Abstract
Insects often release noxious substances for their defence. Larvae of Zygaena filipendulae (Lepidoptera) secrete viscous and cyanogenic glucoside-containing droplets, whose effectiveness was associated with their physical and chemical properties. The droplets glued mandibles and legs of potential predators together and immobilised them. Droplets were characterised by a matrix of an aqueous solution of glycine-rich peptides (H-WG11-NH2) with significant amounts of proteins and glucose. Among the proteins, defensive proteins such as protease inhibitors, proteases and oxidases were abundant. The neurotoxin β-cyanoalanine was also found in the droplets. Despite the presence of cyanogenic glucosides, which release toxic hydrogen cyanide after hydrolysis by a specific β-glucosidase, the only β-glucosidase identified in the droplets (ZfBGD1) was inactive against cyanogenic glucosides. Accordingly, droplets did not release hydrogen cyanide, unless they were mixed with specific β-glucosidases present in the Zygaena haemolymph. Droplets secreted onto the cuticle hardened and formed sharp crystalline-like precipitates that may act as mandible abrasives to chewing predators. Hardening followed water evaporation and formation of antiparallel β-sheets of the peptide oligomers. Consequently, after mild irritation, Zygaena larvae deter predators by viscous and hardening droplets that contain defence proteins and β-cyanoalanine. After severe injury, droplets may mix with exuding haemolymph to release hydrogen cyanide.
Highlights
The cuticular cavity disrupts at its weakest part, i.e. the thin cuticular opening structure (Fig. 1), and a droplet is extruded[16]
Neither specialised muscles nor specific cell types with morphological adaptations are involved in the secretion process, which renders such a defence system quite unique in comparison to other insect defence systems[16]: for example, Chrysomelina leaf beetle larvae possess specialised muscles connected to the secretory gland to control release of defensive secretion[18], and the so-called easy bleeding by sawfly larvae relies on an integument with exceptional low mechanical resistance that ruptures under mechanical stress leading to haemolymph exudation[19]
In Z. filipendulae larvae, defence droplets constitute the main site for accumulation of high concentrations of the two CNglcs linamarin and lotaustralin (~25 μg per μl)[17], which are sequestered from the host plant[20] and/or biosynthesised[21]
Summary
The cuticular cavity disrupts at its weakest part, i.e. the thin cuticular opening structure (Fig. 1), and a droplet is extruded[16]. In Z. filipendulae larvae, defence droplets constitute the main site for accumulation of high concentrations of the two CNglcs linamarin and lotaustralin (~25 μg per μl)[17], which are sequestered from the host plant[20] and/or biosynthesised[21] These CNglc-containing droplets may serve at least two functions in defence against predators: as a deterrent due to their bitter taste and as an active defence due to release of toxic hydrogen cyanide (HCN) by hydrolysing the CNglcs with specific β -glucosidases after tissue damage[22,23]. The absence of a dual toxic/repellent role of HCN may have spurred evolution of additional physical and chemical defences in CNglc-containing secretions This is exemplified by defence droplets in closely related Z. trifolii larvae, which possess strong repellent properties against various vertebrate and invertebrate predators[16,26]. Our study shows that the mode of action of the defence droplets depends on the type of predator as well as on the degree of irritation or injury the larvae are subjected to
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