Bumblebee foraging rhythms under the midnight sun measured with radiofrequency identification

Abstract

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.

Figure 1

Daily average plots of the foraging activity under continuous daylight conditions in the field. The top row shows daily average plots of the Bombus terrestris colonies observed at Kilpisjärvi Biological Station, Finland, in the summer of 2007 and the bottom row shows the data for the colonies observed in the summer of 2008 at the same location. Numbers in brackets indicate the number of tagged workers meeting the requirements to be included in the circadian analysis per colony. Each bar represents an hour of the day and the height of the bars indicates the level of activity.

Figure 2

Exemplary double plotted actograms of a colony and individual foragers. Double-plotted actogram of (a) a Bombus terrestris colony (colony A) and (b) an individual worker of that colony. (c) and (d) actograms of two individual foragers of colony F to highlight the differences in foraging activity of individual workers. Each line represents two consecutive days of the experiment, each bar indicates 1 h of the day and the height of the bars indicates the level of foraging activity in that hour.

Figure 3

Mean traffic at the nest entrance of a natural Bombus pascuorum nest. The nest was located near the field station and traffic was monitored for 30 min in intervals of 2 h. Every leaving or returning bee was counted.

Figure 4

Mean hourly values of environmental cues that could act as possible Zeitgebers on the circadian clocks of bumblebees under continuous daylight conditions. (a) light intensity, (b) ambient temperature and (c) UV radiation (320 nm to 410 nm) recorded between 5 July 2008 and 13 July 2008 at the field station. Two days (7 July 2008 and 8 July 2008) have been excluded from the UB measurements because the values were not recorded for the whole 24 h of these days. Temperature data were obtained from the Finnish Meteorological Institute and UV data were kindly provided by Dr. Iris Zellmer.