Bridging the Gap between Field Experiments and Machine Learning: The EC H2020 B-GOOD Project as a Case Study towards Automated Predictive Health Monitoring of Honey Bee Colonies.

Honey bee colonies have great societal and economic importance. The main challenge that beekeepers face is keeping bee colonies healthy under ever-changing environmental conditions. In the past two decades, beekeepers that manage colonies of Western honey bees (Apis mellifera) have become increasingly concerned by the presence of parasites and pathogens affecting the bees, the reduction in pollen and nectar availability, and the colonies' exposure to pesticides, among others. Hence, beekeepers need to know the health condition of their colonies and how to keep them alive and thriving, which creates a need for a new holistic data collection method to harmonize the flow of information from various sources that can be linked at the colony level for different health determinants, such as bee colony, environmental, socioeconomic, and genetic statuses. For this purpose, we have developed and implemented the B-GOOD (Giving Beekeeping Guidance by computational-assisted Decision Making) project as a case study to categorize the colony's health condition and find a Health Status Index (HSI). Using a 3-tier setup guided by work plans and standardized protocols, we have collected data from inside the colonies (amount of brood, disease load, honey harvest, etc.) and from their environment (floral resource availability). Most of the project's data was automatically collected by the BEEP Base Sensor System. This continuous stream of data served as the basis to determine and validate an algorithm to calculate the HSI using machine learning. In this article, we share our insights on this holistic methodology and also highlight the importance of using a standardized data language to increase the compatibility between different current and future studies. We argue that the combined management of big data will be an essential building block in the development of targeted guidance for beekeepers and for the future of sustainable beekeeping.

Experimental cross species transmission of a major viral pathogen in bees is predominantly from honeybees to bumblebees.

Cross-species transmission of a pathogen from a reservoir to a recipient host species, spillover, can have major impacts on biodiversity, domestic species and human health. Deformed wing virus (DWV) is a panzootic RNA virus in honeybees that is causal in their elevated colony losses, and several correlative field studies have suggested spillover of DWV from managed honeybees to wild bee species such as bumblebees. Yet unequivocal demonstration of DWV spillover is lacking, while spillback, the transmission of DWV from a recipient back to the reservoir host, is rarely considered. Here, we show in fully crossed laboratory experiments that the transmission of DWV (genotype A) from honeybees to bumblebees occurs readily, yet we neither detected viral transmission from bumblebees to honeybees nor onward transmission from experimentally infected to uninoculated bumblebees. Our results support the potential for viral spillover from honeybees to other bee species in the field when robbing resources from heterospecific nests or when visiting the same flowers. They also underscore the importance of studies on the virulence of DWV in wild bee species so as to evaluate viral impact on individual and population fitness as well as viral adaption to new host species.

The Gut Microbiota Can Provide Viral Tolerance in the Honey Bee.

Adult honey bees host a remarkably consistent gut microbial community that is thought to benefit host health and provide protection against parasites and pathogens. Currently, however, we lack experimental evidence for the causal role of the gut microbiota in protecting the Western honey bees (Apis mellifera) against their viral pathogens. Here we set out to fill this knowledge gap by investigating how the gut microbiota modulates the virulence of a major honey bee viral pathogen, deformed wing virus (DWV). We found that, upon oral virus exposure, honey bee survival was significantly increased in bees with an experimentally established normal gut microbiota compared to control bees with a perturbed (dysbiotic) gut microbiota. Interestingly, viral titers were similar in bees with normal gut microbiota and dysbiotic bees, pointing to higher viral tolerance in bees with normal gut microbiota. Taken together, our results provide evidence for a positive role of the gut microbiota for honey bee fitness upon viral infection. We hypothesize that environmental stressors altering honey bee gut microbiota composition, e.g., antibiotics in beekeeping or pesticides in modern agriculture, could interact synergistically with pathogens, leading to negative effects on honey bee health and the epidemiology and impact of their viruses.

Experimental infection of bumblebees with honeybee-associated viruses: no direct fitness costs but potential future threats to novel wild bee hosts.

Pathogen spillover represents an important cause of biodiversity decline. For wild bee species such as bumblebees, many of which are in decline, correlational data point towards viral spillover from managed honeybees as a potential cause. Yet, impacts of these viruses on wild bees are rarely evaluated. Here, in a series of highly controlled laboratory infection assays with well-characterized viral inocula, we show that three viral types isolated from honeybees (deformed wing virus genotype A, deformed wing virus genotype B and black queen cell virus) readily replicate within hosts of the bumblebee Bombus terrestris. Impacts of these honeybee-derived viruses - either injected or fed - on the mortality of B. terrestris workers were, however, negligible and probably dependent on host condition. Our results highlight the potential threat of viral spillover from honeybees to novel wild bee species, though they also underscore the importance of additional studies on this and other wild bee species under field-realistic conditions to evaluate whether pathogen spillover has a negative impact on wild bee individuals and population fitness.

The Two Prevalent Genotypes of an Emerging Infectious Disease, Deformed Wing Virus, Cause Equally Low Pupal Mortality and Equally High Wing Deformities in Host Honey Bees.

Deformed wing virus (DWV) is an emerging infectious disease of the honey bee (Apis mellifera) that is considered a major cause of elevated losses of honey bee colonies. DWV comprises two widespread genotypes: the originally described genotype A, and genotype B. In adult honey bees, DWV-B has been shown to be more virulent than DWV-A. However, their comparative effects on earlier host developmental stages are unknown. Here, we experimentally inoculated honey bee pupae and tested for the relative impact of DWV-A versus DWV-B on mortality and wing deformities in eclosing adults. DWV-A and DWV-B caused similar, and only slightly elevated, pupal mortality (mean 18% greater mortality than control). Both genotypes caused similarly high wing deformities in eclosing adults (mean 60% greater wing deformities than control). Viral titer was high in all of the experimentally inoculated eclosing adults, and was independent of wing deformities, suggesting that the phenotype 'deformed wings' is not directly related to viral titer or viral genotype. These viral traits favor the emergence of both genotypes of DWV by not limiting the reproduction of its vector, the ectoparasitic Varroa destructor mite, in infected pupae, and thereby facilitating the spread of DWV in honey bees infested by the mite.

Impact of managed honey bee viruses on wild bees.

Several viruses found in the Western honey bee (Apis mellifera) have recently been detected in other bee species, raising the possibility of spill-over from managed to wild bee species. Alternatively, these viruses may be shared generalists across flower-visiting insects. Here we explore the former hypothesis, pointing out weaknesses in the current evidence, particularly in relation to deformed wing virus (DWV), and highlighting research areas that may help test it. Data so far suggest that DWV spills over from managed to wild bee species and has the potential to cause population decline. That DWV and other viruses of A. mellifera are found in other bee species needs to be considered for the sustainable management of bee populations.