The formation of muscle scars in articulate brachiopods

Abstract

Distinct impressions (muscle scars) commonly mark the sites of attachment of muscle bases on the interiors of both brachial and pedicle valves of articulate brachiopods. Such impressions are formed as a result of modifications in the fine structure and secretory behaviour of outer epithelial cells (responsible for shell secretion) to which the muscles become attached. Muscles are not attached directly to outer epithelium but are separated from it by a very thin layer of connective tissue. In outer epithelial cells underlying muscle bases the two most apparent changes in cell morphology, compared with epithelial cells unaffected by muscle attachment, are a reduction in optimum cell dimensions and the development of a fibrillar supporting framework (tonofibrils) which extends between the inner and outer plasma membranes. As each muscle base enlarges during ontogeny, outer epithelial cells in the path of the advancing muscle base are progressively overlapped. Below the arcuate anterior margin of the muscle base cell division takes place in the outer epithelium. Changes in secretory behaviour are equally drastic. Around the arcuate anterior margins of scars the standard secondary shell mosaic is replaced by a much more irregular deposit (myotest). Evidence of a zone of vigorous cell division within the associated outer epithelium can be seen in the way that smooth spatulate terminal faces, once they become incorporated within the periphery of scars, split up into two or three minor lobate branches. In addition cell division is accompanied by an increase in organic exudation and a corresponding decrease in mineral secretion. Whereas normal shell secretion involves the exudation of a single organic membrane across an arcuate zone in the anterior part of each secreting plasmalemma and calcite secretion across the remaining surface area, epithelial cells underlying muscle bases exude two thin triple unit membranes which ensheath each individual myotest fibre. The calcite secretory zone is restricted to a narrow central zone on each secreting plasmalemma and the second organic membrane is exuded over the posterior sector and continues posteriorly to join up with the anterior membrane in the cell behind. In some scars, adjacent fibres may amalgamate to produce a localized laminar fabric. In at least one rhynchonellid genus, Notosaria nigricans , mineral secretion under muscle bases may periodically cease with the development of a relatively thick organic layer. Within a species the morphology of exposed parts of fibres in any one muscle scar tends to be fairly consistent and generally each muscle base imparts to the underlying shell a characteristic fabric which can be readily distinguished from that of neighbouring scars. In an initial survey of a number of unrelated genera ultrastructural modifications within homologous muscle scars were found to exhibit a fair degree of similarity. The fact that homologous muscles perform basically the same function would account for this structural similarity. In general it is evident that disruptions and modifications of the standard secretory regime associated with the emplacement of muscle bases arise in response to a need for stronger adhesion between the shell and outer epithelium. Such additional adhesion as is required is facilitated by the widespread exudation of organic membranes to which each outer epithelial cell can remain firmly attached by strong hemidesmosomal connections. The dense framework of tonofibrils extending between the inner and outer plasma membranes serves to brace the cells internally against external stresses applied during muscle contraction. The recognition of myotest fabrics in fossil genera which are closely comparable with the myotest fabrics of living articulates would seem to indicate that similar localized disruptions in secretory behaviour occurred also in the geological past.