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Adaptations to Benthic Development: Functional Morphology of The Adaptations to Benthic Development: Functional Morphology of the Attachment Complex of the Brachiolaria Larva in the Sea Star Asterina gibbosa Author(s): Delphine Haesaerts, Michel Jangoux, Patrick Flammang Reviewed work(s): Source: Biological Bulletin, Vol. 211, No. 2 (Oct., 2006), pp. 172-182 Published by: Marine Biological Laboratory Stable URL: http://www.jstor.org/stable/4134591 . Accessed: 10/01/2012 03:53 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Marine Biological Laboratory is collaborating with JSTOR to digitize, preserve and extend access to Biological Bulletin. http://www.jstor.org Reference: Biol. Bull. 211: 172-182. (October 2006) ? 2006 Marine Biological Laboratory Adaptations to Benthic Development: Functional Morphology of the Attachment Complex of the Brachiolaria Larva in the Sea Star Asterina gibbosa DELPHINE HAESAERTS', MICHEL JANGOUX1'2, AND PATRICK FLAMMANG2,* Universite Libre de Bruxelles, Laboratoire de Biologie Marine, Acadimie universitaire Wallonie- Bruxelles, Brussels, Belgium; and 2 Universite"de Mons-Hainaut, Laboratoire de Biologie Marine, Acadjmie universitaire Wallonie-Bruxelles,Mons, Belgium Abstract. The asteroid Asterina gibbosa lives all its life of attachment to the substratum.The end of this period in close relation to the sea bottom. Indeed, this sea star correspondsto the complete regression of the externallarval possesses an entirely benthic, lecithotrophic development. structures, which also coincides with the opening of the The embryos adhere to the substratum due to particular mouth. This sequence of stages, each possessing its own propertiesof theirjelly coat, and hatching occurs directly at adhesive strategy, is common to all asteroid species having the brachiolariastage. Brachiolariaehave a hypertrophied, a benthic development. In A. gibbosa, morphologicaladap- bilobed attachmentcomplex comprising two asymmetrical tations to this mode of development include the hypertro- brachiolararms and a central adhesive disc. This study aims phic growth of the attachmentcomplex, its bilobed shape at describing the ultrastructureof the attachmentcomplex forming an almost completely adhesive sole, and the regres- and possible adaptations, at the cellular level, to benthic sion of the sensory equipment. development. Immediately after hatching, early brachio- lariae attach the arms. All the anteriorside of each by along Introduction arm, the epidermis encloses several cell types, such as secretory cells of two types (A and B), support cells, and Brachiolarialarvae, which are characterizedby a special- sensory cells. Like their equivalents in planktotrophiclar- ized attachmentcomplex comprising three larval arms (bra- vae, type A and B secretory cells are presumablyinvolved chia) and an adhesive disc, occur in the life cycle of many in a duo-glandularsystem in which the former are adhesive asteroids whatever their nutritional mode (planktotrophy and the latter de-adhesive in function. Unlike what is ob- versus lecithotrophy) or their developmental habitat (pe- served in planktotrophiclarvae, the sensory cells are unspe- lagic, benthic, or intragonadal) (McEdward and Janies, cialized and presumablynot involved in substratumtesting. 1993, 1997; Byrne, 1999; McEdward and Miner, 2001; During the larval period, the brachiolararms progressively Byrne et al., 2003). Among the different development pat- increase in size and the adhesive disc becomes more prom- terns, pelagic planktotrophyis traditionallyconsidered to be inent. At the onset of metamorphosis,brachiolariae cement the ancestral one (see, e.g., McEdward and Janies, 1993, themselves strongly to the substratum with the adhesive 1997). Successive evolutionarytransitions would then have disc. The disc contains two main cell types, support cells occurred to give rise to various types of nonfeeding larval and secretory cells, the latter being responsible for the development by (a) loss of larval feeding structuressuch as cement release. During this metamorphosis,the brachiolar ciliated bands and functional gut, and gain of large, yolky arms regress while post-metamorphicstructures grow con- eggs, followed by (b) loss of planktonicdispersal, and then siderably, especially the tube feet, which take over the role (c) gain of parental brood protection. Recently, however, molecular phylogenetic studies conducted on the family Asterinidae et showed that ordered Received27 July2005; accepted28 May 2006. (Hart al., 1997, 2004) * To whomcorrespondence should be addressed.Patrick.Flammang@ transformationsbetween the four modes of development umh.ac.be comprising brachiolariae(i.e., planktotrophic-pelagic,leci- 172 THE ATTACHMENT COMPLEX OF A BENTHIC ASTEROID LARVA 173 thotrophic-pelagic, lecithotrophic-benthic, and lecithotro- plex of A. gibbosa and to possible adaptations,at the cel- phic-intragonadal)could not be easily reconstructed, and lular level, to benthic development. that many parallel changes in larval form, habitat, and dispersal potential occurred. For example, in this family, Material and Methods benthic lecithotrophyevolved three times independently,in Parvulastra (Patiriella) exigua, in Aquilonastra (Asterina) Larval rearing minor and in the two sister Asterina and species, gibbosa Specimens of Asterina gibbosa (Pennant, 1777) were Asterina et In phylactica (Hart al., 2004; Byrne, 2006). collected intertidallyat Roscoff (Brittany, France) in 2001, these brachiolariaeall a species, possess hypertrophiedat- 2002, and 2003 during spring tides. They were kept in tachment Ko- complex (Ludwig, 1882; MacBride, 1896; marine aquaria (14 'C, 33 psu) at the marine biology labo- matsu et al., 1979; Marthy, 1980; Byrne, 1995, 2006). ratory of the University of Mons-Hainaut.Each year, at the Larvae of A. from those of A. gibbosa differ, however, end of April, groups of about 60 individuals were trans- minor and P. exigua because their attachment complex ferredinto a 10-1 tank filled with unfilteredaerated seawater as a sole-like structurerather than as a develops tripod-like at room temperature.When maintained in such conditions, structureas it is the case in the other two species. individuals spawned spontaneously after a few hours to a little is known about the fine structure and func- Very few days, depending on the group. Fertilized eggs were of the attachment in asteroids with benthic tioning complex collected the day they were laid and transferredinto large larvae; most ultrastructuraland immunocytochemicalinfor- petri dishes at 14 ?C and 21 ?C. Dishes were filled with mation on this comes from larvae. In organ planktotrophic filtered seawater (0.22 am). Water was changed daily, and the brachiolararms tem- planktotrophicdevelopers, provide the larvae were maintainedto the juvenile stage. porary attachmentto and sensory testing of the substratum during settlement, whereas the adhesive disc is involved in Morphological observations the permanentattachment that marks the onset of metamor- phosis (Barker, 1977; Gondolf, 2000; Haesaerts et al., Specimens of A. gibbosa were observed and photo- 2003). In planktoniclarvae, brachiolararms are tipped with graphed in vivo with a Leica MZ8 binocular microscope several sensory-secretory papillae, in which both the epi- equipped with a Nikon Coolpix digital camera. For scan- dermis and the underlying nerve plexus are greatly thick- ning electron microscopy (SEM), larvae were fixed in ened. The papillary epidermis encompasses support cells, Bouin's fluid for 12 h, dehydratedin a gradedethanol series, serotonergic sensory cells, and secretory cells (Barker, dried by the critical point method (with CO2 as transition 1978; Byrne et al., 2001; Haesaertset al., 2005a). The latter fluid), mounted on aluminum stubs, coated with gold in a function as a duo-glandularsystem with some cells acting as sputter coater, and observed with a JEOL JSM-6100 scan- adhesive cells and some others as de-adhesive cells (Her- ning electron microscope. Images were digitized with the mans, 1983; Flammang, 1996; Haesaerts et al., 2005a). As SEMafore 3.0 Pro software (JEOL, Tokyo, Japan). Some for the adhesive disc, it is a rounded,concave structurelying additionallarvae were fixed in glutaraldehydeand postfixed between the brachiolararms. It is made up of supportcells, in osmium tetroxide (see below), a method that does not ciliated secretory cells, and neurons (Barker, 1978; Gon- preserve the cuticle and thus reveals the underlying struc- dolf, 2000; Byrne et al., 2001; Haesaerts et al., 2005a). In tures (Ameye et al., 2000). benthic developers, on the other hand, hypertrophiedgrowth For light microscopy (LM) and transmission electron of the brachiolararms has been described as an adaptative microscopy (TEM), specimens were fixed in 3% glutaral- character to benthic habitat, but it is not known if other dehyde in cacodylate buffer (0.1 mol 1-', pH 7.8, adjusted adaptationsoccur at the cellular level. to an osmolality of 1030 mOsmol kg-' with NaCl) for 30 The present work describes the morphogenesis and ultra- min at 4 'C, rinsed in cacodylate buffer, and postfixed for structureof the
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