Honey Bee Colony Mortality Research Articles

Infectious diseases of bees and their impact on the vital activity and honey productivity of honey bee colonies in Ukraine

The article presents the results of the study of the mass mortality of honey bee colonies in different apiaries from different regions of Ukraine. The epizootic status of 102 honey bee colonies was studied and 607 samples of pathological material were analyzed in 2021–2023. According to the results of the monitoring of the epizootic situation in Ukrainian beekeeping it was found that the share of parasitic diseases (54.4%, 74.0%, 69.3%) constantly prevails over infectious diseases. It was noted that the incidence of varroosis in honey bees (34.4%, 71.4%, 41.47%) remains the highest among other diseases. Against the background of severe damage to honey bee colonies by the Varroa mite, infectious diseases began to appear in an atypical form, which significantly complicates their differential diagnosis. A probable increase in the incidence of nosemosis in adult bees and the detection of Nosema cysts in the intestines of bees, both in spring and summer, and the detection of cysts in honey indicate the spread of another pathogen, Nosema cerana, which causes nosemosis in the summer season. The reason for the periodic mass death of bees in Ukraine is the combination of a high number of parasitic Varroa mites in the honey bee colony with the presence of bee infection with microsporidia Nosema spp. These pathogens negatively affect the immunity of the honey bee colony, and cause exacerbation of latent infections in bees, which leads to a decrease in the number of honey bee colonies, weakening their viability and reducing the quality of honey products

Bridging the buzz: In vivo EPR imaging unlocking the secrets of honey bee health.

Honey bees play a pivotal role in shaping ecosystems and sustaining human health as both pollinators and producers of health-promoting products. However, honey bee colony mortality is on the rise globally, driven by various factors, including parasites, pesticides, habitat loss, poor nutrition, and climate change. This has far-reaching consequences for the environment, economy, and human welfare. While efforts to address these issues are underway, the current progress in electron paramagnetic resonance (EPR) instrumentation affords using the immense potential of this magnetic resonance technique to study small samples such as honey bees. This paper presents the pioneering 2D in vivo EPR imaging experiment on a honey bee, revealing the ongoing redox-status of bees' intestines. This way, by monitoring the spatio-temporal changes of the redox-active spin-probes' EPR signal, it is possible to gain access to valuable information on the course of ongoing bees' pathologies and the prospect of following-up on the efficiency of applied therapies. Employing a selection of diverse spin-probes could further reveal pH levels and oxygen concentrations in bee tissues, allowing a noninvasive assessment of bee physiology. This approach offers promising strategies for safeguarding pollinators and understanding their biology, fostering their well-being and ecological harmony.

Unveiling beekeepers’ use and preference of precision apiculture systems

Amid growing ecological concerns surrounding honey bee colony mortality, Precision Apiculture Systems (PAS) emerge as promising monitoring tools to safeguard bee health as well as to improve the beekeeping practices and economic sustainability of apiary operations. These systems offer critical insights into colony dynamics, aiding decision-making processes in beekeeping. Despite a surge in relevant academic research, knowledge of actual PAS usage and preference among beekeepers remains limited. To fill this gap, a standardized survey was conducted among beekeepers in France, Germany, and Greece. This focused geographical scope survey aimed to determine the extent of current and potential PAS adoption, the motivations behind usage or avoidance, and ascertain future preferences. Among the 538 respondents, 45% reported utilizing some form of PAS, with beekeeping scales being the most commonly used. The study revealed that the use of PAS positively correlates with both the number of hives managed and the distance of the apiary from the beekeeper’s residence. Overall, 90% of respondents expressed a certain degree of satisfaction with their use of PAS, although the high costs of these tools were identified as a primary obstacle to broader adoption. About 48% of the beekeepers preferred systems with external sensors, highlighting a clear demand for non-invasive health-related colony information. The advantages that foster PAS usage include decision-making support and improved efficiency in monitoring colony growth and honey productivity. These findings can assist in making PAS more accessible to beekeepers, with the aim to enhance colony performance and decision-making capabilities, thus addressing honey bee colony mortality.

Indirect exposure to insect growth disruptors affects honey bee (Apis mellifera) reproductive behaviors and ovarian protein expression.

Pesticide exposure and queen loss are considered to be major causes of honey bee colony mortality, yet little is known regarding the effects of regularly encountered agrochemicals on honey bee reproduction. Here, we present the results of a two-generational study using specialized cages to expose queens to commonly used insect growth disrupting pesticides (IGDs) via their retinue of worker bees. Under IGD exposure, we tracked queen performance and worker responses to queens, then the performance of the exposed queens' offspring was assessed to identify patterns that may contribute to the long-term health and stability of a social insect colony. The positive control, novaluron, resulted in deformed larvae hatching from eggs laid by exposed queens, and methoxyfenozide, diflubenzuron, and novaluron caused a slight decrease in daily egg laying rates, but this was not reflected in the total egg production over the course of the experiment. Curiously, eggs laid by queens exposed to pyriproxyfen exhibited increased hatching rates, and those larvae developed into worker progeny with increased responsiveness to their queens. Additionally, pyriproxyfen and novaluron exposure affected the queen ovarian protein expression, with the overwhelming majority of differentially expressed proteins coming from the pyriproxyfen exposure. We discuss these results and the potential implications for honey bee reproduction and colony health.

Potassium ion channels as a molecular target to reduce virus infection and mortality of honey bee colonies

Declines in managed honey bee populations are multifactorial but closely associated with reduced virus immunocompetence and thus, mechanisms to enhance immune function are likely to reduce viral infection rates and increase colony viability. However, gaps in knowledge regarding physiological mechanisms or ‘druggable’ target sites to enhance bee immunocompetence has prevented therapeutics development to reduce virus infection. Our data bridge this knowledge gap by identifying ATP-sensitive inward rectifier potassium (KATP) channels as a pharmacologically tractable target for reducing virus-mediated mortality and viral replication in bees, as well as increasing an aspect of colony-level immunity. Bees infected with Israeli acute paralysis virus and provided KATP channel activators had similar mortality rates as uninfected bees. Furthermore, we show that generation of reactive oxygen species (ROS) and regulation of ROS concentrations through pharmacological activation of KATP channels can stimulate antiviral responses, highlighting a functional framework for physiological regulation of the bee immune system. Next, we tested the influence of pharmacological activation of KATP channels on infection of 6 viruses at the colony level in the field. Data strongly support that KATP channels are a field-relevant target site as colonies treated with pinacidil, a KATP channel activator, had reduced titers of seven bee-relevant viruses by up to 75-fold and reduced them to levels comparable to non-inoculated colonies. Together, these data indicate a functional linkage between KATP channels, ROS, and antiviral defense mechanisms in bees and define a toxicologically relevant pathway that can be used for novel therapeutics development to enhance bee health and colony sustainability in the field.

First identification of Tyrophagus curvipenis (Acari: Acaridae) and pathogen detection in Apis mellifera colonies in the Republic of Korea

Mites of the genus Tyrophagus (Acari: Acaridae) are among the most widely distributed mites. The species in this genus cause damage to stored products and crops, and pose a threat to human health. However, the influence of Tyrophagus spp. in apiculture remains unknown. In 2022, a study focusing on the identification of Tyrophagus species within five apiaries was conducted in Chungcheongnam Province, Republic of Korea. Its specific objective was to investigate the presence of Tyrophagus mites in response to the reported high mortality of honey bee colonies in this area. Morphological identification and phylogenetic analysis using the mitochondrial gene cytochrome-c oxidase subunit 1 (CO1) confirmed for the first time the presence of the mite species Tyrophagus curvipenis in a honey bee colony in the Republic of Korea. Two honey bee pathogens were detected in the mite, a viral pathogen (deformed wing virus, DWV) and a protozoal pathogen (Trypanosoma spp.). The presence of the two honey bee pathogens in the mite suggests that this mite could contribute to the spread of related honey bee diseases. However, the direct influence of the mite T. curvipenis on honey bee health remains unknown and should be further investigated.

Winter mortality, diversification, and self-sufficiency affect honey bee (Hymenoptera: Apidae) colony profit in Canada: a model of commercial Alberta beekeepers.

Canadian beekeepers faced widespread levels of high honey bee colony mortality over the winter of 2021/2022, with an average winter loss of 45%. To understand the economic impact of winter colony mortality in Canada and the beekeeping management strategies used to mitigate these losses, we develop a profit model of commercial beekeeping operations in Alberta, Canada. Our model shows that for operations engaging in commercial pollination as well as honey production (compared to honey production alone), per colony profit is higher and operations are better able to withstand fluctuations in exogenous variables such as prices and environmental factors affecting productivity including winter mortality rates. The results also suggest that beekeeping operations that replace winter colony losses with splits instead of package bees accrue higher per colony profit than those importing packages to replace losses. Further, operations that produce their own queens to use in their replacement splits, accrue even higher profit. Our results demonstrate that the profitability of beekeeping operations is dependent on several factors including winter mortality rates, colony replacement strategies, and the diversification of revenue sources. Beekeepers who are not as susceptible to price and risk fluctuations in international markets and imported bee risks accrue more consistently positive profits.

STUDY OF BEE MORTALITY IN BULGARIA DURING THE WINTER PERIOD OF 2022/2023

The purpose of the study is to investigate and define the main reasons involved in the winter mortality of honeybee colonies during the last winter season of 2022/2023 in Bulgaria. In the survey were included 94 respondents that have reported mortality The mortality rate for farms with up to 50 bee colonies is 31%, for those with 50-150 bee colonies it is 19.27%, and for the largest bee farms that are with over 150 bee colonies, it is 19.9%. Cumulative mortality in the mortality of bee colonies is 29.66% - 1937 bee colonies died from total of 6530 in winter period of 2022/2023. The study identifies several factors such as Varroasis, insufficient nutritional substrate, unfavorable climatic changes, pesticides use, queen bee problems and others.

Using the Honey Bee (Apis mellifera L.) Cell Line AmE-711 to Evaluate Insecticide Toxicity.

One of the main contributors to poor productivity and elevated mortality of honey bee colonies globally is insecticide exposure. Whole-organism and colony-level studies have demonstrated the effects of insecticides on many aspects of honey bee biology and have also shown their interactions with pathogens. However, there is a need for in vitro studies using cell lines to provide greater illumination of the effects of insecticides on honey bee cellular and molecular processes. We used a continuous cell line established from honey bee embryonic tissues (AmE-711) in assays that enabled assessment of cell viability in response to insecticide exposure. We exposed AmE-711 cells to four formulations, each containing a different insecticide. Treatment of cells with the insecticides resulted in a concentration-dependent reduction in viability after a 24-h exposure, whereas long-term exposure (120 h) to sublethal concentrations had limited effects on viability. The 24-h exposure data allowed us to predict the half-maximal lethal concentration (LC50) for each insecticide using a four-parameter logistical model. We then exposed cells for 12 h to the predicted LC50 and observed changes in morphology that would indicate stress and death. Reverse transcription-quantitative polymerase chain reaction analysis corroborated changes in morphology: expression of a cellular stress response gene, 410087a, increased after an 18-h exposure to the predicted LC50. Demonstration of the effects of insecticides through use of AmE-711 provides a foundation for additional research addressing issues specific to honey bee toxicology and complements whole-organism and colony-level approaches. Moreover, advances in the use of AmE-711 in high-throughput screening and in-depth analysis of cell regulatory networks will promote the discovery of novel control agents with decreased negative impacts on honey bees. Environ Toxicol Chem 2023;42:88-99. Published 2022. This article is a U.S. Government work and is in the public domain in the USA. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

An Insight Into the microRNA Profile of the Ectoparasitic Mite Varroa destructor (Acari: Varroidae), the Primary Vector of Honey Bee Deformed Wing Virus.

The remarkably adaptive mite Varroa destructor is the most important honey bee ectoparasite. Varroa mites are competent vectors of deformed wing virus (DWV), and the Varroa-virus complex is a major determinant of annual honey bee colony mortality and collapse. MicroRNAs (miRNAs) are 22-24 nucleotide non-coding RNAs produced by all plants and animals and some viruses that influence biological processes through post-transcriptional regulation of gene expression. Knowledge of miRNAs and their function in mite biology remains limited. Here we constructed small RNA libraries from male and female V. destructor using Illumina’s small RNA-Seq platform. A total of 101,913,208 and 91,904,732 small RNA reads (>18 nucleotides) from male and female mites were analyzed using the miRDeep2 algorithm. A conservative approach predicted 306 miRNAs, 18 of which were upregulated and 13 downregulated in female V. destructor compared with males. Quantitative real-time PCR validated the expression of selected differentially-expressed female Varroa miRNAs. This dataset provides a list of potential miRNA targets involved in regulating vital Varroa biological processes and paves the way for developing strategies to target Varroa and their viruses.

Screening of Honey Bee Pathogens in the Czech Republic and Their Prevalence in Various Habitats.

Simple SummaryWorldwide, mass losses of honey bee colonies are being observed more frequently in recent times. Except for the overuse of pesticides, one of the main reasons for high honey bee colony collapse is diseases. For this reason, nationwide screening of common pathogens involving viruses, bacterial, fungal, and protozoa pathogens was performed in three different types of habitat including agroecosystems, towns, and national parks. The most frequent eukaryotic pathogens were Trypanosomatids and N. ceranae and in the case of viruses DWV-A and ABPV. In addition, the association between the occurrence of particular pathogens and winter colony losses was found. Although the differences in mortality between individual habitats were not significant, results of this study suggest a significant correlation between DWV-B and DWC-C occurrence and mortality of bee colonies, despite their relatively low occurrence.Western honey bee (Apis mellifera) is one of the most important pollinators in the world. Thus, a recent honey bee health decline and frequent honey bee mass losses have drawn attention and concern. Honey bee fitness is primarily reduced by pathogens, parasites, and viral load, exposure to pesticides and their residues, and inadequate nutrition from both the quality and amount of food resources. This study evaluated the prevalence of the most common honey bee pathogens and viruses in different habitats across the Czech Republic. The agroecosystems, urban ecosystems, and national park were chosen for sampling from 250 colonies in 50 apiaries. Surprisingly, the most prevalent honey bee pathogens belong to the family Trypanosomatidae including Lotmaria passim and Crithidia mellificae. As expected, the most prevalent viruses were DWV, followed by ABPV. Additionally, the occurrence of DWV-B and DWV-C were correlated with honey bee colony mortality. From the habitat point of view, most pathogens occurred in the town habitat, less in the agroecosystem and least in the national park. The opposite trend was observed in the occurrence of viruses. However, the prevalence of viruses was not affected by habitat.

Accelerated Varroa destructor population growth in honey bee (Apis mellifera) colonies is associated with visitation from non-natal bees

A leading cause of managed honey bee colony mortality in the US, Varroa destructor populations typically exceed damaging levels in the fall. One explanation for rapid population increases is migration of mite carrying bees between colonies. Here, the degree to which bees from high and low mite donor colonies move between apiaries, and the effect visitation has on Varroa populations was monitored. More bees from low mite colonies (n = 37) were detected in receiver apiaries than bees from high mite colonies (n = 10, p < 0.001). Receiver colony Varroa population growth was associated with visitation by non-natal bees (p = 0.03), but not high mite bees alone (p = 0.19). Finally, colonies lacking robbing screens experienced faster Varroa population growth than screened neighbors (p = 0.01). Results indicate visiting non-natal bees may vector mites to receiver colonies. These results do not support the current two leading theories regarding mite immigration – the “mite bomb” theory (bees from high mite colonies emigrating to collapsing colonies), or the “robbing” theory (natal robbing bees return home with mites from collapsing colonies). Potential host-parasite effects to bee behavior, as well as important management implications both for Varroa treatment regimens and breeding Varroa resistant bees are discussed.

Varroa destructor infestation impairs the improvement of landing performance in foraging honeybees.

The parasitic mite Varroa destructor is an important contributor to the high losses of western honeybees. Forager bees from Varroa-infested colonies show reduced homing and flight capacity; it is not known whether flight manoeuvrability and related learning capability are also affected. Here, we test how honeybees from Varroa-infested and control colonies fly in an environment that is unfamiliar at the beginning of each experimental day. Using stereoscopic high-speed videography, we analysed 555 landing manoeuvres recorded during 12 days of approximately 5 h in length. From this, we quantified landing success as percentage of successful landings, and assessed how this changed over time. We found that the forager workforce of Varroa-infested colonies did not improve their landing success over time, while for control bees landing success improved with approximately 10% each hour. Analysis of the landing trajectories showed that control bees improved landing success by increasing the ratio between in-flight aerodynamic braking and braking at impact on the landing platform; bees from Varroa-infested colonies did not increase this ratio over time. The Varroa-induced detriment to this landing skill-learning capability might limit forager bees from Varroa-infested colonies to adapt to new or challenging conditions; this might consequently contribute to Varroa-induced mortality of honeybee colonies.

A National Survey of Managed Honey Bee Colony Winter Losses (Apis mellifera) in China (2013–2017)

Surveys of managed honey bee colony losses worldwide have become fundamental for engineering a sustainable and systematic approach to protect honey bees. Though China is a member of the world’s apiculture superpowers, the investigation of honey bee colony losses from Chinese government was not formally launched until recently. In this study, we investigated the colony winter losses of the western honey bee (Apis mellifera) of four consecutive years in 2013–2017 from 19 provinces in China, with a total of 2387 responding Chinese beekeepers (195 hobby beekeepers, 1789 side-line beekeepers, 403 commercial beekeepers) providing the records of overwintering mortality of honey bee colonies. The calculated colony losses were 8.7%, a relatively low mortality below the world average. There still exist considerable variations in total losses among provinces (ranging from 0.9% to 22.0%), years (ranging from 8.1% to 10.6%) and scales of apiaries (ranging from 7.5% to 10.0%). Furthermore, we deeply analyzed and estimated the effects of potential risk factors on the colonies’ winter losses, and speculated that the queen problems, the operation sizes and proportion of new queens are leading causes of the high honey bee colony mortality in China. More research and advanced technical methods are still required for correlation analysis and verification in future surveys of managed honey bee colony winter losses.

Identification of a novel host protein interacting with the structural protein VP2 of deformed wing virus by yeast two-hybrid screening

Deformed wing virus (DWV) interacting with Varroa destructor is a possible cause of honeybee colony mortality. VP2 is the structural protein of DWV but its function remains unknown. To clarify the function of VP2 and screen for novel binding proteins that interact with VP2, we carried out a membrane protein yeast two-hybrid screening using VP2 as bait. Subsequently, the interaction between VP2 and the host interacting protein [heat shock protein 10 (Hsp10)] was further verified using glutathione S-transferase pull-down assay in vitro and co-immunoprecipitation assay in cells. Furthermore, fluorescence confocal microscopy revealed that VP2 and Hsp10 were mainly co-localized in the cytoplasm. Using real-time polymerase chain reaction, we found that Hsp10 expression in DWV-infected worker honey bees were downregulated compared with that in healthy honey bees. Additionally, we showed that overexpression of VP2 protein could reduce the expression of Hsp10. These results suggest that Hsp10 plays a vital role in host immunity and antiviral effects.

Effect of Oral Administration of 1,3-1,6 β-Glucans in DWV Naturally Infected Newly Emerged Bees (Apis mellifera L.).

Honeybee pathogens have an important role in honeybee colony mortality and colony losses; most of them are widely spread and necessitate worldwide solutions to contrast honeybee’s decline. Possible accepted solutions to cope with the spread of honeybee’s pathogens are focused on the study of experimental protocols to enhance the insect’s immune defenses. Honeybee’s artificial diet capable to stimulate the immune system is a promising field of investigation as ascertained by the introduction of 1,3-1,6 β-glucans as a dietary supplement. In this work, by collecting faecal samples of honeybees exposed to different dietary conditions of 1,3-1,6 β-glucans (0.5% and 2% w/w), it has been possible to investigate the Deformed wing virus (DWV) viral load kinetic without harming the insects. Virological data obtained by a one-step TaqMan RT-PCR highlighted the ability of 1,3-1,6 β-glucans to reduce the viral load at the 24th day of rearing. The results indicated that the diet supplemented with 1,3-1,6 β-glucans was associated with a dose-dependent activation of phenoloxidase. The control group showed a higher survival rate than the experimental groups. This research confirmed 1,3-1,6 β-glucans as molecules able to modulate honeybees’ defense pathways, and this is the first report in which the kinetic of DWV infection in honeybee faeces has been monitored by a RT-qPCR.

Comparison of apiculture and winter mortality of honey bee colonies (Apis mellifera) in Austria and Czechia

Honey bees are the most important managed pollinators and provide income because of bee products. In Austria and Czechia, we monitored winter losses of honey bee colonies and also collected information on the apicultural sector, hive management, population dynamics and treatment against the mite Varroa destructor from 2013–14 to 2016–17. Numbers of beekeepers and colonies, colony density and percentage of beekeepers in human population are higher in Czechia than in Austria. Winter loss rates of honey bee colonies ranged from 8.1% to 28.4% in Austria and 6.4% to 19.4% in Czechia, with significantly higher loss rates in all 4 investigated winters in Austria. The portion of colonies lost because of living colonies with unsolvable queen problems ranged from 3.6 to 4.4% in Austria and from 2.2 to 3.0% in Czechia. Despite of colony losses during winter, colony production in summer allows for compensation or even expansion of colony populations in both countries. We identified differences between the two countries in the treatments applied by beekeepers against the parasitic varroa mite. In Austria, organic acids are most commonly used, whereas the application of synthetic acaricides is widely spread in Czechia. Our study points at the better understanding of apiculture and the importance of international comparisons to facilitate our knowledge on honey bee colony losses.

Is the Brood Pattern within a Honey Bee Colony a Reliable Indicator of Queen Quality?

Failure of the queen is often identified as a leading cause of honey bee colony mortality. However, the factors that can contribute to “queen failure” are poorly defined and often misunderstood. We studied one specific sign attributed to queen failure: poor brood pattern. In 2016 and 2017, we identified pairs of colonies with “good” and “poor” brood patterns in commercial beekeeping operations and used standard metrics to assess queen and colony health. We found no queen quality measures reliably associated with poor-brood colonies. In the second year (2017), we exchanged queens between colony pairs (n = 21): a queen from a poor-brood colony was introduced into a good-brood colony and vice versa. We observed that brood patterns of queens originally from poor-brood colonies significantly improved after placement into a good-brood colony after 21 days, suggesting factors other than the queen contributed to brood pattern. Our study challenges the notion that brood pattern alone is sufficient to judge queen quality. Our results emphasize the challenges in determining the root source for problems related to the queen when assessing honey bee colony health.

Bee colony health indicators: synthesis and future directions.

Abstract The western honey bee Apis melifera plays an important role in human well-being by producing honey, sustaining populations of wild plants and supporting human-dependant crop production. Unfortunately, abnormal high-mortality rates of colonies have been revealed all over the world. This paper reviews the stress factors that are likely involved in the cause of honey bee poor health, the mechanisms underlying bee health and survival and the different early warning indicators of bee colony mortality. Honey bee colonies can be assimilated to a complex system for which survival depends on its individual quality, its adaptive capacity and its threshold of resilience to pressures. Many stress factors are likely involved, by interaction, in the cause of honey bee colony mortality. Three main groups of stressors are highlighted to affect the colony survival, including (i) environmental pressures such as lack of flowers and pesticide exposure, (ii) biotic pressures such as parasites and pathogens and (iii) beekeeping management such as the use of chemical treatments. Routine monitoring of colonies provides robust approaches to assess the health status of honey bees. By tracking specific colony parameters such as queen performance, colony dynamics, in-hive products and the prevalence of pathogens, beekeepers can establish a health status of the colony. By comparing this field-based health status with model-based predictions, a new area is emerging towards the detection of early warning indicators of colony mortality.

Glyphosate perturbs the gut microbiota of honey bees.

Glyphosate, the primary herbicide used globally for weed control, targets the 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) enzyme in the shikimate pathway found in plants and some microorganisms. Thus, glyphosate may affect bacterial symbionts of animals living near agricultural sites, including pollinators such as bees. The honey bee gut microbiota is dominated by eight bacterial species that promote weight gain and reduce pathogen susceptibility. The gene encoding EPSPS is present in almost all sequenced genomes of bee gut bacteria, indicating that they are potentially susceptible to glyphosate. We demonstrated that the relative and absolute abundances of dominant gut microbiota species are decreased in bees exposed to glyphosate at concentrations documented in the environment. Glyphosate exposure of young workers increased mortality of bees subsequently exposed to the opportunistic pathogen Serratia marcescens Members of the bee gut microbiota varied in susceptibility to glyphosate, largely corresponding to whether they possessed an EPSPS of class I (sensitive to glyphosate) or class II (insensitive to glyphosate). This basis for differences in sensitivity was confirmed using in vitro experiments in which the EPSPS gene from bee gut bacteria was cloned into Escherichia coli All strains of the core bee gut species, Snodgrassella alvi, encode a sensitive class I EPSPS, and reduction in S. alvi levels was a consistent experimental result. However, some S. alvi strains appear to possess an alternative mechanism of glyphosate resistance. Thus, exposure of bees to glyphosate can perturb their beneficial gut microbiota, potentially affecting bee health and their effectiveness as pollinators.