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 Darwin(1.)

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.

Radar tracking and motion-sensitive cameras on flowers reveal the development of pollinator multi-destination routes over large spatial scales.

Central place foragers, such as pollinating bees, typically develop circuits (traplines) to visit multiple foraging sites in a manner that minimizes overall travel distance. Despite being taxonomically widespread, these routing behaviours remain poorly understood due to the difficulty of tracking the foraging history of animals in the wild. Here we examine how bumblebees (Bombus terrestris) develop and optimise traplines over large spatial scales by setting up an array of five artificial flowers arranged in a regular pentagon (50 m side length) and fitted with motion-sensitive video cameras to determine the sequence of visitation. Stable traplines that linked together all the flowers in an optimal sequence were typically established after a bee made 26 foraging bouts, during which time only about 20 of the 120 possible routes were tried. Radar tracking of selected flights revealed a dramatic decrease by 80% (ca. 1500 m) of the total travel distance between the first and the last foraging bout. When a flower was removed and replaced by a more distant one, bees engaged in localised search flights, a strategy that can facilitate the discovery of a new flower and its integration into a novel optimal trapline. Based on these observations, we developed and tested an iterative improvement heuristic to capture how bees could learn and refine their routes each time a shorter route is found. Our findings suggest that complex dynamic routing problems can be solved by small-brained animals using simple learning heuristics, without the need for a cognitive map.

Bumblebee foraging rhythms under the midnight sun measured with radiofrequency identification.

BACKGROUND: In 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. RESULTS: Foragers 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. CONCLUSIONS: The 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.

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.

Bird pollination of Canary Island endemic plants.

The Canary Islands are home to a guild of endemic, threatened bird-pollinated plants. Previous work has suggested that these plants evolved floral traits as adaptations to pollination by flower specialist sunbirds, but subsequently, they appear to have co-opted generalist passerine birds as sub-optimal pollinators. To test this idea, we carried out a quantitative study of the pollination biology of three of the bird-pollinated plants, Canarina canariensis (Campanulaceae), Isoplexis canariensis (Veronicaceae) and Lotus berthelotii (Fabaceae), on the island of Tenerife. Using colour vision models, we predicted the detectability of flowers to bird and bee pollinators. We measured pollinator visitation rates, nectar standing crops as well as seed-set and pollen removal and deposition. These data showed that the plants are effectively pollinated by non-flower specialist passerine birds that only occasionally visit flowers. The large nectar standing crops and extended flower longevities (>10 days) of Canarina and Isoplexis suggests that they have evolved a bird pollination system that effectively exploits these low frequency non-specialist pollen vectors and is in no way sub-optimal. Seed set in two of the three species was high and was significantly reduced or zero in flowers where pollinator access was restricted. In L. berthelotii, however, no fruit set was observed, probably because the plants were self-incompatible horticultural clones of a single genet. We also show that, while all three species are easily detectable for birds, the orange Canarina and the red Lotus (but less so the yellow-orange Isoplexis) should be difficult to detect for insect pollinators without specialised red receptors, such as bumblebees. Contrary to expectations if we accept that the flowers are primarily adapted to sunbird pollination, the chiffchaff (Phylloscopus canariensis) was an effective pollinator of these species.