Fine structure of the mantle epithelium and shell growth in rhynchonellide brachiopod Hemithiris psittacea

Abstract

Brachiopods are marine benthic invertebrates that secrete a calcitic bivalve shell via mantle epithelia. This study examines the shell and mantle structure of the rhynchonellide Hemithiris psittacea. The shell consists of an organic uppermost sheet, comprising mucopolysaccharide and periostracal layers, and a mineralized part composed of primary and secondary layers. The secondary layer is formed by fibers, enclosed in organic sheaths. We identified distinct mantle epithelial cell types: inner, columnar, oval, lobate, and vesicular cells, as well as two types of outer epithelial cells. Each cell type exhibits ultrastructural features that correspond to putative specialized functions: columnar and lobate cells secrete the mucopolysaccharide layer; the vesicular cells synthesize the periostracum; the first type of outer epithelial cells contributes to primary layer secretion; and the second type produces the fibers of the secondary layer. Oval cells in the mantle groove display undifferentiated morphology, supporting the existence of a putative generative zone in rhynchonellide brachiopods. Our analysis identifies three distinct morphological and functional zones of the shell. The primary zone is the marginal shell region, consisting only of the primary layer. The transitional zone exhibits progressive changes in both fiber morphology and epithelial cell dimensions without constant relative position of cells and fibers, while the stable pattern zone maintains regular cells and fibers arrangement. Based on these findings, we propose regional modifications to the classical conveyor belt model for mantle growth and shell thickening in rhynchonelliform brachiopods. In the transitional zone, several cells may cooperatively secrete fibers and translocate the fiber during synthesis, while in the stable pattern zone each cell produces two adjacent fibers throughout its lifespan. In the posterior zone shell secretion terminates.