The roles of vision and antennal mechanoreception in hawkmoth flight control

Abstract

Flying animals need constant sensory feedback about their body position and orientation for flight control. The visual system provides essential but slow feedback. In contrast, mechanosensory channels can provide feedback at much shorter timescales. How the contributions from these two senses are integrated remains an open question in most insect groups. In Diptera, fast mechanosensory feedback is provided by organs called halteres, and is crucial for the control of rapid flight manoeuvres, while vision controls manoeuvres in lower temporal frequency bands. Here we have investigated the visual-mechanosensory integration in an insect which lacks halteres: the hawkmoth Macroglossum stellatarum. They represent a large group of insects that use Johnston’s organs in their antennae to provide mechanosensory feedback on perturbations in body position. High-speed videos of freely-flying hawkmoths hovering at stationary or oscillating artificial flowers showed that positional fidelity during flight was reduced in flagella ablated animals, but was recovered after flagella re-attachment. Our experiments show that antennal mechanosensory feedback specifically mediates fast flight manoeuvres, but not slow ones. Differences in the latency of visual feedback (in different light intensities) affected all antennal conditions equally, suggesting there was no compensatory interaction between antennal and visual feedback under the tested conditions. These results establish the importance of antennal mechanosensors in providing rapid mechanosensory feedback for finer control of flight manoeuvres, acting in parallel to visual feedback.