The role of lateral optic flow cues in hawkmoth flight control

Abstract

Flying animals require sensory feedback on changes of their body position, as well as on their distance from nearby objects. The apparent image motion, or optic flow, which is generated as animals move through the air, can provide this information. Flight tunnel experiments have been crucial for our understanding of how insects use optic flow for flight control in confined spaces. However, previous work mainly focused on species from two insect orders: Hymenoptera and Diptera. We therefore set out to investigate whether the previously described control strategies to navigate enclosed environments are also used by insects with a different optical system, flight kinematics and phylogenetic background. We tested the role of lateral visual cues for forward flight control in the hummingbird hawkmoth Macroglossum stellatarum (Sphingidae, Lepidoptera), which possesses superposition compound eyes, and has the ability to hover in addition to its capacity for fast forward flight. Our results show that hawkmoths use a similar strategy for lateral position control to bees and flies in balancing the magnitude of translational optic flow perceived in both eyes. However, the influence of lateral optic flow on flight speed in hawkmoths differed from that in bees and flies. Moreover, hawkmoths showed individually attributable differences in position and speed control when the presented optic flow was unbalanced.

A new innovative real-time tracking method for flying insects applicable under natural conditions

“…To test the tracking system on an insect species that has a high maneuverability and vastly different flight speeds within the same flight bouts [ 34 , 35 ], we tracked several individuals of the hummingbird hawkmoth Macroglossum stellatarum . In the free-flight arena, the hawkmoths showed typical exploration and escape behaviour (flying towards the brightest side of the arena, Fig.…”

Ecological Entomology: How Is Gibson’s Framework Useful?

“…Centering and wall following (lateral) "image angular velocity" in [34] "horizontal optic flow cues" in [34] "speed of retinal image motion" in [26] "apparent angular speed" in [26] "lateral optic flow" in [20] "the magnitude of translational optic flow perceived in both eyes" in [23] "translational optic flow cues" in [35] Apis mellifera, Bombus terrestris, Megalopta genalis, Macroglossum stellatarum Speed adjustment (lateral) "image angular velocity" in [11,27] "optic flow cues in the lateral visual field" in [27] "velocity of the perceived image motion" in [27] "rate of optic flow" in [21,27] "image motion signal" in [27] "optic flow cues" in [27] "apparent velocity of the surrounding environment" in [26] "apparent movement of the surrounding patterns relative to themselves" in [10] "retinal slip speed" in [29] Apis mellifera, Bombus terrestris, Drosophila hydei, Drosophila melanogaster Terrain following "ventral optic flow" in [13] "apparent (ventral) speed of image" in [26] "image angular velocity" in [27] "optic flow cues in the ventral region of the visual speed" in [27] "rate of optic flow" in [27] "perceived image velocity of motion of the image" in [27] Apis mellifera Landing on vertical surface "tau: apparent rate of expansion of the image" in [11] "magnitude of optic flow" in [36] "speed of image motion on the retina" in [36] Apis mellifera Landing on horizontal surface "angular velocity of the image" in [11,26] Apis mellifera…”

“…Centering and wall-following tasks: The lateral/frontal parts of the optic flow are useful to center in a narrow corridor by balancing the lateral parts of the optic flow (in honeybees [3,19,20], in bumblebees [15,21], in flies [10,22], in hawkmoths [23]), or to follow a wall along a wide corridor by restoring the optic flow pattern from one side (in honeybees [19,20,24], in bumblebees [25]). Kirchner and Srinivasan [24] suggested "bees maintained equidistance by balancing the apparent angular velocities of the two walls, or, equivalently, the velocities of the retinal images in the two eyes".…”

“…Lecoeur et al [15] found that "lateral position is controlled by balancing the maximum optic flow in the frontal visual field". Stöckl et al [23] found that "hawkmoths use a similar strategy for lateral position control to bees and flies in balancing the magnitude of translational optic flow perceived in both eyes". Serres et al [20] found that "bee follows the right or left wall by regulating whichever lateral optic flow (right or left) is greater".…”

The (Under)Use of Eye-Tracking in Evolutionary Ecology

“…The ability to navigate effectively through the environment underpins the success or failure of all the key survival behaviours, and fundamental eye mechanics, gaze behaviours and navigation strategies are inextricable linked to evolutionary demands [43]. During locomotion optic flow is an important visual signal for direction of movement in many species, including during flight in birds and moths [44,45]. Given that decisions regarding trajectory and route path are made rapidly, we would argue that the temporal resolution provided by eye-tracking is essential in studying locomotion in visually guided animals.…”