Combining the senses: Looking at the interaction of wind and vision on a honeybee’s streamlining
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1
University of Queensland, Queensland Brain Institute, Australia
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2
Queensland University of Technology, Science and Engineering Faculty, Australia
In their flight through the world, honeybees are exposed to complex combinations of sensory cues. For example, the bee perceives at least two sources of velocity information -- derived from optic flow, and from air flow -- that it can use to control its flight. As these cues can even conflict if a gust of wind blows over the insect, reliable integration of information from the two senses poses a challenge.
To investigate how honeybees combine information from vision and air flow to control flight, we used a virtual reality flight simulator in which tethered honey bees were exposed to controlled combinations of moving visual stimulus, and air flow. The insect’s abdomen angle was used as an indicator of its perception of the strength of the combined stimuli. In the absence of wind, honeybees actively raise their abdomens as the rate of optic flow simulating forward flight increases, apparently attempting to streamline the body’s posture to reduce energy consumption. Optic flow is required to elicit sustained flight in tethered bees. With only wind stimulation, bees are not guaranteed to fly, and are unlikely to hold a stable abdomen position.
When exposed to optic flow and wind concurrently, wind speed was generally found to combine additively with optic flow, resulting in higher abdomen positions as wind speed increased, until a plateau was reached at a wind speed of 3 m/s. The wind-evoked component of the response would aid the honeybee to further reduce energy consumption for flight through streamlining. Experiments with freshly deceased bees show that the wind-evoked raising of the abdomen is mediated by sensory mechanisms, and unlikely to be caused by passive, drag-induced lift. However, the curve of abdomen pitch versus wind speed (for any given optic flow) is complex, showing a minimum, at around 1.5 m/s, flanked by two maxima (at 0.5 and 2.5 m/s), suggesting that this response may serve additional purposes to streamlining.
Honeybees with amputated antennae or immobilized Johnston’s organs do not modulate their abdomen angle in response to air flow. These bees displayed an elevated response at lower wind speeds, and no minimum at 1.5 m/s. Despite the apparent additive nature of wind and optic flow on the response at high wind speeds in normal bees, this finding indicates that feedback from the antenna acts to inhibit the streamlining response at low wind speeds. Additionally, the streamlining response was also inhibited by vertical optic flow, directed upwards or downwards. This suggests that, under certain conditions, there are other reasons for lowering the abdomen (e.g. the presence of turbulence in the air flow) that may have a higher priority than reducing energy consumption.
Surprisingly, although wind results in the abdomen being raised at high wind speeds, it actually inhibits the response at low wind speeds. These findings reveal the importance of exposing tethered insects to the broad range of sensory modalities that they normally experience during flight, as multiple sensory inputs may act to regulate even seemingly straight-forward responses, such as streamlining.
Acknowledgements
This work was supported partly bygrants from theARC Special Research Initiative on Thinking Systems (TS0669699), the ARC Centre of Excellence in Vision Science (CE0561903), and by a Queensland Smart State Premier’s Fellowship.
References
Luu, T., Cheung, A., Ball, D. and Srinivasan, M. V. (2011) Honeybee flight: a novel 'streamlining' response. Journal of Experimental Biology 214, 2215-2225
Keywords:
insect flight,
Mechanosensation,
Streamlining,
virtual reality,
Vision
Conference:
Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.
Presentation Type:
Poster (but consider for participant symposium and student poster award)
Topic:
Sensorimotor Integration
Citation:
Taylor
G,
Luu
T,
Ball
DM and
Srinivasan
M
(2012). Combining the senses: Looking at the interaction of wind and vision on a honeybee’s streamlining.
Conference Abstract:
Tenth International Congress of Neuroethology.
doi: 10.3389/conf.fnbeh.2012.27.00192
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Received:
29 Apr 2012;
Published Online:
07 Jul 2012.
*
Correspondence:
Mr. Gavin Taylor, University of Queensland, Queensland Brain Institute, Brisbane, Australia, gavin.taylor@biol.lu.se