Ralph J. Stelzer

Radar Tracking and Motion-Sensitive Cameras on Flowers Reveal the Development of Pollinator Multi-Destination Routes over Large Spatial Scales

Automated tracking of bumblebees and computer simulations reveal how bees locate a series of flowers and optimize their routes to visit them all.

Colony nutritional status modulates worker responses to foraging recruitment pheromone in the bumblebee Bombus terrestris

Foraging activity in social insects should be regulated by colony nutritional status and food availability, such that both the emission of, and response to, recruitment signals depend on current conditions. Using fully automatic radio-frequency identification (RFID) technology to follow the foraging activity of tagged bumblebees (Bombus terrestris) during 16,000 foraging bouts, we tested whether the cue provided by stored food (the number of full honeypots) could modulate the response of workers to the recruitment pheromone signal. Artificial foraging pheromones were applied to colonies with varied levels of food reserves. The response to recruitment pheromones was stronger in colonies with low food, resulting in more workers becoming active and more foraging bouts being performed. In addition to previous reports showing that in colonies with low food successful foragers perform more excited runs during which they release recruitment pheromone and inactive workers are more prone to leave the nest following nectar influx, our results indicate that evolution has shaped a third pathway that modulates bumblebee foraging activity, thus preventing needless energy expenditure and exposure to risk when food stores are already high. This new feedback loop is intriguing since it involves context-dependent response to a signal. It highlights the integration of information from both forager-released pheromones (signal) and nutritional status (cue) that occurs within individual workers before making the decision to start foraging. Our results support the emerging view that responses to pheromones may be less hardwired than commonly acknowledged.

Winter Active Bumblebees (Bombus terrestris) Achieve High Foraging Rates in Urban Britain

Background Foraging bumblebees are normally associated with spring and summer in northern Europe. However, there have been sightings of the bumblebee Bombus terrestris during the warmer winters in recent years in southern England. But what floral resources are they relying upon during winter and how much winter forage can they collect? Methodology/Principal Findings To test if urban areas in the UK provide a rich foraging niche for bees we set up colonies of B. terrestris in the field during two late winter periods (2005/6 & 2006/7) in London, UK, and measured their foraging performance. Fully automatic radio-frequency identification (RFID) technology was used in 2006/7 to enable us to record the complete foraging activity of individually tagged bees. The number of bumblebees present during winter (October 2007 to March 2008) and the main plants they visited were also recorded during transect walks. Queens and workers were observed throughout the winter, suggesting a second generation of bee colonies active during the winter months. Mass flowering shrubs such as Mahonia spp. were identified as important food resources. The foraging experiments showed that bees active during the winter can attain nectar and pollen foraging rates that match, and even surpass, those recorded during summer. Conclusions/Significance B. terrestris in the UK are now able to utilise a rich winter foraging resource in urban parks and gardens that might at present still be under-exploited, opening up the possibility of further changes in pollinator phenology.

Bumblebee foraging rhythms under the midnight sun measured with radiofrequency identification

BackgroundIn the permanent daylight conditions north of the Arctic circle, there is a unique opportunity for bumblebee foragers to maximise intake, and therefore colony growth, by remaining active during the entire available 24-h period. We tested the foraging rhythms of bumblebee (Bombus terrestris and B. pascuorum) colonies in northern Finland during the summer, when the sun stays above the horizon for weeks. We used fully automatic radio-frequency identification to monitor the foraging activity of more than 1,000 workers and analysed their circadian foraging rhythms.ResultsForagers did not use the available 24-h foraging period but exhibited robust diurnal rhythms instead. A mean of 95.2% of the tested B. terrestris workers showed robust diurnal rhythms with a mean period of 23.8 h. Foraging activity took place mainly between 08:00 and 23:00, with only low or almost no activity during the rest of the day. Activity levels increased steadily during the morning, reached a maximum around midday and decreased again during late afternoon and early evening. Foraging patterns of native B. pascuorum followed the same temporal organisation, with the foraging activity being restricted to the period between 06:00 and 22:00.ConclusionsThe results of the present study indicate that the circadian clock of the foragers must have been entrained by some external cue, the most prominent being daily cycles in light intensity and temperature. Daily fluctuations in the spectral composition of light, especially in the UV range, could also be responsible for synchronising the circadian clock of the foragers under continuous daylight conditions.

Circadian foraging rhythms of bumblebees monitored by radio-frequency identification.

Circadian clocks enable organisms to anticipate changes of environmental conditions. In social insects, the colony as a superorganism has a foraging rhythm aligned to the diurnal patterns of resource availability. Within this colony rhythm, the diurnal patterns of individuals are embedded, and various tasks within the colony are performed at different times by different individuals to best serve the colony as a whole. Recent studies have shown that social cues influence the traits of the circadian clock in social insects, but keeping track of the activity of individual workers is not an easy task. Here the authors use fully automatic radio-frequency identification (RFID) to analyze the circadian rhythms of bumblebee foragers (Bombus terrestris) in the normal social context of their nest. They monitored their foraging patterns under different light conditions in the laboratory, including light:dark cycles (LD) as well as constant darkness (DD) and constant light conditions (LL). Their results show that the majority of bumblebee foragers exhibit robust circadian rhythms in LD under laboratory conditions, while they show free-running rhythms both in DD and LL, with free-running periods being significantly shorter in LL conditions. The authors also found that bumblebee workers show an increased level of arrhythmic activity (“death dance”) in the hours or days before their death.

Unravelling the mechanisms of trapline foraging in bees

Trapline foraging (repeated sequential visits to a series of feeding locations) is a taxonomically widespread but poorly understood behavior. Investigating these routing strategies in the field is particularly difficult, as it requires extensive tracking of animal movements to retrace their complete foraging history. In a recent study, we used harmonic radar and motion-triggered video cameras to track bumblebees foraging between artificial flowers in a large open field. We describe how all bees gradually developed a near optimal trapline to link all flowers and have identified a simple learning heuristic capable of replicating this optimisation behavior. Our results provide new perspectives to clarify the sequence of decisions made by pollinating insects during trapline foraging, and explore how spatial memory is organized in their small brains. “I have always regretted that I did not mark the bees by attaching bits of cotton wool or eiderdown to them with rubber, because this would have made it much easier to follow their paths.” Charles Darwin1

Daily changes in ultraviolet light levels can synchronize the circadian clock of bumblebees (Bombus terrestris).

Endogenous circadian clocks are synchronized to the 24-h day by external zeitgebers such as daily light and temperature cycles. Bumblebee foragers show diurnal rhythms under daily light:dark cycles and short-period free-running circadian rhythms in constant light conditions in the laboratory. In contrast, during the continuous light conditions of the arctic summer, they show robust 24-h rhythms in their foraging patterns, meaning that some external zeitgeber must entrain their circadian clocks in the presence of constant light. Although the sun stays above the horizon for weeks during the arctic summer, the light quality, especially in the ultraviolet (UV) range, exhibits pronounced daily changes. Since the photoreceptors and photopigments that synchronize the circadian system of bees are not known, we tested if the circadian clocks of bumblebees (Bombus terrestris) can be entrained by daily cycles in UV light levels. Bumblebee colonies were set up in the laboratory and exposed to 12 h:12 h UV + :UV− cycles in otherwise continuous lighting conditions by placing UV filters on their foraging arenas for 12 h each day. The activity patterns of individual bees were recorded using fully automatic radiofrequency identification (RFID). We found that colonies manipulated in such a way showed synchronized 24-h rhythms, whereas simultaneously tested control colonies with no variation in UV light levels showed free-running rhythms instead. The results of our study show that bumblebee circadian rhythms can indeed be synchronized by daily cycles in ambient light spectral composition. (Author correspondence: r.stanewsky@qmul.ac.uk)