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First published online June 15, 2007
Journal of Experimental Biology 210, v (2007)
Copyright © 2007 The Company of Biologists Limited
doi: 10.1242/jeb.000844
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HOVERING IN THE DARK
University of Guelph dfudge{at}uoguelph.ca
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In spite of the huge selective advantages that it can give an animal, powered flight has evolved only four times in the history of life on Earth: in insects, pterosaurs, birds and bats. One of the things that makes powered flight complex in animals is that it has to be accomplished via flapping, which generates inherently unsteady aerodynamic forces as the wings move back and forth. These challenges are greatest for hovering animals, which require an intricate feedback system to remain in one place. In dragonflies, flight stability is probably accomplished using visual feedback from the eyes. In other insect groups, one pair of wings has been modified into a pair of club-shaped structures called halteres. These structures allow two-winged insects such as flies and mosquitoes to detect rotational movements of their bodies, which is critical for the maintenance of flight stability in the face of external perturbations like gusts of wind.
In a recent article in Science, Sanjay Sane and colleagues ask the question of how moths achieve flight stability in the absence of both visual cues and halteres, since moths fly in low-light conditions and have two pairs of functional wings. In this paper, they test the hypothesis that hawkmoths (Manduca sexta), which are excellent hoverers, use their antennae in the same way that flies use their halteres. This hypothesis predicts that moth antennae, like halteres, should vibrate at a rate that is comparable to the wing beat frequency. This is exactly what they found when they used high-speed video to analyze the motion of moth antennae during hovering. By recording from neurons in the base of the antennae, they also demonstrated that antennae are capable of detecting the kinds of mechanical perturbations that they would experience as a result of bodily rotations during hovering flight.
While these experiments showed that the antennae could act as rotation sensors, they did not demonstrate that they actually do. To directly measure the contribution of the antennae to flight stability, the researchers amputated antennae from a group of moths and measured their flight performance. Moths lacking antennae were far more likely to crash to the ground or into the walls of the test chamber, which was compelling evidence that the antennae contribute to flight stability. Antennae are endowed with a rich diversity of sensory neurons that detect not only mechanical input but also chemicals, humidity and temperature. To test whether any of these sensory systems is involved in flight stability, the investigators re-attached antennae with cyanoacrylate glue and found that this rescued flight performance.
These results lead to two important conclusions. The first is that the odor, humidity and temperature sensors are not involved in flight stability, since the axons from these structures were still severed in moths with re-attached antennae, and these moths could still fly. The second is that the mechanical sensors used for flight stability must be located at the base of each antenna, below the point where they were cut. Structures called Johnston's organs are located in this area and are known to detect antennal movements associated with sound perception, so it is likely that the Johnston's organs are also used in flight stability in moths. These findings are interesting because they suggest that although the evolution of powered flight has been a rare event, mechanisms of achieving flight stability have evolved several times in insects using a variety of sensory structures including the eyes, wings and antennae.
References
Sane, S. P., Dieudonné, A., Willis, M. A. and Daniel, T.
L. (2007). Antennal mechanosensors mediate flight control in
moths. Science 315,863
-866.
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