The gizzard plates in the Cephalaspidean gastropod Philine quadripartita: Analysis of structure and function

Cephalaspidean gastropods are common marine mollusks with a unique digestive apparatus containing 3 hardened plates of millimeter size inside the muscular esophageal crop (gizzard). The gizzard plates are reported to either grind or crush shelled prey. The current study aims at better understanding the manner in which the gizzard plates of the cephalaspid Philine quadripartita function in the overall digestion process by relating their structural and mechanical properties. Philine quadripartita possesses 3 gizzard plates which have one of the common configurations of cephalaspidean gizzard plates: two paired plates that are mirror images of each other and one smaller unpaired plate. We used micro-CT to characterize the gizzard musculature, the food which is present at different stages of the digestion process and the working surface of the gizzard plates. We show that the gizzard plates are used to crush the shelled prey, and that the functional mode of the small unpaired plate is different from the larger plates. All 3 plates are composed of a mixture of amorphous calcium carbonate and amorphous calcium phosphate embedded in a chitinous matrix. The proportions of these two mineral phases vary systematically within the plate. The plates have a complex layered structure, whose elastic moduli and hardness also vary in a continuous systematic manner. We observed that the stiffest layer is below the working surface, unlike most teeth where the stiffest layer is at the surface. Rigorous analysis of the elasticity indices of the gizzard plates as compared with sea urchin teeth and synthetic calcite provided insights into the connection between the biological function and the mechanical properties of biological composites. Specifically, we show that materials used for grinding require harder surfaces to avoid excessive wear compared to materials for crushing, whereas both of these functions require high toughness.