Automated 3D image-based tracking systems are new and promising devices to investigate the foraging behavior of flying animals with great accuracy and precision. 3D analyses can provide accurate assessments of flight performance in regard to speed, curvature, and hovering. However, there have been few applications of this technology in ecology, particularly for insects. We used this technology to analyze the behavioral interactions between the Western honey bee Apis mellifera and its invasive predator the Asian hornet, Vespa velutina nigrithorax. We investigated whether predation success could be affected by flight speed, flight curvature, and hovering of the Asian hornet and honey bees in front of one beehive. We recorded a total of 603,259 flight trajectories and 5175 predator-prey flight interactions leading to 126 successful predation events, representing 2.4% predation success. Flight speeds of hornets in front of hive entrances were much lower than that of their bee prey; in contrast to hovering capacity, while curvature range overlapped between the two species. There were large differences in speed, curvature, and hovering between the exit and entrance flights of honey bees. Interestingly, we found hornet density affected flight performance of both honey bees and hornets. Higher hornet density led to a decrease in the speed of honey bees leaving the hive, and an increase in the speed of honey bees entering the hive, together with more curved flight trajectories. These effects suggest some predator avoidance behavior by the bees. Higher honey bee flight curvature resulted in lower hornet predation success. Results showed an increase in predation success when hornet number increased up to 8 individuals, above which predation success decreased, likely due to competition among predators. Although based on a single colony, this study reveals interesting outcomes derived from the use of automated 3D tracking to derive accurate measures of individual behavior and behavioral interactions among flying species.

The invasive hornet Vespa velutina nigrithorax is considered a proliferating threat to pollinators in Europe and Asia. While the impact of this species on managed honey bees is well-documented, effects upon other pollinator populations remain poorly understood. Nonetheless, dietary analyses indicate that the hornets consume a diversity of prey, fuelling concerns for at-risk taxa. Here, we quantify the impact of V. velutina upon standardised commercially-reared colonies of the European bumblebee, Bombus terrestris terrestris. Using a landscape-scale experimental design, we deploy colonies across a gradient of local V. velutina densities, utilising automated tracking to non-invasively observe bee and hornet behaviour, and quantify subsequent effects upon colony outcomes. Our results demonstrate that hornets frequently hunt at B. terrestris colonies, being preferentially attracted to those with high foraging traffic, and engaging in repeated-yet entirely unsuccessful-predation attempts at nest entrances. Notably however, we show that B. terrestris colony weights are negatively associated with local V. velutina densities, indicating potential indirect effects upon colony growth. Taken together, these findings provide the first empirical insight into impacts on bumblebees at the colony level, and inform future mitigation efforts for wild and managed pollinators.

Forage availability has been suggested as one driver of the observed decline in honey bees. However, little is known about the effects of its spatiotemporal variation on colony success. We present a modeling framework for assessing honey bee colony viability in cropping systems. Based on two real farmland structures, we developed a landscape generator to design cropping systems varying in crop species identity, diversity, and relative abundance. The landscape scenarios generated were evaluated using the existing honey bee colony model BEEHAVE, which links foraging to in-hive dynamics. We thereby explored how different cropping systems determine spatiotemporal forage availability and, in turn, honey bee colony viability (e.g. time to extinction, TTE) and resilience (indicated by, e.g. brood mortality). To assess overall colony viability, we developed metrics, PH and PP, which quantified how much nectar and pollen provided by a cropping system per year was converted into a colony's adult worker population. Both crop species identity and diversity determined the temporal continuity in nectar and pollen supply and thus colony viability. Overall farmland structure and relative crop abundance were less important, but details mattered. For monocultures and for four-crop species systems composed of cereals, oilseed rape, maize, and sunflower, PH and PP were below the viability threshold. Such cropping systems showed frequent, badly timed, and prolonged forage gaps leading to detrimental cascading effects on life stages and in-hive work force, which critically reduced colony resilience. Four-crop systems composed of rye-grass-dandelion pasture, trefoil-grass pasture, sunflower, and phacelia ensured continuous nectar and pollen supply resulting in TTE > 5 yr, and PH (269.5 kg) and PP (108 kg) being above viability thresholds for 5 yr. Overall, trefoil-grass pasture, oilseed rape, buckwheat, and phacelia improved the temporal continuity in forage supply and colony's viability. Our results are hypothetical as they are obtained from simplified landscape settings, but they nevertheless match empirical observations, in particular the viability threshold. Our framework can be used to assess the effects of cropping systems on honey bee viability and to develop land-use strategies that help maintain pollination services by avoiding prolonged and badly timed forage gaps.

Varroa destructor is one of the major contributors to the significant losses of Western honey bee colonies worldwide. The synthetic pyrethroids tau-fluvalinate and flumethrin were very popular among beekeepers to control levels of parasitism until reports of therapeutic failures increased during the early 1990s. Three different mutations at position 925 of the V. destructor voltage-gated sodium channel have been associated with the resistance to these compounds. Resistant mites collected in the UK and in the Czech Republic showed only a substitution of leucine to valine (L925V), while those collected in the USA carried alternative mutations to isoleucine (L925I) or methionine (L925M). Here, we have used high-throughput genotyping assays to investigate the distribution of resistance mutations across Europe. Our data show that the mutation L925V is present in most of the European countries tested, albeit with an uneven distribution. We also show new evidence for the significant correlation of the mutation with resistance and conclude that it is likely that resistant mites have a reduced fitness. The implications for integrated management of the parasite are discussed.

Asian hornets (Vespa velutina) are voracious predators of bees, and are the latest emerging threat to managed and wild pollinator populations in Europe. To prevent establishment or reduce the rate of spread of V. velutina, early detection and destruction of nests is considered the only option. Detection is difficult as their nests are well hidden and flying hornets are difficult to follow over long distances. We address this challenge by tracking individual V. velutina workers flying back to their nests using radio telemetry for the first time, finding five previously undiscovered nests, up to 1.33 km from hornet release points. Hornets can fly with 0.28 g tags if the tag:hornet ratio is less than 0.8. This method offers a step-change in options to tackle the spread of this invader, providing an efficient means of finding V. velutina nests in complex environments to manage this emerging threat to pollinators.

Full text:. http://www.nature.com/articles/s42003-018-0092-9

The causes underlying the increased mortality of honeybee Apis mellifera colonies observed over the past decade remain unclear. Since so far the evidence for monocausal explanations is equivocal, involvement of multiple stressors is generally assumed. We here focus on various aspects of forage availability, which have received less attention than other stressors because it is virtually impossible to explore them empirically. We applied the colony model BEEHAVE, which links within‐hive dynamics and foraging, to stylized landscape settings to explore how foraging distance, forage supply, and “forage gaps”, i.e. periods in which honeybees cannot find any nectar and pollen, affect colony resilience and the mechanisms behind. We found that colony extinction was mainly driven by foraging distance, but the timing of forage gaps had strongest effects on time to extinction. Sensitivity to forage gaps of 15 days was highest in June or July even if otherwise forage availability was sufficient to survive. Forage availability affected colonies via cascading effects on queen's egg‐laying rate, reduction of new‐emerging brood stages developing into adult workers, pollen debt, lack of workforce for nursing, and reduced foraging activity. Forage gaps in July led to reduction in egg‐laying and increased mortality of brood stages at a time when the queen's seasonal egg‐laying rate is at its maximum, leading to colony failure over time. Our results demonstrate that badly timed forage gaps interacting with poor overall forage supply reduce honeybee colony resilience. Existing regulation mechanisms which in principle enable colonies to cope with varying forage supply in a given landscape and year, such as a reduction in egg‐laying, have only a certain capacity. Our results are hypothetical, as they are obtained from simplified landscape settings, but they are consistent with existing empirical knowledge. They offer ample opportunities for testing the predicted effects of forage stress in controlled experiments.

To simulate effects of pesticides on different honeybee (Apis mellifera L.) life stages, we used the BEEHAVE model to explore how increased mortalities of larvae, in-hive workers, and foragers, as well as reduced egg-laying rate, could impact colony dynamics over multiple years. Stresses were applied for 30 days, both as multiples of the modeled control mortality and as set percentage daily mortalities to assess the sensitivity of the modeled colony both to small fluctuations in mortality and periods of low to very high daily mortality. These stresses simulate stylized exposure of the different life stages to nectar and pollen contaminated with pesticide for 30 days. Increasing adult bee mortality had a much greater impact on colony survival than mortality of bee larvae or reduction in egg laying rate. Importantly, the seasonal timing of the imposed mortality affected the magnitude of the impact at colony level. In line with the LD50, we propose a new index of "lethal imposed stress": the LIS50 which indicates the level of stress on individuals that results in 50% colony mortality. This (or any LISx) is a comparative index for exploring the effects of different stressors at colony level in model simulations. While colony failure is not an acceptable protection goal, this index could be used to inform the setting of future regulatory protection goals.

Summary: a notable increase in failure of managed European honeybee Apis mellifera L. colonies has been reported in various regions in recent years. Although the underlying causes remain unclear, it is likely that a combination of stressors act together, particularly varroa mites and other pathogens, forage availability and potentially pesticides. It is experimentally challenging to address causality at the colony scale when multiple factors interact. In silico experiments offer a fast and cost-effective way to begin to address these challenges and inform experiments. However, none of the published bee models combine colony dynamics with foraging patterns and varroa dynamics. We have developed a honeybee model, BEEHAVE, which integrates colony dynamics, population dynamics of the varroa mite, epidemiology of varroa-transmitted viruses and allows foragers in an agent-based foraging model to collect food from a representation of a spatially explicit landscape. We describe the model, which is freely available online (www.beehave-model.net). Extensive sensitivity analyses and tests illustrate the model's robustness and realism. Simulation experiments with various combinations of stressors demonstrate, in simplified landscape settings, the model's potential: predicting colony dynamics and potential losses with and without varroa mites under different foraging conditions and under pesticide application. We also show how mitigation measures can be tested. Synthesis and applications. BEEHAVE offers a valuable tool for researchers to design and focus field experiments, for regulators to explore the relative importance of stressors to devise management and policy advice and for beekeepers to understand and predict varroa dynamics and effects of management interventions. We expect that scientists and stakeholders will find a variety of applications for BEEHAVE, stimulating further model development and the possible inclusion of other stressors of potential importance to honeybee colony dynamics. © 2014 the Authors. Journal of Applied Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.

The Varroa mite, Varroa destructor, is an important pest of honeybees and has played a prominent role in the decline in bee colony numbers over recent years. Although pyrethroids such as tau-fluvalinate and flumethrin can be highly effective in removing the mites from hives, their intensive use has led to many reports of resistance. To investigate the mechanism of resistance in UK Varroa samples, the transmembrane domain regions of the V. destructor voltage-gated sodium channel (the main target site for pyrethroids) were PCR amplified and sequenced from pyrethroid treated/untreated mites collected at several locations in Central/Southern England. A novel amino acid substitution, L925V, was identified that maps to a known hot spot for resistance within the domain IIS5 helix of the channel protein; a region that has also been proposed to form part of the pyrethroid binding site. Using a high throughput diagnostic assay capable of detecting the mutation in individual mites, the L925V substitution was found to correlate well with resistance, being present in all mites that had survived tau-fluvalinate treatment but in only 8% of control, untreated samples. The potential for using this assay to detect and manage resistance in Varroa-infected hives is discussed. © 2013 González-Cabrera et al.

The health of managed and wild honeybee colonies appears to have declined substantially in Europe and the United States over the last decade. Sustainability of honeybee colonies is important not only for honey production, but also for pollination of crops and wild plants alongside other insect pollinators. A combination of causal factors, including parasites, pathogens, land use changes and pesticide usage, are cited as responsible for the increased colony mortality. However, despite detailed knowledge of the behaviour of honeybees and their colonies, there are no suitable tools to explore the resilience mechanisms of this complex system under stress. Empirically testing all combinations of stressors in a systematic fashion is not feasible. We therefore suggest a cross-level systems approach, based on mechanistic modelling, to investigate the impacts of (and interactions between) colony and land management. We review existing honeybee models that are relevant to examining the effects of different stressors on colony growth and survival. Most of these models describe honeybee colony dynamics, foraging behaviour or honeybee - varroa mite - virus interactions. We found that many, but not all, processes within honeybee colonies, epidemiology and foraging are well understood and described in the models, but there is no model that couples in-hive dynamics and pathology with foraging dynamics in realistic landscapes. Synthesis and applications. We describe how a new integrated model could be built to simulate multifactorial impacts on the honeybee colony system, using building blocks from the reviewed models. The development of such a tool would not only highlight empirical research priorities but also provide an important forecasting tool for policy makers and beekeepers, and we list examples of relevant applications to bee disease and landscape management decisions. We describe how a new integrated model could be built to simulate multifactorial impacts on the honeybee colony system, using building blocks from the reviewed models. The development of such a tool would not only highlight empirical research priorities but also provide an important forecasting tool for policy makers and beekeepers, and we list examples of relevant applications to bee disease and landscape management decisions. © 2013 British Ecological Society.

Spatially explicit predator-prey interactions can alter the predatory potential of natural enemies augmented through conservation biological control. To test hypotheses regarding such interactions and predatory efficiency, we used a combination of molecular techniques and mark-release-recapture to study the foraging behaviour of a generalist carabid predator, Poecilus cupreus, in response to spatial patterns of its cereal aphid prey (Metapolophium dirhodum and Sitobion avenae). Beetle and aphid numbers were measured across two grids of sampling locations, within which aphid spatial pattern had been manipulated to generate patchy and more homogenous distributions. Aphid consumption was measured by enzyme-linked immunosorbent assays (ELISA) of beetle gut contents, using an aphid-specific monoclonal antibody. Movement and distribution patterns suggest that P. cupreus does not aggregate at, nor instigate prey-taxis within, aphid patches. However, more than two-thirds of the 2169 P. cupreus tested by ELISA had consumed aphids and the proportion of beetles containing aphid proteins was positively related to aphid density. Against expectation, the proportion of predators feeding on aphids was greatest where prey were homogenously distributed, and this was attributed to the loss of partial refuges for prey in aphid patches. The functional value of this type of uniform foraging strategy is ideally suited to early colonization of the crop habitat, when aphid numbers are low, before populations build up and form strong spatial patterns.

A field-scale study of the spatially explicit interaction between the carabid Poecilus cupreus Linnaeus, and two common aphid species (Sitobion avenae (Fabricius) and Metopolophium dirhodum (Walker)) in winter wheat was conducted. All three species showed considerable spatial pattern at the field scale. Activity-density of P. cupreus was an order of magnitude higher in the central part of the field compared to its periphery. Where P. cupreus activity-density was highest, S. avenae and M. dirhodum population peaks were delayed. Additionally, in the case of M. dirhodum, lower maximum counts were evident where P. cupreus activity-density was highest. An analysis of the movement of individual P. cupreus using release-recapture indicated that those beetles within the centre of the field exhibited reduced displacement, which may have caused the generation or maintenance of spatial pattern. Crop density was also measured throughout the field. Although crop density had no large-scale spatial pattern, its variability at the small-scale was consistent with an influence on aphid population dynamics. This study demonstrates empirically that both large-scale spatially explicit and small-scale localized processes influenced aphid population dynamics simultaneously.

In the UK, recommended field trial protocols for assessing within-season effects of insecticides on non-target arthropods in cereals utilise either large (1 ha or greater) open plots or small (not less than 10m × 10m) enclosed plots. Prior to this study, no direct comparison of the relative effectiveness and reliability in discerning such effects of these two approaches had been attempted. In a 2-year study, the effects of dimethoate and pirimicarb on polyphagous predators were investigated using both small enclosed plots and large open plots in the same experiment. The activity-density of Carabidae, Staphylinidae and Linyphiidae was measured using pitfall traps over at least five pre- and four post-treatment weeks in each year. More species were caught in greater numbers in large open plots than in small enclosed plots. Both approaches caught sufficient individuals to analyse effects of insecticides on whole taxonomic families but too few individuals were caught in small enclosed plots to analyse effects on species other than those most abundant. More individuals were caught per trap and catch variability was less in large open plots than in small enclosed plots. The impact of plot type on pitfall trap catch was greatest for Carabidae and least for Staphylinidae. Treatment with dimethoate led to significant short-term reductions in catches of Carabidae and Linyphiidae, while treatment with pirimicarb had no significant effect on polyphagous predators. Neither of the insecticides applied in 1993 affected pitfall trap catches, in the following year, of predators that were active pre-treatment. No significant interactions were recorded between plot type and insecticide treatment, but low and variable pitfall trap catches in small enclosed plots makes the detection of such interactions difficult. Small enclosed plots, with pitfall traps placed centrally, should not be used in field trials as an alternative to large open plots without modifying sampling methods to increase trap captures and decrease overall variability in numbers caught. The use of more traps, more efficient trapping and greater replication all need to be investigated. © 2001 Elsevier Science B.V.