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Biomechanics of adhesion in sea cucumber cuvierian tubules (echinodermata, holothuroidea)1

Integrative and Comparative Biology,  Dec 2002  by Flammang, Patrick,  Ribesse, Je ro me,  Jangoux, Michel

SYNOPSIS. Several species of sea cucumbers, all belonging to a single family, possess a peculiar and specialized defense system, the Cuvierian tubules. It is mobilized when the animal is mechanically stimulated, resulting in the discharge of a few white filaments, the tubules. In seawater, the expelled tubules lengthen considerably and become sticky upon contact with any object. The adhesiveness of their outer epithelium combined with the tensile strength of their collagenous core make Cuvierian tubules very efficient at entangling and immobilizing most potential predators. We have designed a method to measure the adhesion of holothuroid Cuvierian tubules. Tubule adhesive strength was measured in seven species of sea cucumbers belonging to the genera Bohadschia, Holothuria and Pearsonothuria. The tenacities (force per unit area) varied from 30 to 135 kPa, falling within the range reported for marine organisms using non-permanent adhesion. Two species, H. forskali and H. leucospilota, were selected as model species to study the influence of various factors on Cuvierian tubule adhesive strength. Tubule tenacity varied with substratum, temperature and salinity of the seawater, and time following expulsion. These differences give insight into the molecular mechanisms underlying Cuvierian tubule adhesion. Tenacity differences between substrata of varying surface free energy indicate the importance of polar interactions in adhesion. Variation due to temperature and time after expulsion suggests that an increase of tubule rigidity, presumably under enzymatic control, takes place after tubule elongation and reinforces adhesion by minimizing peeling effects.

INTRODUCTION

Cuvierian tubules are peculiar organs found in several species of holothuroids (sea cucumbers), all belonging exclusively to the family Holothuriidae (Smiley, 1994; Lawrence, 2001). Two main types of Cuvierian tubules can be distinguished, smooth and lobulated (Lawrence, 2001). The smooth tubules occurring in holothuroids of the genera Bohadschia, Holothuria and Pearsonothuria are expelled as sticky white threads that function in defense against predators (VandenSpiegel and Jangoux, 1987; Hamel and Mercier, 2000). On the other hand, the lobulated tubules occurring in holothuroids of the genus Actinopyga are never expelled and are not sticky (VandenSpiegel and Jangoux, 1993). The question remains, therefore, whether these tubules also function defensively (Lawrence, 2001).

Smooth Cuvierian tubules occur in great numbers (between 200 and 600 in H. forskali; VandenSpiegel and Jangoux, 1987) in the posterior part of the body cavity of the holothuroid. Proximally they are attached to the basal part of the left respiratory tree and their distal, blind ends float freely in the coelomic fluid. When irritated, the sea cucumber directs its aboral end toward the stimulating source and undergoes a general body contraction (Fig. 1). The anus opens, the wall of the cloaca tears, and the free ends of a few tubules (usually 10 to 20 in H. forskali; VandenSpiegel and Jangoux, 1987), together with coelomic fluid, are expelled through the tear and the anus. As water from the respiratory tree is forcefully injected into their lumen, the emitted tubules elongate up to 20 times their original length (VandenSpiegel and Jangoux, 1987). Upon contact with any surface, the elongated tubules instantly are sticky. The adhesiveness of Cuvierian tubules combined with their tensile strength make them very efficient at entangling and immobilizing most potential predators (VandenSpiegel and Jangoux, 1987; Hamel and Mercier, 2000). Finally, the expelled tubules autotomize at their attachment point on the left respiratory tree and are left behind as the holothuroid crawls away (VandenSpiegel and Jangoux, 1987). After expulsion and autotomy, Cuvierian tubules are readily regenerated. The regeneration of a complete set of tubules takes 15 to 18 days in H. leucospilota (Hamel and Mercier, 2000) and about five weeks in H. forskali (VandenSpiegel et al, 2000). Smooth Cuvierian tubules thus constitute an efficient defensive mechanism. Their large number, sparing use and regeneration dynamics make them a formidable line of defense (Hamel and Mercier, 2000; VandenSpiegel et al., 2000).

Most of the ultrastructural information available on Cuvierian tubules comes from VandenSpiegel and Jangoux (1987), who clarified much of the structure and function of these organs in the temperate species Holothuria forskali. The tubules consist of, from the inside to the outside, an inner epithelium surrounding the narrow lumen, a thick connective tissue layer and a mesothelium lining the surface of the tubule that is exposed to the coelomic cavity. The inner epithelium consists of cells enclosing large heterogeneous spherules composed of proteinic and glucidic fractions (Guislain, 1953; VandenSpiegel and Jangoux, 1987).

The connective tissue layer encloses up to six imbricated collagen helices, each of them being parallel to the long axis of the tubule. It also includes longitudinal and circular muscle fibers. The mesothelium is the tissue layer responsible for adhesion. In quiescent tubules, it is a pseudostratified epithelium made up of two superposed cell layers, an outer layer of peritoneocytes and an inner layer of granular cells which is highly folded along the long axis of the tubule. Granular cells are filled with densely packed membrane-bound granules enclosing a proteinaceous material (Endean, 1957; VandenSpiegel and Jangoux, 1987). During elongation, the structure of the Cuvierian tubule is modified (VandenSpiegel and Jangoux, 1987). The inner epithelium is dissociated and the spherule contents are released, the helices of collagen fibers in the connective tissue layer are stretched, and, at the level of the mesothelium, the protective outer layer of peritoneocytes disintegrates and the granular cell layer, now unfolded, thus becomes outermost on the tubule. Granular cells empty the contents of their granules when the elongated tubule comes into contact with a surface, resulting in adhesion (VandenSpiegel and Jangoux, 1987; De Moor et al, 2003).