Abstract
Sponges thrive in marine benthic communities due to their specific and diverse chemical arsenal against predators and competitors. Yet, some animals specifically overcome these defences and use sponges as food and home. Most research on sponge chemical ecology has characterised crude extracts and investigated defences against generalist predators like fish. Consequently, we know little about chemical dynamics in the tissue and responses to specialist grazers. Here, we studied the response of the sponge Aplysina aerophoba to grazing by the opisthobranch Tylodina perversa, in comparison to mechanical damage, at the cellular (via microscopy) and chemical level (via matrix-assisted laser desorption/ionization imaging mass spectrometry, MALDI-imaging MS). We characterised the distribution of two major brominated alkaloids in A. aerophoba, aerophobin-2 and aeroplysinin-1, and identified a generalised wounding response that was similar in both wounding treatments: (i) brominated compound-carrying cells (spherulous cells) accumulated at the wound and (ii) secondary metabolites reallocated to the sponge surface. Upon mechanical damage, the wound turned dark due to oxidised compounds, causing T. perversa deterrence. During grazing, T. perversa’s way of feeding prevented oxidation. Thus, the sponge has not evolved a specific response to this specialist predator, but rather relies on rapid regeneration and flexible allocation of constitutive defences.
Highlights
Sponges thrive in marine benthic communities due to their specific and diverse chemical arsenal against predators and competitors
A great variety of beautiful opisthobranchs are specialised in living and feeding on one or a narrow range of sponge species. These specialised sea slugs defend themselves by accumulating and modifying the secondary metabolites they acquire from the sponges they e at[4]. Despite these well-known associations, and the extensive literature on sponge chemical defences, we know little about the response of sponges to grazing by these specialists and whether it differs from the response to predation by generalists or wounding
We focused on the fate of spherulous cells, in which brominated compounds are s tored[29], via light and transmission electron microscopy
Summary
Sponges thrive in marine benthic communities due to their specific and diverse chemical arsenal against predators and competitors. Each sponge species produces a specific, yet diverse chemical arsenal with fish-deterrent, antifouling and antimicrobial properties, to name a few[3,4,11,12,13] Despite these chemical defences, a great variety of beautiful opisthobranchs are specialised in living and feeding on one or a narrow range of sponge species. These specialised sea slugs defend themselves by accumulating and modifying the secondary metabolites they acquire from the sponges they e at[4] Despite these well-known associations, and the extensive literature on sponge chemical defences, we know little about the response of sponges to grazing by these specialists and whether it differs from the response to predation by generalists or wounding. These works exemplify that it remains unclear to what extent and under which conditions sponges may show flexible antipredatory defences
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