Bridging the gap: wound healing in insects restores mechanical strength by targeted cuticle deposition

Abstract

If an insect is injured, can it repair its skeleton in a manner which is mechanically strong and viable? Previous work has described the biological processes that occur during repair of insect cuticle, but until now, there has been no biomechanical assessment of the repaired area. We analysed the biomechanics of the injury repair process in the desert locust (Schistocerca gregaria). We show that after an incision, a healing process occurred which almost doubled the mechanical strength of locust tibial cuticle, restoring it to 66% of the original, intact strength. This repair process occurred by targeted cuticle deposition, stimulated by the presence of the injury. The cut surfaces remained unrepaired, but a patch of endocuticle was deposited, reinforcing the area and thus increasing the effective fracture toughness. The deposition rate of endocuticle inside the tibia increased fourfold compared with uninjured controls, but only on the dorsal side, where the incision was placed. The limb is highly loaded during jumping, so this partial restoration of strength will have a profound effect on the fitness of the insect. A finite-element model provided insights into the mechanics of the repair, predicting that the patch material reaches its ultimate strength before the fracture toughness of the existing cuticle is exceeded.

Damage, repair and regeneration in insect cuticle: The story so far, and possibilities for the future

“…This is then sclerotized (or tanned) over the next 12 he3 days (Andersen et al, 1996;Hepburn and Joffe, 1974;Chapman, 2013). In experiments conducted after this tanning process was complete, it has been shown (Parle et al, 2016b) that in the first 21 days post moult, the insect deposits cuticle quite rapidly, slowing down after this time period. This rapid deposition undoubtedly serves to reinforce the leg which would be prone to buckling failures early on while still relatively slender (Parle et al, 2016c).…”

“…Much research has been done into the roles played by chemistry (Lai-Fook, 1968;Rowley and Ratcliffe, 1978;Wright, 1987), biology (Wigglesworth, 1937;Locke, 1966;Marmaras et al, 1996;Dillaman and Roer, 1980;Lai et al, 2001) and genetics (Galko and Krasnow, 2004;Belacortu and Paricio, 2011) involved during the wound healing of insects, but how effective are these processes at restoring the original preinjury properties such as strength, stiffness and toughness e crucial for the survival of a limb and the fitness of the insect e to the cuticle? One such study (Parle et al, 2016b) showed that the deposition of a patch of new cuticle underneath a wound is crucial, and can restore the strength of an injured leg to 66% of its original strength. The patch (coloured in green in Fig.…”

“…The smooth surface on the dorsal side (coloured in red) shows the initial scalpel cut (indicated by dashed line). Underneath this is the newly deposited repair cuticle (coloured in green), apparent by the rough fracture surface indicating the separation of normal cuticle during testing (similar to the normal cuticle on the rest of the fracture surface e coloured blue) (Adapted fromParle et al, 2016b).…”

Self‐healing materials: what can nature teach us?

“…This new material can be seen to have fractured during the bending test. It was found that the repair process increased the strength of the damaged leg by about a factor of two, bringing it to about 66% of the strength of the original, intact leg . The repair seems to rely mainly on the effect of the patch material to reduce the stress concentration effect of the cut, although it is also possible that the properties of the material itself may change.…”

Repair of microdamage caused by cyclic loading in insect cuticle

“…This phenomenon has, until now, not been investigated for any other biological material. In our previous work on insect cuticle, we showed that desert locusts are capable of repairing macroscopic damage (O'Neill, DeLandro, & Taylor, , Parle, Dirks, & Taylor, ). We applied scalpel cuts and puncture wounds to the hind tibia, sufficiently large to induce significant loss of strength, and found that repair occurred in the form of targeted cuticle deposition.…”