Abstract

Many insects actively explore their near-range environment with their antennae. Stick insects (Carausius morosus) rhythmically move their antennae during walking and respond to antennal touch by repetitive tactile sampling of the object. Despite its relevance for spatial orientation, neither the spatial sampling patterns nor the kinematics of antennation behavior in insects are understood. Here we investigate unrestrained bilateral sampling movements during climbing of steps. The main objectives are: (1) How does the antennal contact pattern relate to particular object features? (2) How are the antennal joints coordinated during bilateral tactile sampling? We conducted motion capture experiments on freely climbing insects, using steps of different height. Tactile sampling was analyzed at the level of antennal joint angles. Moreover, we analyzed contact patterns on the surfaces of both the obstacle and the antenna itself. Before the first contact, both antennae move in a broad, mostly elliptical exploratory pattern. After touching the obstacle, the pattern switches to a narrower and faster movement, caused by higher cycle frequencies and lower cycle amplitudes in all joints. Contact events were divided into wall- and edge-contacts. Wall contacts occurred mostly with the distal third of the flagellum, which is flexible, whereas edge contacts often occurred proximally, where the flagellum is stiff. The movement of both antennae was found to be coordinated, exhibiting bilateral coupling of functionally analogous joints [e.g., left head-scape (HS) joint with right scape-pedicel (SP) joint] throughout tactile sampling. In comparison, bilateral coupling between homologous joints (e.g., both HS joints) was significantly weaker. Moreover, inter-joint coupling was significantly weaker during the contact episode than before. In summary, stick insects show contact-induced changes in frequency, amplitude and inter-joint coordination during tactile sampling of climbed obstacles.

Highlights

  • The tactile sense provides important sensory cues about the near-range environment, with detailed information about shape, location, and surface properties of touched objects, not all of which is accessible to other senses, including surface texture and stiffness

  • We report how climbing insects sample the obstacle climbed, and how the antennal movement pattern changes during tactile sampling

  • In most of the contact events shown, both antennal joint angles reach a local minimum soon after onset of contact, indicating that all antennal joints tended to switch to levation upon tactile contact. This is similar to the situation in unilateral sampling of vertical objects as reported by www.frontiersin.org height 19 mm height 32 mm Active tactile sampling during step-climbing height 66 mm HS joint 120

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Summary

Introduction

The tactile sense provides important sensory cues about the near-range environment, with detailed information about shape, location, and surface properties of touched objects, not all of which is accessible to other senses, including surface texture and stiffness. Animals that operate under difficult lighting conditions, for example nocturnal or aquatic animals, use their tactile sense to acquire vital information about the surrounding environment Harbor seals use their whiskers to detect subtle currents of water flow, collecting hydrodynamic information about other aquatic animals (prey, predators, or conspecifics; Dehnhardt et al, 1998; Miersch et al, 2011). Shrews use their vibrissae to catch prey in demanding environments, for example hunting insects in complete darkness or underwater. Rats can tactually localise objects (Ahissar and Knutsen, 2008) and discriminate fine-scale surface textures (Diamond et al, 2008; Morita et al, 2011)

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