Rapid preflexes in smooth adhesive pads of insects prevent sudden detachment

Abstract

Many insects possess adhesive organs that can produce extreme attachment forces of more than 100 times body weight but they can rapidly release adhesion to allow locomotion. During walking, weaver ants (Oecophylla smaragdina) use only a fraction of their maximally available contact area, even upside-down on a smooth surface. To test whether the reduced contact area makes the ants more susceptible to sudden and unexpected detachment forces, for example, by rain or wind gusts, we investigated the reaction of untethered ants to rapid horizontal displacements of the substrate. Highspeed video recordings revealed that the pad's contact area could more than double within the first millisecond after the perturbation. This contact area expansion is much faster than any neuromuscular reflex and therefore represents a passive 'preflex', resulting from the mechanical properties and geometrical arrangement of the (pre-)tarsus. This preflex reaction protects ants effectively against unexpected detachment, and allows them to use less contact area during locomotion. Contact area expanded most strongly when the substrate displacement generated a pull along the axis of the tarsus, showing that the ants' preflex is direction-dependent. The preflex may be based on the ability of Hymenopteran adhesive pads to unfold when pulled towards the body. We tested Indian stick insects (Carausius morosus), which have smooth pads that lack this motility. Similar to the ants, they showed a rapid and direction-dependent expansion of the contact area mainly in the lateral direction. We propose that the preflex reaction in stick insects is based on the reorientation of internal cuticle fibrils in a constant-volume system, whereas the ants' pad cuticle is probably not a hydrostat, and pad extension is achieved by the arcus, an endoscelerite of the arolium.

Mechanotransduction: use the force(s)

“…f Rapid increase in adhesive contact area in stick insects ( Carausius morosus ) in response to a rapid displacement of the substrate. Adapted from [ 121 ]. g B16 melanoma cell (expressing fluorescent marker for focal adhesions) before and 5 minutes after displacement of cell body by a microneedle (direction shown by arrow), showing growth of peripheral focal contacts in the region opposite the cell body (enlarged in insets), stimulated by tension.…”

“…Passive ‘preflex’ reactions do not depend on the neuromuscular system and thus have the advantage that they can occur extremely rapidly, thereby preventing detachment by unexpected perturbations such as raindrops (Fig. 3f ) [ 116 ].…”

“…That is, cells sense mechanical stresses and convert them into intracellular signaling and biochemical reactions. While preflexes can double the adhesive contact area within less than a millisecond [ 121 ], the active nature of cells’ adhesion reaction implies that it is much slower and occurs within seconds or minutes [ 93 , 122 , 123 ].…”

Biomechanics of shear-sensitive adhesion in climbing animals: peeling, pre-tension and sliding-induced changes in interface strength

“…Many insects, spiders, lizards and tree frogs can climb on plants and in the canopy of trees by employing adhesive footpads, which allow them to switch between strong attachment and effortless detachment within fractions of a second [1,2,3,4]. The functional principles underlying this impressive dynamic control of attachment forces have attracted considerable interest amongst physicists, engineers and biologists, aiming to develop technical adhesives with similar properties [5].…”

Non-visually-guided distance perception depends on matching torso fluctuations between training and test

“…Of course, the signals travel through neural tracts in humans, but postural adaptations occur faster than neural transmission allows in multicellular organisms much smaller than humans posing shorter neural distances to traverse (e.g., Endlein & Federle, 2013) but also in humans, supporting quiet standing (Marsden, Merton, & Morton, 1983), speech (Kelso, Tuller, Vatikiotis-Bateson, & Fowler, 1984), and hopping (Moritz & Farley, 2004). The connective tissues constitute a hierarchically organized network of small prestressed structures (e.g., at the level of actin filaments composing a single cell's skeleton) nested within larger prestressed structures (e.g., extracellular matrix) nested within yet larger pre-stressed structures (e.g., the fascial encasings around muscles and joints).…”