Tarsal movements in flies during leg attachment and detachment on a smooth substrate

Abstract

In order to understand the attachment mechanism of flies, it is important to clarify the question of how the adhesive pad (pulvillus) builds and breaks the contact with the substrate. By using normal and high-speed video recordings, the present study revealed that pulvilli are positioned on the surface in a particular way. The pulvilli are apparently loaded or pressed upon the substrate after leg contact, as evidenced by splaying of the claws. Detachment of pulvilli from the substrate may be achieved in four different modes depending on the leg (fore-, mid- or hindleg): pulling, shifting, twisting, and lifting. Lifting is the only detachment mode depending on the claws’ action. Kinematics of the tarsal chain is studied in leg preparations, in which the tendon of the claw flexor muscle was pulled by tweezers and video recorded. The morphological background of tarsal movements during attachment and detachment is studied by scanning electron microscopy, fluorescent microscopy, and bright field light microscopy followed by serial semithin sectioning of pretarsal structures. Several resilin-bearing springs are involved in the recoil of the tarsal segments to their initial position, when the tendon is released after pull.

Introduction

Debates about functional mechanisms of the devices which allow insects to adhere to the bottom side of a smooth horizontal surface were held more than one century ago (West, 1862, Dahl, 1884, Rombouts, 1884, Simmermacher, 1884, Dahl, 1885). After the initial discovery that the phenomenon of adhesion is based on the presence of specialized pad-like tarsal structures, the interest in the fly attachment system has been renewed as technical equipment for the analysis of small structures greatly improved. The ultra structure of the fly adhesive pads was studied in detail (Bauchhenß and Renner, 1977, Hasenfuss, 1977, Bauchhenß, 1979, Walker et al., 1985, Gorb, 1998). The pad area (Gorb and Beutel, 2001), presence of an epidermal secretion (Bauchhenß, 1979) in the contact area, and material flexibility (Bauchhenß, 1979, Niederegger et al., 2002) were named as factors enhancing adhesion in the fly attachment system. It was also demonstrated that the fly walking pattern on the ceiling differs from that on the horizontal surface (Niederegger et al., 2002). However, the tarsus kinematics during contact formation and release between the pad and surface remained unclear.

Basically the insect pretarsus is controlled by one flexor muscle (Walther, 1969, Radnikow and Bässler, 1991), which apodeme inserts to the unguitractor plate (Goel, 1972, Gorb, 1996). No antagonist muscle is present in the pretarsus. Elastic elements allow the leg to jump back to its default position after the muscle is relaxed (Gorb, 1996, Frazier et al., 1999). The intention of the present study was to visualize and analyze pretarsus movements during attachment and detachment processes in the fly pads (pulvilli) during free walk on the ceiling. The questions asked were (1) which tarsus movement is required for contact formation between attachment pads and surface; (2) how is the fly able to overcome its own adhesion to detach the leg from the ceiling surface, and (3) what is the morphological background allowing these kinds of movements?