Sex or Food? bumblebee males and queens as a model to understand the foraging-mating trade-off in animals
Final Report Abstract
This DFG grant strategically supported the scientific establishment of reproductive bumblebees for cognitive and evolutionary research in context of sexual selection. We could show for the first time that male bumblebees have highly developed learning abilities, which allow them to successfully identify and memorize rewarding resources in a similar fashion as is known from workers. This work is the vital basis of any exploration of sexspecific effects on learning abilities in bees. Going way beyond the initial experimental plan, we could demonstrate that the learning abilities in both males and workers are highly flexible and behaviour can be readily adjusted to changes in foraging conditions in both sexes. The main driver of learning speed and discrimination performance in both males and workers was the colour distance between available floral resources. Assessing the learning abilities and long-term memory retention in hibernating queens we experimentally validated the hypothesis of a putative selective advantage of pre-hibernation learning even beyond the retention of the long-term memory. Expectedly, freshly emerged and colour naïve queens showed excellent colour learning abilities. However, assessing choice accuracy after the hibernation period our data indicated no (ultra) long-term memory retention of the learnt floral features after 10 weeks. However, the pre-hibernation learning did facilitate the re-learning of the same features after hibernation and post-hibernation queens (re-)learning the floral cues significantly faster than in the initial training and it can be argued that learning of floral features in autumn can result in a significant advantage in flower exploration in post-hibernated queens. This study is the first to demonstrate the indirect effects of learning over long periods of time and strongly encourages further in-depth exploration of this novel aspect of bee cognition as promising route to integrate cognitive behaviour with neuro-anatomical and -functional factors. Based a re-designed experimental approach I successfully explored how male and worker bumblebees utilize conflicting cues while foraging. Centred on the concept of selective attention and the ability to flexibly adjust information filtering, this experiment provides entirely novel insights into sex-specific cognitive abilities of bumblebees that inform about how selective processes shaped the neuronal substrate in order to facilitate sex-specific behavioural requirements. Using a combination of salient yet non-indicative cues and superimposed subtle indicators of reward, we could show that, other than for salient cues alone, males and workers embark on different foraging strategies which are aligned with their evolutionary history providing an ideal opportunity to further investigate evolutionary cognition in animals using a well-established model system. Surprisingly, we could show that floral/feeder arrangement on the vertical or horizontal plane can markedly affect how bees utilize environmental cues thus strongly affecting behavioural experiments. While bees showed expectedly excellent learning abilities for both colour and achromatic pattern cues on the horizontal plane, foragers did not use the same cues to guide their foraging when distributed vertically resulting in a random feeder visitation pattern as expected for un-labelled feeders. The non-utilization of clearly discriminable visual cues is at odds with the prevailing idea that visual learning in bees is solely restricted by the economics of cue discriminability and has both bearing on our understanding of visually guided foraging in bees in general as well as significant practical implications for any subsequent experimental work. The funding thus enabled the scientific access to a largely unexplored and fundamentally important research area – How does the sex shape our brains and why? BBC2 Documentary “Hive Alive” Episode 1 & 2, first aired 06.08.2014 QMUL press release: “Bumblebees differentiate flower types when arranged horizontally but not vertically”. Released 07.04.2015 QMUL press release: “Male bees have more than a one-track mind”. Released 12.11.2015
Publications
- (2015) A universal 'idling-mode' activity template in flying and pedestrian insects. Royal Society Open Science 2:150085
Reynolds AM, Jones H, Hill JK, Pearson A, Wilson K, Wolf S, Lim KS, Reynolds DR & Chapman JW
(See online at https://doi.org/10.1098/rsos.150085) - (2015) Bumblebees utilize floral cues differently on vertically and horizontally arranged flowers. Behavioural Ecology 26(3), 773-781
Wolf S, Roper M & Chittka L
(See online at https://doi.org/10.1093/beheco/arv010) - (2016) Male bumblebees (Bombus terrestris) perform equally well as workers in a serial colour learning task. Animal Behaviour 111: 147-155
Wolf S & Chittka L
(See online at https://doi.org/10.1016/j.anbehav.2015.10.009)
