite and pathogen transmission has not been addressed for many important species in urban systems. We focus on urban gardens, resource-rich "islands" within the urban matrix, to examine how the availability of floral resources at local and landscape scales influences the prevalence of six RNA viruses and three parasites in honey bees and bumble bees. Because parasites and pathogens are transmitted at flowers between visitors, we expected that floral abundance would concentrate bees within gardens, amplifying infection rates in pollinators, unless increases in floral resources would enhance bee diversity enough to dilute transmission. We found that garden size and flowering perennial plant abundance had a positive, direct effect on parasite and pathogen richness in bumble bees, suggesting that resource provisioning amplifies transmission. We also found that parasitism rates in honey bees were positively associated with parasites and pathogens in bumble bees, suggesting spillover between species. Encouragingly, we found evidence that management may mitigate parasitism through indirect effects: garden size had a positive impact on bee diversity, which in turn was negatively associated with parasite and pathogen richness in bumble bees. Unexpectedly, we observed that that parasite and pathogen richness in honey bees had no significant predictors, highlighting the complexity of comparing transmission dynamics between species. Although floral resources provide bees with food, we suggest more research on the tradeoffs between resource provisioning and disease transmission to implement conservation plantings in changing landscapes.

Diet and gut microbiomes are intricately linked on both short and long timescales. Changes in diet can alter the microbiome, while microbes in turn allow hosts to access novel diets. Bees are wasps that switched to a vegetarian lifestyle, and the vast majority of bees feed on pollen and nectar. Some stingless bee species, however, also collect carrion, and a few have fully reverted to a necrophagous lifestyle, relying on carrion for protein and forgoing flower visitation altogether. These "vulture" bees belong to the corbiculate apid clade, which is known for its ancient association with a small group of core microbiome phylotypes. Here, we investigate the vulture bee microbiome, along with closely related facultatively necrophagous and obligately pollinivorous species, to understand how these diets interact with microbiome structure. Via deep sequencing of the 16S rRNA gene and subsequent community analyses, we find that vulture bees have lost some core microbes, retained others, and entered into novel associations with acidophilic microbes found in the environment and on carrion. The abundance of acidophilic bacteria suggests that an acidic gut is important for vulture bee nutrition and health, as has been found in other carrion-feeding animals. Facultatively necrophagous bees have more variable microbiomes than strictly pollinivorous bees, suggesting that bee diet may interact with microbiomes on both short and long timescales. Further study of vulture bees promises to provide rich insights into the role of the microbiome in extreme diet switches. IMPORTANCE When asked where to find bees, people often picture fields of wildflowers. While true for almost all species, there is a group of specialized bees, also known as the vulture bees, that instead can be found slicing chunks of meat from carcasses in tropical rainforests. In this study, researchers compared the microbiomes of closely related bees that live in the same region but vary in their dietary lifestyles: some exclusively consume pollen and nectar, others exclusively depend on carrion for their protein, and some consume all of the above. Researchers found that vulture bees lost some ancestral "core" microbes, retained others, and entered into novel associations with acidophilic microbes, which have similarly been found in other carrion-feeding animals such as vultures, these bees' namesake. This research expands our understanding of how diet interacts with microbiomes on both short and long timescales in one of the world's biodiversity hot spots.

Wild bees encounter environmental microbes while foraging. While environmental context affects bee diversity, little is known about it how affects the wild bee microbiome. We used field surveys in 17 urban gardens to examine whether and how variation in local and landscape habitat features shapes the microbiome of the solitary Blue Orchard Bee, Osmia lignaria. We installed O. lignaria cocoons at each site, allowed bees to emerge and forage, then collected them. We measured local features of gardens using vegetation transects and landscape features with GIS. We found that in microbiome composition between bee individuals varied by environmental features such as natural habitat, floral resources, and bee species richness. We also found that environmental features were associated with the abundance of bacterial groups important for bee health, such as Lactobacillus. Our study highlights complex interactions between environment context, bee species diversity, and the bee-associated microbes.

The genus Saccharibacter is currently understudied, with only one described species, Saccharibacter floricola, isolated from a flower. In an effort to better understand the microbes that come in contact with native bee pollinators, we isolated and sequenced four additional strains of Saccharibacter from native bees in the genera Melissodes and Anthophora These genomes range in size from 2,104,494 to 2,316,791 bp (mean, 2,246,664 bp) and contain between 1,860 and 2,167 (mean, 2,060) protein-coding genes.

The honey bee, Apis mellifera, pollinates a wide variety of essential crops in numerous ecosystems around the world but faces many modern challenges. Among these, the microsporidian pathogen Nosema ceranae is one of the primary detriments to honey bee health. Nosema infects the honey bee gut, which harbors a highly specific, coevolved microbiota heavily involved in bee immune function and nutrition. Here, we extend previous work investigating interactions between the honey bee gut microbiome and N. ceranae by studying experimentally infected bees that were returned to their colonies and sampled 5, 10, and 21 days post-infection. We measured Nosema load with quantitative PCR and characterized microbiota with 16S rRNA gene amplicon sequencing. We found significant colony level variation in infection levels, and subtle differences between the microbiota of colonies with high infection levels versus those with low infection levels. Two exact sequence variants of Gilliamella, a core gut symbiont that has previously been associated with gut dysbiosis, were significantly more abundant in bees from colonies with high Nosema loads versus those with low Nosema loads. These bacteria deserve further study to determine if they facilitate more intense infection by Nosema ceranae.

Many countries are utilizing reclaimed wastewater for agriculture because drought, rising temperatures, and expanding human populations are increasing water demands. Unfortunately, wastewater often contains biologically active, pseudopersistent pharmaceuticals, even after treatment. Runoff from farms and output from wastewater treatment plants also contribute high concentrations of pharmaceuticals to the environment. This study assessed the effects of common pharmaceuticals on an agricultural pest, Trichoplusia ni (Lepidoptera: Noctuidae). Larvae were reared on artificial diets spiked with contaminants of emerging concern (CECs) at environmentally relevant concentrations. Trichoplusia ni showed increased developmental time and mortality when reared on artificial diets containing antibiotics, hormones, or a mixture of contaminants. Mortality was also increased when T. ni were reared on tomatoes grown hydroponically with the same concentrations of antibiotics. The antibiotic-treated plants translocated ciprofloxacin through their tissues to roots, shoots, and leaves. Microbial communities of T. ni changed substantially between developmental stages and when exposed to CECs in their diets. Our results suggest that use of reclaimed wastewater for irrigation of crops can affect the developmental biology and microbial communities of an insect of agricultural importance.

Drought, rising temperatures, and expanding human populations are increasing water demands. Many countries are extending potable water supplies by irrigating crops with wastewater. Unfortunately, wastewater contains biologically active, long-lived pharmaceuticals, even after treatment. Run-off from farms and wastewater treatment plant overflows contribute high concentrations of pharmaceuticals to the environment. This study assessed the effects of common pharmaceuticals on a cosmopolitan saprophagous insect, Megaselia scalaris (Diptera: Phoridae). Larvae were reared on artificial diets spiked with contaminants of emerging concern (CECs) at environmentally relevant concentrations. Female flies showed no oviposition preference for treated or untreated diets. Larvae exposed to caffeine in diets showed increased mortality, and larvae fed antibiotics and hormones showed signs of slowed development, especially in females. The normal sex ratio observed in M. scalaris from control diets was affected by exposure to caffeine and pharmaceutical mixture treatments. There was an overall effect of treatment on the flies' microbial communities; notably, caffeine fed insects displayed higher microbial variability. Eight bacterial families accounted for approximately 95% of the total microbes in diet and insects. Our results suggest that CECs at environmentally relevant concentrations can affect the biology and microbial communities of an insect of ecological and medical importance.

For most animals, the microbiome is key for nutrition and pathogen defence, and is often shaped by diet. Corbiculate bees, including honey bees, bumble bees, and stingless bees, share a core microbiome that has been shaped, at least in part, by the challenges associated with pollen digestion. However, three species of stingless bees deviate from the general rule of bees obtaining their protein exclusively from pollen (obligate pollinivores) and instead consume carrion as their sole protein source (obligate necrophages) or consume both pollen and carrion (facultative necrophages). These three life histories can provide missing insights into microbiome evolution associated with extreme dietary transitions. Here, we investigate, via shotgun metagenomics, the functionality of the microbiome across three bee diet types: obligate pollinivory, obligate necrophagy, and facultative necrophagy. We find distinct differences in microbiome composition and gene functional profiles between the diet types. Obligate necrophages and pollinivores have more specialized microbes, whereas facultative necrophages have a diversity of environmental microbes associated with several dietary niches. Our study suggests that necrophagous bee microbiomes may have evolved to overcome cellular stress and microbial competition associated with carrion. We hypothesize that the microbiome evolved social phenotypes, such as biofilms, that protect the bees from opportunistic pathogens present on carcasses, allowing them to overcome novel nutritional challenges. Whether specific microbes enabled diet shifts or diet shifts occurred first and microbial evolution followed requires further research to disentangle. Nonetheless, we find that necrophagous microbiomes, vertebrate and invertebrate alike, have functional commonalities regardless of their taxonomy. [ABSTRACT FROM AUTHOR]

Land-use change and intensification threaten bee populations worldwide, imperilling pollination services. Global models are needed to better characterise, project, and mitigate bees' responses to these human impacts. The available data are, however, geographically and taxonomically unrepresentative; most data are from North America and Western Europe, overrepresenting bumblebees and raising concerns that model results may not be generalizable to other regions and taxa. To assess whether the geographic and taxonomic biases of data could undermine effectiveness of models for conservation policy, we have collated from the published literature a global dataset of bee diversity at sites facing land-use change and intensification, and assess whether bee responses to these pressures vary across 11 regions (Western, Northern, Eastern and Southern Europe; North, Central and South America; Australia and New Zealand; South East Asia; Middle and Southern Africa) and between bumblebees and other bees. Our analyses highlight strong regionally-based responses of total abundance, species richness and Simpson's diversity to land use, caused by variation in the sensitivity of species and potentially in the nature of threats. These results suggest that global extrapolation of models based on geographically and taxonomically restricted data may underestimate the true uncertainty, increasing the risk of ecological surprises.

The honey bee hive environment contains a rich microbial community that differs according to niche. Acetobacteraceae Alpha 2.2 (Alpha 2.2) bacteria are present in the food stores, the forager crop, and larvae but at negligible levels in the nurse and forager midgut and hindgut. We first sought to determine the source of Alpha 2.2 in young larvae by assaying the diversity of microbes in nurse crops, hypopharyngeal glands (HGs), and royal jelly (RJ). Amplicon-based pyrosequencing showed that Alpha 2.2 bacteria occupy each of these environments along with a variety of other bacteria, including Lactobacillus kunkeei. RJ and the crop contained fewer bacteria than the HGs, suggesting that these tissues are rather selective environments. Phylogenetic analyses showed that honey bee-derived Alpha 2.2 bacteria are specific to bees that "nurse" the hive's developing brood with HG secretions and are distinct from the Saccharibacter-type bacteria found in bees that provision their young differently, such as with a pollen ball coated in crop-derived contents. Acetobacteraceae can form symbiotic relationships with insects, so we next tested whether Alpha 2.2 increased larval fitness. We cultured 44 Alpha 2.2 strains from young larvae that grouped into nine distinct clades. Three isolates from these nine clades flourished in royal jelly, and one isolate increased larval survival in vitro. We conclude that Alpha 2.2 bacteria are not gut bacteria but are prolific in the crop-HG-RJ-larva niche, passed to the developing brood through nurse worker feeding behavior. We propose the name Parasaccharibacter apium for this bacterial symbiont of bees in the genus Apis.