Larval Adhesive Organs

For most echinoderms, metamorphosis transforms a bilaterally symmetrical and pelagic larva into a radially symmetrical and benthic postmetamorphic individual. Settlement always takes place during the so-called perimetamor-

phic period (Gosselin and Jangoux 1998; Haesaerts et al. 2003), but either before or after the metamorphic stage according to the class considered (Strathmann 1978). In both cases, adhesive organs attach either the competent larva or the postlarva to the substratum during settlement. In three of the five extant echinoderm classes, these organs are the tube feet, viz. the five primary tube feet of competent echinoplutei in echinoids, the five primary tentacles (and, for some species, two posterior tube feet) of pentactulae in holothuroids, the five primary tube feet and the five first pairs of tube feet of ophiuroid postlarvae (Strathmann 1978). These tube feet are similar in structure and function to tube feet of adults (Cameron and Fankboner 1984; Flammang et al. 1998b). Larval adhesive organs of crinoids and asteroids are, on the other hand, unique and have no equivalent in the postmetamorphic stage (Strathmann 1978).

The perimetamorphic period of crinoids comprises three stages: the dolio-laria (free-swimming larval stage), the cystidean (attached metamorphic stage) and the pentacrinoid stages (attached postlarval stage) (Mladenov and Chia 1983; Lahaye and Jangoux 1987; Nakano et al. 2003). Competent doliolar-iae are small barrel-shaped larvae. They possess an attachment complex at their anterior end which consists of a ciliary cap surrounding an apical tuft of elongated cilia and a ventrally located and slightly depressed adhesive pit (Fig. 3A,B). The ultrastructure of this attachment complex has been studied in comatulids (Chia et al. 1986; Jangoux and Lahaye 1990). It is strictly epidermal and made up of elongated ciliated cells associated with a thick basiepidermal nerve plexus. The four cell types forming the complex are sensory cells, covering cells and two types of secretory cells. Sensory cells and secretory cells of the first type occur exclusively in the ciliary cap. The former bear a long vibratile cilium whereas the latter are filled with secretory granules, which contain a flocculent mucopolysaccharidic material. Secretory cells of the second type are restricted to the adhesive pit where they are the most abundant cell type. These cells are filled with secretory granules with an electron-dense fibrillar proteinaceous content. At the beginning of the settlement phase, the doliolaria becomes demersal and brushes the substratum with its apical tuft (sensory structure) (Mladenov and Chia 1983; Lahaye and Jangoux 1988). This implies the occurrence of a mechanism allowing the larva to combine loose adhesion to the substratum with movement. This transitory adhesion is achieved by the combined action of the secretory cells of the ciliary cap which produce a thin mucous film retaining the larva at the water-substratum interface, and of the covering cells whose cilia beat in this mucus (Jangoux and Lahaye 1990; Flammang 1996). When reaching a suitable site, the larva stops moving and turns itself round to have its body directed obliquely (the adhesive pit facing the substratum). It then becomes permanently fixed and transforms into a cystidean larva (Mladenov and Chia 1983; Lahaye and Jangoux 1988). Permanent adhesion starts with the release of the proteinaceous cement by the secretory cells of the adhesive pit and continues during both cystidean and pentacrinoid stages (Chia et al. 1986; Jangoux and Lahaye

Fig. 3A-C. Larval adhesive organs of crinoids and asteroids. SEM photographs of the dolio-laria larva of Antedon bifida (A) and of its anterior adhesive pit (B) (from Lahaye 1987), and of the brachiolaria larva of Asterias rubens (C) (original). AD Adhesive disc; AdP adhesive pit; AP apical papilla; AT apical tuft; CC ciliary cap; LBA lateral brachiolar arm; LP lateral papilla; M mouth; MBA median brachiolar arm; PL preoral lobe; V vestibule; 1-4 ciliary bands

Fig. 3A-C. Larval adhesive organs of crinoids and asteroids. SEM photographs of the dolio-laria larva of Antedon bifida (A) and of its anterior adhesive pit (B) (from Lahaye 1987), and of the brachiolaria larva of Asterias rubens (C) (original). AD Adhesive disc; AdP adhesive pit; AP apical papilla; AT apical tuft; CC ciliary cap; LBA lateral brachiolar arm; LP lateral papilla; M mouth; MBA median brachiolar arm; PL preoral lobe; V vestibule; 1-4 ciliary bands

1990). After development of the cirri during this last stage, the juvenile detaches from its cemented stalk (Lahaye and Jangoux 1987).

Competent larvae in asteroids are called brachiolariae because they possess a specialized attachment complex on their anterior part comprising three bra-chiolar arms and an adhesive disc (Fig. 3C; Barker 1978; Haesaerts et al. 2003). Brachiolar arms are hollow tubular structures occupied by an extension of the larval anterior coelom. Their histological organization comprises four tissue layers: an inner myomesothelium, a connective tissue layer, a subepidermal nerve plexus and an outer epidermis. Each brachiolar arm is tipped by several sensory-secretory areas named papillae, where both the epidermis and the nerve plexus are greatly thickened. The papillary epidermis encompasses three types of secretory cells (cell types A, B and C), sensory cells and support cells (Barker 1978; Haesaerts et al. 2005). Type A and B secretory cells are numerous and occupy most of the volume of the papilla, while type C secretory cells are scarce and occur only at the base of the papilla. Type A secretory cells bear an apical cilium and contain large ovoid granules that enclose an electron-dense heterogeneous material staining histochemically as neutral mucopolysaccharides. Type B secretory cells bear a subcuticular cilium and are filled with small granules containing a homogeneous electron-dense material. The adhesive disc is a round, concave structure lying between the brachiolar arms. It is an epidermal structure composed of two main cell types: ciliated secretory cells and support cells (Barker 1978; Haesaerts et al. 2005). The former are full of large secretory granules enclosing a fibrous pro-teinaceous content of woven aspect. When exploring the substratum, the competent larva orients itself ventral side down and successively attaches and detaches its brachiolar arms (Barker 1978; Strathmann 1978; Haesaerts et al. 2003). Papillae, when making contact with the substratum, are responsible for sensory testing and temporary adhesion. Like adult tube feet, they function as a duo-glandular system, with type A and B secretory cells acting as adhesive and de-adhesive cells, respectively (Hermans 1983; Flammang 1996; Hae-saerts et al. 2005). In addition, the contents of type A secretory cells cross-react with antibodies raised against tube foot adhesive of A. rubens, indicating that adhesives from both brachiolar arms and podia are related to each other and probably share identical molecules, or, at least, identical epitopes on their constituents (Haesaerts et al. 2005). Once the larva has found a suitable site for metamorphosis, brachiolar arms are gradually splayed out, enabling the disc to release its cement (Barker 1978; Haesaerts et al. 2003). This attaches the larva permanently to the substratum and marks the onset of the meta-morphic stage. During this stage, tube feet become functional and ultimately help the newly formed postlarva to detach from the cemented disc (Haesaerts et al. 2003).

Among marine invertebrates, crinoids and asteroids are unique in using non-permanent adhesion during settlement (transitory adhesion for the doliolariae and temporary adhesion for the brachiolariae), permanent adhesion for fixation during metamorphosis, and then reversing to non-permanent adhesion for their whole postmetamorphic life (mechanical attachment for the comatulids and temporary adhesion for the asteroids). Indeed, in general, invertebrates that remain mobile as adults use a single type of adhesion throughout their perimetamorphic period. For example, during settlement, pediveligers of gastropod molluscs adhere to the substratum through a viscous film of mucus produced by their foot on which they creep (transitory adhesion; Koehl and Hadfield 2004). This type of adhesion is then conserved up until the adult form (Walker 1987). Sessile invertebrates, on the other hand, cannot rely on a single type of adhesion during their perimetamorphic period. These organisms, which as adults use permanent adhesion and live cemented to the substratum, need a non-permanent type of adhesion during settlement to enable them to move around while exploring the substratum (Crisp 1984). For premetamorphic attachment, they can therefore use either transitory adhesion like bryozoan larvae or temporary adhesion like barnacle cyprids. From meta-morphic attachment onwards, all these organisms then rely on permanent adhesion to remain cemented to the substratum (Crisp 1984).

Adhesion strength of marine invertebrate larvae is difficult to measure due to the small size of these organisms. It can be estimated, however, from the water current required to wash larvae off a glass substratum. Using this technique, the nominal wall shear stress needed to dislodge temporarily attached individuals of the asteroid Asterina gibbosa was about 1 Pa for brachiolariae attached by the arms and 6 Pa for postmetamorphic individuals attached by tube feet (Haesaerts, Callow and Flammang, unpubl. data). These values are comparable to those required to dislodge newly settled barnacle cyprids (0.2-8.7 Pa) and nudibranch larvae (4.26 Pa) (Koehl and Hadfield 2004). On the other hand, a nominal wall shear stress of about 40 Pa was needed to detach metamorphic larvae of A. gibbosa permanently attached by the disc (Haesaerts, Callow and Flammang, unpubl. data), showing the very high adhesive strength of this permanent adhesive.

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