Turning the game around: toxicity in a nudibranch-sponge predator–prey association

Abstract

Escalation theory proposes enemy-related selection as the most relevant factor of natural selection among individual organisms. When hazardous to predators, prey might be considered enemies that influence predator evolution. Opisthobranch molluscs that prey on chemically defended prey are an interesting study case on this subject. Predation on chemically defended species paved the way for opisthobranchs to enter in an arms race, developing means to detoxify and/or excrete harmful compounds, which led to the sequestration of those compounds and their self-defensive use, an escalation of defenses. Here we aim to understand whether the opisthobranch predator is better protected than its chemically defended prey, using as predator–prey model, a nudibranch (Hypselodoris cantabrica) and the sponge it preys upon (Dysidea fragilis), and from which it obtains deterrent chemical compounds. Specimens of both species were collected on the Portuguese coast, and their crude extracts were analyzed and used in palatability tests. Nudibranchs revealed a higher natural concentration of crude extract, probably due to a progressive accumulation of the compounds. Both predator and prey extracts revealed similar mixtures of deterrent metabolites (furanosesquiterpenes). Palatability tests revealed a more effective deterrence in the nudibranch extracts because significant rejection rates were observed at lower concentrations than those necessary for the sponge extracts to have the same effect. We concluded that the predator is chemically better protected than its prey, which suggests that its acquisition of chemical defenses reveals a defensive escalation.