Our results showed that honeybees have a very good ability to adjust their flight strategies under different loading states. When honeybees were under a low loading state (20 mg), their flight patterns were highly similar to the control group. Their flight paths during landing were more flexible with significantly larger curvatures but lower flight speeds compared to the 40 mg and 60 mg groups (Fig. 3). The control and 20 mg groups also rapidly decreased their flight speeds and notably increased their curvatures before reaching their hive entrance (Fig. 4A, B, E and F). These findings suggest that honeybees can flexibly make sharp turns under a low loading state, which is a general flight pattern during their homing process. The large turnings and low velocity would help honeybees to avoid traffic accidents in a heavy “bee cloud”11. The large turns possibly also benefit honeybees to avoid natural enemies such as hornets14 and birds15. Moreover, Feuerbacher et al showed that loading a small amount of pollen has no effect on honeybees’ wingbeat frequency, stroke amplitude, body angle or inclination of stroke plane but increases the mechanical power output9. Our results of the control and 20 mg groups are consistent with the previous study. Therefore, honeybee pollen foragers use a flight strategy of large curvatures and low velocity in their homing process.
For the 40 mg group, our results indicated that honeybees could adjust their flight pattern with significantly lower curvatures and higher flight speed compared to the control and 20 mg groups (Fig. 3). From upper to lower spaces, the 40 mg group had smaller but more stable average curvature but significantly higher flight speed compared to the control and 20 mg groups (Fig. 4). These findings clear revealed a different flight strategy in heavy-loading bees compared to the low-loading or unloaded bees. The smaller curvatures help heavy-loading bees to maintain balance during flight, however, their stable flight paths may be easy to be captured by enemies. Hence, heavy-loading bees increased their flight speed to reduce the risk of being caught as well as energy consumption.
For the 60 mg group, the over-loading weight strongly influenced honeybee flight behavior. We observed that most 60 mg loaded bees could not smoothly land but fall rapidly and hit onto the ground and then crawled into the hive entrance. The falling behaviour results in high curvatures, hence our results showed that the 60 mg group had a significantly higher curvature than that of 40 mg group, especially in terms of the top 20 turns (Fig. 3). These high curvatures of 60 mg group happened in the upper and middle spaces and they had a very low curvature in the lower space (Fig. 4D). The over-loading bees had significantly lower average flight speed than that of 40 mg groups (Fig. 3), but they surprisingly increased their velocities in the lower space (Fig. 4H). These results indicated that over-loading bees use a special flight strategy that rapidly fall down firstly and then keep a stable path and quickly land on the ground. This flight strategy increases the risk of injury but offers many benefits to them, such as rapidly falling down to the ground before the hive to avoid heavy traffic in front of the entrance and reducing energy consumption.
When comparing the vertical landing behaivour of these four groups, all load-bearing groups had significantly higher vertical landing velocities in the upper space compared to the control (Fig. 5A), indicating that load-bearing tasks could dramatically affect honeybee flight behaviour. The 20 mg group could rapidly decrease their vertical landing velocity before reaching to the entrance, whereas the 40 mg group kept a much higher vertical landing velocity but could still reduce it into a regular into a regular speed and landed smoothly (Fig. 5). However, the 60 mg group kept a high vertical landing velocity over 0.2 m/s through the whole landing process (Fig. 5) and hit onto the ground.
Consequently, this study clearly demonstrated that honeybees are able to adjust various smart flight strategies to adapt different load-bearing states. Although the bees’ landing process seems quite simple, our results revealed an extraordinary capability of honeybees on flight control under different load-bearing tasks. As an ideal model for aerodynamic and bionic aircraft studies, this study not only enriches our understanding on the flight-controlling ability of honeybees, but also provides scientific reference for future research into flight modes of micro air vehicles under different load states.