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, 281 (1779), 20133072

Static Antennae Act as Locomotory Guides That Compensate for Visual Motion Blur in a Diurnal, Keen-Eyed Predator

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Static Antennae Act as Locomotory Guides That Compensate for Visual Motion Blur in a Diurnal, Keen-Eyed Predator

Daniel B Zurek et al. Proc Biol Sci.

Abstract

High visual acuity allows parallel processing of distant environmental features, but only when photons are abundant enough. Diurnal tiger beetles (Carabidae: Cicindelinae) have acute vision for insects and visually pursue prey in open, flat habitats. Their fast running speed causes motion blur that degrades visual contrast, forces stop-and-go pursuit and potentially impairs obstacle detection. We demonstrate here that vision is insufficient for obstacle detection during running, and show instead that antennal touch is both necessary and sufficient for obstacle detection. While running, tiger beetle vision appears to be photon-limited in a way reminiscent of animals in low-light habitats. Such animals often acquire wide-field spatial information through mechanosensation mediated by longer, more mobile appendages. We show that a nocturnal tiger beetle species waves its antennae in elliptical patterns typical of poorly sighted insects. While antennae of diurnal species are also used for mechanosensation, they are rigidly held forward with the tips close to the substrate. This enables timely detection of path obstructions followed by an increase in body pitch to avoid collision. Our results demonstrate adaptive mechanosensory augmentation of blurred visual information during fast locomotion, and suggest that future studies may reveal non-visual sensory compensation in other fast-moving animals.

Keywords: antenna; insect locomotion; motion blur; vision.

Figures

Figure 1.
Figure 1.
Antennal positions during two-step cycles in running tiger beetles (note different timescales in (a) and (b)). Top row: vertical included angle α between the longitudinal body axis and antennal tip. Middle row: horizontal spread angle β between lines from antenna tip through the basal segment. Bottom row: height of the antenna tip above ground (th). (a) Nocturnal O. dejeanii move antennae up and down and from medial to lateral at twice the stepping frequency. (b) Diurnal C. hirticollis holds the antennae in a rigid, downward posture with the tips close to the ground. (c) Vertical antenna angle α of O. dejeanii and C. hirticollis plotted as a function of the horizontal spread angle β. The nocturnal beetles carry out wide elliptical movements, while the diurnal beetle holds its antennae in a steady position. (d) C. hirticollis, measured angles and tip height above ground overlaid. The centroid of the beetle's body image was determined automatically by image analysis (see Methods) and provided a measure of ground clearance of the body (gc). Inset shows antennal spread angle β. (Online version in colour.)
Figure 2.
Figure 2.
Outcomes of obstacle runs (means ± s.d., Ncontrol = 20 beetles, other groups N = 5 beetles; 10 runs per obstacle height for each beetle). ‘Success’ means surmounting of the obstacle without any part of the head coming into contact. ‘Failure’ means that the head contacted the obstacle, stopping the beetle. White and black rectangles indicate low- and high-contrast treatments, respectively. Beetle icons represent unimpaired, blinded and antennectomized beetles. (Online version in colour.)
Figure 3.
Figure 3.
Velocity, pitch angle and ground clearance of beetles during runs on flat ground, before and after covering eyes or clipping antennae (mean ± s.d. control: N = 20 beetles, n = 225 runs; blind: N = 5, n = 46; clipped: N = 10, n = 75); (a,b) treatments had no effect on velocity and body pitch angle (c) antennectomized beetles slightly decreased ground clearance (Kruskal–Wallis test (H = 8.43, d.f. = 2, p = 0.015) followed by comparison with control using Steel method (p = 0.023)).
Figure 4.
Figure 4.
(a–c) Pitch angle and (d–f) ground clearance as function of distance to the ‘high’ obstacle (4 mm). Black line represents mean of all runs in a treatment group (±s.d., grey overlay). Individual run data were offset so that traces started at the same y-value (offset to the mean of the first 4 mm of all runs in the group). Vertical line is the mean of the distance at first contact with the obstacle (±s.d., shaded overlay). Top panels: control group (N = 20 beetles, n = 172 runs), middle panels: blind group (N = 5 beetles, n = 34 runs), bottom panels: antennectomized group (N = 5 beetles, n = 33 runs). (Online version in colour.)

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