The biomechanical and neural control of hydrostatic limb movements in Manduca sexta

Abstract

SUMMARY Caterpillars are ecologically successful soft-bodied climbers. They are able to grip tightly to foliage using cuticular hooks at the tips of specialized abdominal limbs called prolegs. The neural control of proleg retraction has been examined in some detail but little is known about how prolegs extend and adduct. This is of particular interest because there are no extensor muscles or any obvious mechanisms for directing hydraulic flow into the proleg. In restrained tobacco hornworms (Manduca sexta),adduction can be evoked by stimulating mechanosensory hairs on the medial surface of the proleg. 3-D kinematics show that extension and adduction occur simultaneously through an unfolding of membrane between the pseudo segments. Hemolymph pressure pulses are not necessary to extend the proleg; instead, the pressure at the base of the proleg decreases before adduction and increases before retraction. It is proposed that these pressure changes are caused by muscles that stiffen and relax the body wall during cycles of retraction and adduction. Electromyographic recordings show that relaxation of the principal planta retractor muscle is essential for normal adduction. Extracellular nerve and muscle recordings in reduced preparations show that medial hair stimulation of one proleg can strongly and bilaterally excite motoneurons controlling the ventral internal lateral muscles of all the proleg-bearing segments. Ablation, nerve section and electromyographic experiments show that this muscle is not essential for adduction in restrained larvae but that it is coactive with the retractors and may be responsible for stiffening the body wall during proleg movements.

The diversity of hydrostatic skeletons

“…The notochord of ascidians, cephalochordates, many larval and adult fish, and frog tadpoles (Adams et al, 1990;Grotmol, 2006;Koob and Long, 2000;Jiang and Smith, 2007) is considered to employ hydrostatic support. Support for movement of many larval insects, whose cuticle is soft and thus generally cannot bear compressive and bending forces, may also depend on a hydrostatic mechanism (Berrigan and Pepin, 1995;Brackenbury, 1999;Casey, 1991;Mezoff et al, 2004), although the mechanical properties of the body wall, air loss from the tracheal system and use of legs make the situation more complex (Lin et al, 2011).…”

Kinematics of horizontal and vertical caterpillar crawling

“…The gripping system is used regardless of the orientation the caterpillar is in. The passive state of the prolegs is in the adducted position with the crochets extended by tonic body pressure and body wall elasticity (Mezoff et al, 2004). Release is achieved by unhooking the crochets and retracting the prolegs by active muscle contraction Mezoff et al, 2004).…”

“…The passive state of the prolegs is in the adducted position with the crochets extended by tonic body pressure and body wall elasticity (Mezoff et al, 2004). Release is achieved by unhooking the crochets and retracting the prolegs by active muscle contraction Mezoff et al, 2004). As the gripping system is equally strong in horizontal and vertical orientation, the hooking and unhooking activities do not lead to differences in the kinematics.…”

A Bio-Inspired Small-Sized Wall-Climbing Caterpillar Robot

“…Caterpillars are among the most successful climbers and can maneuver in complex threedimensional environments, burrow, and hold on to the substrate using a very effective passive grasping system (Mezoff, et al, 2004). They consist of a head and neck part, a body with several segments and a tail end part, as shown in Fig.…”