Structure and Formation of the Egg Capsule Tendrils in the Dogfish Scyliorhinus canicula

Abstract

The tendrils of the egg capsule of the dogfish Scyliorhinus canicula appear to act as damped springs which become entagled with one another, attaching the capsule firmly to the seaweed Halidrys siliquosa. The present paper describes the structure of tendrils and their method of formation in a specialized region of the nidamental gland which we have termed the tendril-forming region (TFR). The tendrils provide a unique system for studying the assembly of a complexly ordered collagenous material. Tendrils show primary twisting and then undergo secondary helical coiling. In cross section they have a lamellated, spiral construction. Each lamella appears to consist of a broad and a narrow lamina. Collagen fibril orientation is approximately longitudinal in the broad lamina and approximately circumferential in the narrow one. Fine, longitudinal fluid-filled canaliculi lie between the lamellae and may act as shock absorbers. Spherical granules containing a high concentration of tyrosine residues are present in large numbers in the outermost lamellae and may have rubber-like properties. The collagen is probably heavily cross-linked and gives the tendril high tensile strength. The tendril appears to be formed from the adhesion of successive lamellae which are wrapped round a central core as the forming tendril undergoes counter-clockwise (left-handed) rotation within the TFR. The latter appears to represent a modification of the structure of the simpler capsule wall-forming region (CWFR). A wave of progressive activation of tubular glands of the TFR travelling anteriorly followed by a wave of deactivation in the opposite direction appears to be responsible for the secretion of first the posterior tendril, then the marginal rib of the egg capsule and finally the anterior tendril. Secreted material passes from glandular tubules through secretory ducts to a series of parallel transverse grooves which act as complex extrusion dies to form the lamellae of the tendril. We have gone some way towards describing how the complex three-dimensional organization of the tendril is produced by these dies. Observations suggested the following sequence of events within the extrusion dies: secreted material becomes uniaxially oriented in the secretory duct and is then passed between ciliated plates we have termed `baffle plates'. These separate the material into an anterior flow containing vertically oriented collagen molecules and a thinner posterior flow containing approximately horizontally oriented ones. These two flows then pass through a transverse groove to become respectively the broad and the narrow lamina of a single lamella of the tendril. The lamellae become pleated within the transverse grooves probably by anisotropic shrinkage. The canaliculi appear to be formed by the partial adhesion of the pleated lamellae as they are wound onto the forming tendril by rotation within the TFR. The mechanism of rotation of the forming thread and its subsequent coiling in the posterior oviduct is discussed.