Feeding strategy, morphological specialisation and presence of bacterial episymbionts in lepetodrilid gastropods from hydrothermal vents

Hydrothermal vent gastropods use diverse feeding mechanisms and can gain nutrition from symbionts. The Juan de Fuca Ridge limpet Lepetodrilus fucensis forms conspicuous stacks in hydrothermal flows and hosts filamentous bacterial episymbionts on its gill. The present study investigates whether its feeding strategy differs from those of several Lepetodrilus species without epibionts. A comparative approach was used to detect morphological features of the gill and digestive tissues that would indicate feeding specialisation. The gill lamellae of L. fucensis possess distinct features that are shared by several suspension-feeding gastropod genera: dense spacing of enlarged, unattached lamellae that do not narrow towards the tip and are stabilised by ciliary junctions. These modifications increase surface area and fluid velocities across the gill. Furthermore, the radular ribbon length, tooth cusp area and stomach volume of adult L. fucensis are significantly reduced, indicating that grazing may not be as efficient a feeding mechanism in comparison to non-symbiotic Lepetodrilus. Next, the feeding abilities of L. fucensis were evaluated using carmine red as a tracer for particle uptake in shipboard pressure vessels. Occasional grazing and active suspension feeding were documented. Dissections of animals and microscopy revealed that bacterium-like filaments accumulate at the lamellar tips, are formed into a cylindrical mass that is moved by cilia to the neck, and are sorted into accepted (passes to the mouth) and rejected material. The morphological specialisations of L. fucensis gills allow effective processing of suspended particles and provide a pathway whereby the episymbionts can be cultivated and ingested. The reduction in the radula and stomach are consistent with the hypothesis that adult L. fucensis primarily suspension feed and/or farm their gill symbionts. However, in peripheral locations, where suspended particle concentrations and chemical fluxes are low, grazing may be the only feasible option. Thus, L. fucensis can survive in a variety of habitats by using multiple feeding mechanisms.