The role of the excavating sponge Cliona celata in oyster shells

Abstract

Excavating sponges are the most common and destructive macro-eroders present in carbonate dominated habitats, such as coral- and oyster reefs. These sponges penetrate in carbonate skeletons and shells, forming a complex network of tunnels and chambers. In temperate climates, their presence can pose a threat to services provided by oyster reefs due to weakening and damaging the oyster shells, which in the long term leads to loss of the reef structure. Sponge bioerosion proceeds by a combination of chemical dissolution and mechanical chip removal. However, the exact chemical conditions during sponge bioerosion are largely unknown. Here, we provided insights into the bioeroding mechanism of Cliona celata present in oyster shells collected from the Grevelingenmeer and the Oosterschelde, The Netherlands. By growing C. celata on pieces of Iceland spar (a pure transparent form of crystalline calcium carbonate) the conditions of dissolution at the sponge-CaCO3 interface were investigated. Using a pH fluorescent probe followed by fluorescence microscopy, we were able to show that the intracellular pH at this interface is lower compared to ambient seawater. This suggests active proton pumping and release of low proton bundles, to be responsible for creating an acidic microenvironment and hence promoting dissolution of CaCO3. Using a model based on the linear Heat-Diffusion equation, we estimated a local proton flux of 3.02 x 10-8 mol dm-2 s-1 towards the edge of the sponge tissue where etching takes place. Additionally, using scanning electron microscopy we showed that bioerosion by C. celata occurs in successive phases; from dissolution of lattice deficiencies, to etching marks that over time form well-developed pitted holes/tunnels and chips. This study adds to the understanding of the mechanisms that drive sponge bioerosion and provides more insight on how environmental conditions can affect calcium carbonate dissolution by excavating sponges as well as making predictions about future rates of sponge activity.