Synergy between mechanical injury and toxins triggers the urticating system of marine fireworms

Marine fireworms (Annelida, Amphinomidae) are notorious for their stinging dorsal bristles (notochaetae). In the large-size species Hermodice carunculata, characterized by invasive potential and great predatory ability, notochaetae deter consumers and damage prey. The origin of fireworm defensive and offensive capacities, the mechanism of action of the stinging chaetae, and whether other chemical defenses occur are still uncertain. In the present study, we tested if the urticating system of fireworms is the result of a synergy between mechanical injury, due to notochaetae penetration, and the release of toxins vehiculated. To determine whether and where chemical or structural deterrents were present, different body parts of H. carunculata involved in inter-specific interactions were assayed (i.e. dorsal body wall, gills, dorsal and ventral parapodia). Feeding bioassays were performed to assess palatability against a fish (generalist consumer) and deterrent action on contact with two sea anemones (fireworm prey). In all the assays, only the offers bearing the dorsal chaetae (notochaetae) strongly deterred consumers and induced paralysis in prey. The notochaetae treated with organic solvents lost their deterrence against fish. Besides, the notopodia were palatable to fish and anemones after the removal of the notochaetae. These findings support a powerful synergy between chemical deterrence and physical structure. To date, the only acute inflammation inducer isolated from an amphinomid is “complanine”, a trimethylammonium compound. High-resolution LC-MS/MS and preliminary NMR analyses suggested the presence of complanine-related compounds in the notochaetae. The present results suggest that the release of compounds and their strong deterrent effect should be mediated by mechanical injury. The sharp, fragile and hollow structure of the notochaetae combined with inflammatory substances could support the success of fireworms in marine benthic environments. Further research is required to ascertain the nature and localization of these chemicals in H. carunculata, broadening knowledge on the chemical ecology of amphinomids.