Stephan Wolf

Foraging distance in Bombus terrestris L. (Hymenoptera: Apidae)*

A major determinant of bumblebees pollination efficiency is the distance of pollen dispersal, which depends on the foraging distance of workers. We employ a transect setting, controlling for both forage and nest location, to assess the foraging distance of Bombus terrestris workers and the influence of environmental factors on foraging frequency over distance. The mean foraging distance of B. terrestris workers was 267.2 m ± 180.3 m (max. 800 m). Nearly 40% of the workers foraged within 100 m around the nest. B. terrestris workers have thus rather moderate foraging ranges if rewarding forage is available within vicinity of the nests. We found the spatial distribution and the quality of forage plots to be the major determinants for the bees foraging decision-making, explaining over 80% of the foraging frequency. This low foraging range has implications for using B. terrestris colonies as pollinators in agriculture.ZusammenfassungPollenverbreitung durch Tiere ist eine Schlüsselfunktion in Ökosystemen. Hummeln (Bombus sp.) gehören zu den effizientesten Bestäubern, sowohl von Wildpflanzen, als auch von Nutzpflanzen. Ein wesentliches Merkmal zur Bestimmung dieser Bestäubungseffizienz ist die Distanz, über die Pollen verbreitet werden können. Diese Entfernung hängt stark von der Flugdistanz von individuellen Sammlerinnen ab und dieser Parameter ist schon mehrfach untersucht worden, wobei eine große Vielfalt von Methoden genutzt wurde. So wurden Transekt-Beobachtungen, genetische Studien, Fang-Wiederfang-Experimente, Radar-Monitoring und theoretische Modelle angewendet, um die Flugdistanz abzuschätzen. Die Ergebnisse dieser Untersuchungen zeichnen sich hauptsächlich durch eine hohe Variabilität aus. Schätzungen reichen von wenigen hundert Metern bis zu mehreren Kilometern.Wir nutzen hier ein Transekt-Experiment, bei dem wir sowohl die Entfernung der Blüten als Futterquellen als auch der Nestposition kontrollierten. Sechs B. terrestris-Kolonien mit farbmarkierten Arbeiterinnen wurden in einer ausgeräumten Agrarlandschaft an den Anfang eines als Transekt genutzten Feldweges positioniert. Die einzig vorhandenen Futterquellen wuchsen entlang dieses Feldweges (Abb. 1). Über zehn Tage wurden Sammlerinnen beobachtet und deren Entfernung zum Nest festgehalten. Unser experimenteller Aufbau erlaubte weiterhin die Abschätzung der Qualität der vorhandenen Futterquellen gemessen als Anzahl der blühenden Disteln (die einzig genutzte Futterquelle) pro 100 m-Intervall. Damit konnten auch Umwelteinflüsse auf das Flugverhalten einbezogen werden.Die durchschnittliche Foragierdistanz von B. terrestris Arbeiterinnen betrug 267,2 m ± 180,3 m (Maximum: 800 m). Fast 40 % der beobachteten Arbeiterinnen sammelten innerhalb von 100 m vom Nest. Über 60 % der Sammlerinnen entfernten sich nicht weiter als 200 m von der Kolonie. Insgesamt nahm die Foragierfrequenz exponentiell ab, je weiter sich eine Futterquelle von Nest entfernt befand (Abb. 2). Signifikante Abweichungen von dieser Verteilung bei 300 m und 500 m konnten auf die Qualität der Futterquellen (= Anzahl der Blütenstände) zurückgeführt werden. Blütenangebot konnte 40 % der Varianz erklären, die nicht von der Entfernung zum Nest abhängig war (Abb. 3). Im Einklang mit früheren Untersuchungen zeigten Sammlerinnen eher kurze Flugdistanzen, wenn die Qualität der vorhandenen Blüten gut und Blüten in direkter Nähe zum Nest vorhanden sind. Wir konnten zeigen, dass die räumliche Verteilung und Qualität der vorhandenen Futterquellen Haupteinflussfaktoren für das Sammelflugverhalten von Hummeln sind und über 80 % der Foragierfrequenz erklären konnten. Die kurze Flugdistanz von Sammlerinnen sollte beim Einsatz von B. terrestris Kolonien für Bestäubungszwecke in der Landwirtschaft berücksichtigt werden.

So Near and Yet So Far: Harmonic Radar Reveals Reduced Homing Ability of Nosema Infected Honeybees

Pathogens may gain a fitness advantage through manipulation of the behaviour of their hosts. Likewise, host behavioural changes can be a defence mechanism, counteracting the impact of pathogens on host fitness. We apply harmonic radar technology to characterize the impact of an emerging pathogen - Nosema ceranae (Microsporidia) - on honeybee (Apis mellifera) flight and orientation performance in the field. Honeybees are the most important commercial pollinators. Emerging diseases have been proposed to play a prominent role in colony decline, partly through sub-lethal behavioural manipulation of their hosts. We found that homing success was significantly reduced in diseased (65.8%) versus healthy foragers (92.5%). Although lost bees had significantly reduced continuous flight times and prolonged resting times, other flight characteristics and navigational abilities showed no significant difference between infected and non-infected bees. Our results suggest that infected bees express normal flight characteristics but are constrained in their homing ability, potentially compromising the colony by reducing its resource inputs, but also counteracting the intra-colony spread of infection. We provide the first high-resolution analysis of sub-lethal effects of an emerging disease on insect flight behaviour. The potential causes and the implications for both host and parasite are discussed.

The reliability of morphological traits in the differentiation of Bombus terrestris and B. lucorum (Hymenoptera: Apidae)*

The bumblebees of the subgenus Bombus sensu strictu are a notoriously difficult taxonomic group because identification keys are based on the morphology of the sexuals, yet the workers are easily confused based on morphological characters alone. Based on a large field sample of workers putatively belonging to either B. terrestris or B. lucorum, we here test the applicability and accuracy of a frequently used taxonomic identification key for continental European bumblebees and mtDNA restriction fragment length polymorphism (RFLP) that are diagnostic for queens to distinguish between B. terrestris and B. lucorum, two highly abundant but easily confused species in Central Europe. Bumblebee workers were grouped into B. terrestris and B. lucorum either based on the taxonomic key or their mtDNA RFLP. We also genotyped all workers with six polymorphic microsatellite loci to show which grouping better matched a coherent Hardy-Weinberg population. Firstly we could show that the mtDNA RFLPs diagnostic in queens also allowed an unambiguous discrimination of the two species. Moreover, the population genetic data confirmed that the mtDNA RFLP method is superior to the taxonomic tools available. The morphological key provided 45% misclassifications for B. lucorum and 5% for B. terrestris. Hence, for studies on B. terrestris we recommend to double check species identity with mtDNA RFLP analysis, especially when conducted in Central Europe.ZusammenfassungDie Artbestimmung bei Hummelarbeiterinnen der Untergattung Bombus sensu strictu mittles morphologischer Merkmale hat sich wiederholt als schwierig erwiesen, da morphologische Bestimmungsmerkmale zwar bei Geschlechtstieren (Königinnen und Drohnen) eine gute Unterscheidung zulassen, bei Arbeiterinnen jedoch häufig uneindeutig sind.Basierend auf einer grossen Freilandstichprobe von B. terrestris / B. lucorum Arbeiterinnen, zwei häufige, aber schwer zu unterscheidende mitteleuropäische Arten, testen wir hier die Anwendbarkeit und diagnostische Verlässlichkeit zweier Bestimmungsmethoden. Zum Einen, die eines häufig genutzten Bestimmungsschlüssels für mitteleuropäische Hummeln, zum Anderen, mtDNA Restriktions-Fragmentlängen-Polymorphismen (RFLP), die eine Artunterscheidung bei Königinnen von B. terrestris und B. lucorum erlauben. Die Hummelarbeiterinnen wurden dabei basierend auf entweder morphologischen Merkmalen oder anhand ihrer mtDNA RFLPs zu B. terrestris oder B. lucorum zugeordnet. Alle Individuen wurden an sechs Mikrosatelliten-Loci genotypisiert um zu testen, welche der beiden Artgruppierungen (Morphologie- oder mtDNA-basiert) besser mit einer zu erwartenden Hardy-Weinberg Population übereinstimmt.Zum Ersten konnten wir zeigen, dass die für Königinnen diagnostischen mtDNA RFLPs auch bei Arbeiterinnen eine eindeutige Artbestimmung zulassen. Darüber hinaus konnten wir durch unsere populationsgenetischen Analysen bestätigen, dass die Artbestimmung mittels mtDNA RFLPs der durch morphologische Merkmale in Präzision deutlich überlegen ist. Die Artbestimmung mittels des Bestimmungsschlüssels führte zu 45% Fehlbestimmungen bei B. lucorum, Fehlbestimmungen bei B. terrestris wurden in 5% aller Fälle gefunden. Folglich empfehlen wir die verlässliche Artbestimmung mittels genetischer Methoden bei Studien an B. terrestris, vor allem, wenn diese in Mitteleuropa durchgeführt werden und populationsgenetische Untersuchungen beinhalten.

Evidence for a pervasive 'idling-mode' activity template in flying and pedestrian insects

Understanding the complex movement patterns of animals in natural environments is a key objective of ‘movement ecology’. Complexity results from behavioural responses to external stimuli but can also arise spontaneously in their absence. Drawing on theoretical arguments about decision-making circuitry, we predict that the spontaneous patterns will be scale-free and universal, being independent of taxon and mode of locomotion. To test this hypothesis, we examined the activity patterns of the European honeybee, and multiple species of noctuid moth, tethered to flight mills and exposed to minimal external cues. We also reanalysed pre-existing data for Drosophila flies walking in featureless environments. Across these species, we found evidence of common scale-invariant properties in their movement patterns; pause and movement durations were typically power law distributed over a range of scales and characterized by exponents close to 3/2. Our analyses are suggestive of the presence of a pervasive scale-invariant template for locomotion which, when acted on by environmental cues, produces the movements with characteristic scales observed in nature. Our results indicate that scale-finite complexity as embodied, for instance, in correlated random walk models, may be the result of environmental cues overriding innate behaviour, and that scale-free movements may be intrinsic and not limited to ‘blind’ foragers as previously thought.

Sex, horizontal transmission, and multiple hosts prevent local adaptation of Crithidia bombi, a parasite of bumblebees (Bombus spp.)

Local adaptation within host-parasite systems can evolve by several non-exclusive drivers (e.g., host species-genetic adaptation; ecological conditions-ecological adaptation, and time-temporal adaptation). Social insects, especially bumblebees, with an annual colony life history not only provide an ideal system to test parasite transmission within and between different host colonies, but also parasite adaptation to specific host species and environments. Here, we study local adaptation in a multiple-host parasite characterized by high levels of horizontal transmission. Crithidia bombi occurs as a gut parasite in several bumblebee species. Parasites were sampled from five different host species in two subsequent years. Population genetic tools were used to test for the several types of adaptation. Although we found no evidence for local adaptation of the parasite toward host species, there was a slight temporal differentiation of the parasite populations, which might have resulted from severe bottlenecks during queen hibernation. Parasite populations were in Hardy-Weinberg equilibrium and showed no signs of linkage disequilibrium suggesting that sexual reproduction is an alternative strategy in this otherwise clonal parasite. Moreover, high levels of multiple infections were found, which might facilitate sexual genetic exchange. The detection of identical clones in different host species suggested that horizontal transmission occurs between host species and underpins the lack of host-specific adaptation.

Optimal search patterns in honeybee orientation flights are robust against emerging infectious diseases

Lévy flights are scale-free (fractal) search patterns found in a wide range of animals. They can be an advantageous strategy promoting high encounter rates with rare cues that may indicate prey items, mating partners or navigational landmarks. The robustness of this behavioural strategy to ubiquitous threats to animal performance, such as pathogens, remains poorly understood. Using honeybees radar-tracked during their orientation flights in a novel landscape, we assess for the first time how two emerging infectious diseases (Nosema sp. and the Varroa-associated Deformed wing virus (DWV)) affect bees’ behavioural performance and search strategy. Nosema infection, unlike DWV, affected the spatial scale of orientation flights, causing significantly shorter and more compact flights. However, in stark contrast to disease-dependent temporal fractals, we find the same prevalence of optimal Lévy flight characteristics (μ ≈ 2) in both healthy and infected bees. We discuss the ecological and evolutionary implications of these surprising insights, arguing that Lévy search patterns are an emergent property of fundamental characteristics of neuronal and sensory components of the decision-making process, making them robust against diverse physiological effects of pathogen infection and possibly other stressors.

Flight performance of actively foraging honey bees is reduced by a common pathogen

Summary Sudden and severe declines in honey bee (Apis mellifera) colony health in the US and Europe have been attributed, in part, to emergent microbial pathogens, however, the mechanisms behind the impact are unclear. Using roundabout flight mills, we measured the flight distance and duration of actively foraging, healthy‐looking honey bees sampled from standard colonies, before quantifying the level of infection by Nosema ceranae and Deformed Wing Virus complex (DWV) for each bee. Neither the presence nor the quantity of N. ceranae were at low, natural levels of infection had any effect on flight distance or duration, but presence of DWV reduced flight distance by two thirds and duration by one half. Quantity of DWV was shown to have a significant, but weakly positive relation with flight distance and duration, however, the low amount of variation that was accounted for suggests further investigation by dose‐response assays is required. We conclude that widespread, naturally occurring levels of infection by DWV weaken the flight ability of honey bees and high levels of within‐colony prevalence are likely to reduce efficiency and increase the cost of resource acquisition. Predictions of implications of pathogens on colony health and function should take account of sublethal effects on flight performance.

Male bumblebees, Bombus terrestris, perform equally well as workers in a serial colour-learning task.

The learning capacities of males and females may differ with sex-specific behavioural requirements. Bumblebees provide a useful model system to explore how different lifestyles are reflected in learning abilities, because their (female but sterile) workers and males engage in fundamentally different behaviour routines. Bumblebee males, like workers, embark on active flower foraging but in contrast to workers they have to trade off their feeding with mate search, potentially affecting their abilities to learn and utilize floral cues efficiently during foraging. We used a serial colour-learning task with freely flying males and workers to compare their ability to flexibly learn visual floral cues with reward in a foraging scenario that changed over time. Male bumblebees did not differ from workers in both their learning speed and their ability to overcome previously acquired associations, when these ceased to predict reward. In all foraging tasks we found a significant improvement in choice accuracy in both sexes over the course of the training. In both sexes, the characteristics of the foraging performance depended largely on the colour difference of the two presented feeder types. Large colour distances entailed fast and reliable learning of the rewarding feeders whereas choice accuracy on highly similar colours improved significantly more slowly. Conversely, switching from a learned feeder type to a novel one was fastest for similar feeder colours and slow for highly different ones. Overall, we show that behavioural sex dimorphism in bumblebees did not affect their learning abilities beyond the mating context. We discuss the possible drivers and limitations shaping the foraging abilities of males and workers and implications for pollination ecology. We also suggest stingless male bumblebees as an advantageous alternative model system for the study of pollinator cognition.

Number of honeybee colonies in areas with high and low beekeeping activity in Southern Mexico

The number of colonies in feral and managed honeybee populations (Apis mellifera) was determined for various sampling locations in Chiapas and Yucatan (Mexico) to assess the impact of apiculture on feral honeybee populations. We used a comparative sampling approach determining the number of colonies in similar habitats and landscapes but with different intensity of beekeeping. Sampling sites included nature reserves, and mango and shaded coffee plantations. The agricultural sites were all set in high-diversity landscapes with plenty of surrounding secondary forest. The number of colonies was determined by genotyping drones caught on drone congregation areas and assigning the drone genotypes to mother queens each heading a colony. We used three sets of linked markers each to achieve sufficient resolution for a precise colony assignment. The estimated colony numbers ranged from 34 to 54 colonies, with an average of 38.3 ± 6.9 colonies in areas with high and 43.5 ± 6.6 colonies in areas with low beekeeping activity. There was no significant difference in colony numbers between the sites with high and low beekeeping activity suggesting that the managed honeybee populations do not substantially add to the overall number of honeybee colonies supported in the wild. This might indicate that restrictions on apicultural activities to prevent any potential conservation conflict with native pollinators might not be useful, since honeybee colonies are very abundant in many different landscapes in Southern Mexico independent of apiculture.