Shrinking to fit: fluid jettison from a haemocoelic hydrostatic skeleton during defensive withdrawals of a gastropod larva

Abstract

Although most of the basic animal body plans are supported by hydrostatic skeletons consisting of fluid maintained at constant volume, studies on how animals have solved biomechanical scaling dilemmas during evolution of large body size have emphasized cases where skeletons are formed by rigid solids. Larvae of gastropod molluscs swim using ciliated velar lobes supported by a constant volume hydrostatic skeleton. Defensive behaviour involves rapid withdrawal of the velar lobes and foot into a protective biomineralized shell. Some gastropod larvae grow to giant size and the velar lobes enlarge allometrically, but the lobes and foot of many can still withdraw completely into the mineral-stiffened shell. I dyed internal fluid of a large gastropod larva with fluorescein to show that fluid supporting the extended velar lobes is expelled from discrete release sites during defensive withdrawals. Scanning electron microscopy suggested that release sites are distinctive papillae on the upper velar epidermis. Ultrathin sections revealed that branched tracks of microvilli-free membrane on the surface of these papillae were formed by very thin epithelial cells, which may rupture and re-anneal during and after defensive withdrawals. Behaviours facilitated by fluid discharge from a haemocoelic (non-coelomic) body compartment have been rarely reported among aquatic invertebrates, but may be more widespread than currently recognized.