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

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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 brachiolariae 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 metamorphosis (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 larval attachmentcomplex in Asterina gib- 1 h in 1% osmium tetroxide in the same buffer. After a final bosa. This common European asteroid produces large, buffer wash, they were dehydratedin a gradedethanol series yolky eggs that are laid in masses attachedto the substratum and embedded in Spurr's resin. For LM analysis, semithin throughtheir jelly coat (Marthy, 1980; Crump and Emson, sections (1-pm) were cut with a Reichert OmU2 ultramic- 1983). Eggs develop directly into lecithotrophic brachio- rotome equipped with a glass knife, stained with an equiv- lariaethat, from hatchinguntil metamorphosis,adhere to the olumic mixture of 1% Azur II and 1% methylene blue seafloor by means of a hypertrophiedattachment complex solutions, and observed and photographed with a Leitz (Ludwig, 1882; MacBride, 1896; Marthy, 1980). This at- Orthoplanlight microscope equipped with a Leica DC 300F tachmentcomplex, which has been described as bilobed or digital camera. For TEM analysis, ultrathinsections (70-80 sole-like, appearsto be unique among asteroidbrachiolariae nm) were cut with a Leica UCT ultramicrotomeequipped (Byrne, 2006). In this study, particularattention is paid to with a diamond knife. Sections were contrastedwith uranyl the different cell types that constitute the attachmentcom- acetate and lead citrateand observed and photographedwith 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

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Figure 1. Light microscopy of the development of live specimens of Asterina gibbosa. (A) One-cell stage surroundedby the jelly coat (jc): fe, fertilization envelope. (B) Early gastrulae with a large blastopore. (C) Gastrulae with a reduced blastopore (bp). (D) Pre-hatchinglarva marked by a groove separating the future anteriorand posteriorparts (arrow). (E) Hatching larva, with particles still attached to the jelly coat. (F) Early brachiolariawith a truncatedshape, attachedto other embryos and particles;shorter brachiolar arm (arrow):ap, anterior part; pp, posterior part. (G) Brachiolariawith well-developed brachiolararms (arrows); anteriorpart translucentwhile posteriorpart remains opaque. (H) Competentbrachiolaria with a fully developed attachment complex (arms and disc) and developing tube feet on the left side of the larva: ad, adhesive disc; ba, brachiolar arms; tf, tube feet. (I) Early metamorphiclarva (arrow indicates developing tube feet): ad, adhesive disc; rba, resorbing brachiolararm. (J) Metamorphiclarva: rac, resorbing attachmentcomplex; tf, tube feet. (K) Meta- morphic larva still attached to the substratumby the adhesive disc (ad). (L) Post-metamorphicindividual. 176 D. HAESAERTS ET AL.

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Figure 2. Scanning electron microscopy of the development of Asterina gibbosa during its perimetamor- phic period. (A) Left side of a 2-armbrachiolaria (regular larval form) showing the hypertrophyof the brachiolar arms (ba): ap, anteriorpart; pp, posterior part. (B) View of a 3-arm brachiolaria(exceptional larval form). (C) Left side of a late brachiolaria.Arrowhead indicates the location of the disc, and arrows show the epidermal bulges aroundthe disc: tf, tube feet. (D) Left side of a competentlarva: ad, adhesive disc; o, oral side of the future adult. (E) Metamorphiclarva attachedby the disc to particles,brachiolar arms regressing. (F) Early metamorphic larva with a detached resorbing attachmentcomplex (rac) showing the location of the adhesive disc (arrow). Arrowhead indicates the location of the mouth of the future adult. (G) Metamorphiclarva with a resorbing attachmentcomplex, functional tube feet, and a peristomium(per). (H) Juvenile with opened mouth (m). THE ATTACHMENT COMPLEX OF A BENTHIC ASTEROID LARVA 175

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Figure 4. Fine structureof the brachiolararms of the competentlarva of Asterinagibbosa (light microscopy [LM] andtransmission electron microscopy [TEM]). (A) Longitudinalsection in a brachiolararm (LM): AE, adhesive epidermis;CC, coelomic cavity;CTL, connectivetissue layer;M, mesothelium;SE, stem epidermis.Arrow indicates the presenceof the nerve plexus. (B, C) Section througha sensory secretoryarea in the arm (TEM):ASC, type A secretorycell; BSC, type B secretorycell; Ci, cilium; SC, supportcell; Fi, fibers;Mi, microvilli;RC, cell containing rod-shapedgranules; SG, secretorygranule; SP, secretorypore; VC, vacuolatedcell; Y, yolk granule.Arrowheads indicatethe presenceof zonulaadherens. (D) Detail of a type B secretorycell (TEM):BSC, type B secretorycell, SG, secretorygranule; Y, yolk granule.(E) Detail of the apicalpart of a sensoryciliated cell (TEM):AP, apicalprocess; Ci, cilium; Mi, microvilli;SCC, sensoryciliated cell. (F) Section throughthe nerve plexus and the basal partof a sensoryciliated cell (TEM):BP, basalprocess; CTL, connective tissue layer;NP, nerveplexus; SCC, sensoryciliated cell. (G) Detail of the stem epidermis(TEM): Ci, cilium; Fi, fiber;SC, supportcell; VC, vacuolatedcell. plasm with small vesicles of light-to-mediumelectron den- ing cells (Fig. 4E), and whose basal part intimatelycontacts sity (Fig. 4E). These are ciliated cells whose apical part the underlying nerve plexus (Fig. 4F). develops processes that extend laterally over the neighbor- The epidermisof the bulges observed on the inner surface THE ATTACHMENT COMPLEX OF A BENTHIC ASTEROID LARVA 179

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Figure 5. Fine structureof the disc of the competent brachiolariaof Asterina gibbosa (light microscopy [LM] and transmission electron microscopy [TEM]). (A) Longitudinal section through the disc (LM): CC, coelomic cavity; CTL, connective tissue layer; E, epidermis;M, mesothelium.Arrow indicatesthe nerve plexus. (B, C) Longitudinalsections throughthe disc epidermis(TEM): ASC, type A secretorycell; DSC, disc secretory cell; Mi, microvilli; SC, disc supportcell; SCC, sensory ciliated cell; VC, vacuolatedcell; Y, yolk granule. (D) Detail (TEM) of the basal epidermis (E) showing the thin subepidermalnerve plexus (NP) and fibers (Fi) from support cells that anchor to the basal lamina (BL): CTL, connective tissue layer. (E) Detail (TEM) of the subepidermalnerve plexus (NP) and a sensory ciliated cell (SCC): BL, basal lamina; CF, collagen fiber; CTL, connective tissue layer. (F) Detail of a secretorygranule (SG) from a disc secretorycell (TEM): Ci, cilium. (G) Detail (TEM) of a type B secretory cell (BSC): DSC, disc secretory cell; Y, yolk granule. (H) Longitudinal section through the disc epidermis (TEM): DSC, disc secretory cell; RC, cell containing rod-shapedgranules; SC, disc supportcell; VC, vacuolated cell; Y, yolk granule. 180 D. HAESAERTS ET AL of arms and aroundthe disc has the same structureas that of In additionto its peculiar shape, the attachmentcomplex the arm tip. The rest of the arm epidermis (stem epidermis) of A. gibbosa is also very large and occupies all the anterior consists only of supportcells, vacuolated cells, and sensory part of the larva. This is a characteristic shared by other cells. Sensory cells are, however, more numerous in the benthic developers-for example, Aquilonastra [Asterina] vicinity of the arm secretory cells. minor (Komatsu et al., 1979); Parvulastra [Patiriella] ex- At the level of the adhesive disc, the epidermisis made up igua (Byrne, 1995); and Leptasteriasochotensis similispinis of two main cell types that cover most of the disc surface: (Kubo, 1951). Generally, the brachiolar arms are well- disc secretory cells (type D cells) and disc support cells developed or hypertrophied,while the diameterof the disc (Fig. 5B, C, H). Disc secretorycells bear a short cilium and does not exceed the range of size found in planktotrophic house numerous large spherical membrane-boundgranules developers (Haesaerts et al., 2005a). (2.8 ? 0.6 /m; n = 16) whose fibrous content has a woven Although the brachiolararms of A. gibbosa do not pos- appearanceand is of medium electron density (Fig. 5F, G). sess the well-defined domelike papillae characteristicof the Disc supportcells contain a conspicuous bundle of filaments arms of planktotrophiclarvae (Barker, 1978; Byrne and up to 2 [m in diameterrunning from the base to the apex of Barker, 1991; Haesaertset al., 2005a), they have, however, the cell (Fig. 5B, D). These bundles are much thicker than large secretory areas specialized in temporaryattachment. those in the supportcells of the arms. Othercell types (such These areas, which occur not only at the tip of the arms but as type A and type B secretory cells and sensory cells) also also all along the anterior surface of the attachmentcom- occur in the disc epidermis, though much less frequently plex, are characterizedby the presence of secretory cells than type D cells and support cells. named types A and B. These cells are also scatteredin the adhesive disc epidermis. Goto (1898) already describedthe Discussion occurrenceof unicellularglands all over the anteriorsurface of the larval attachmentcomplex of A. gibbosa, including The attachment complex of benthic brachiolaria larvae the adhesive disc. According to his description, these are The attachmentcomplex of Asterina gibbosa has a typi- likely to correspondto type A secretory cells. Type A and cal bilobed shape due to its two asymmetrically sized bra- type B cells share many morphological similarities with chiolar arms. This unique organization differs from the their equivalents in the brachiolar arms of the planktotro- typical conformation of the complex consisting of a long phic larvae where secretorycells form a duo-glandadhesive anteriorand two shorterlateral brachiolararms surrounding system that is responsible for temporary adhesion (Flam- the adhesive disc, as it occurs in planktotrophicbrachio- mang, 1996; Haesaerts et al., 2005a). Concerning type A lariae such as those of Coscinasterias calamaria and Sti- cells (adhesive cells), the morphology of their secretory chaster australis (Barker, 1978), Patiriella regularis (Byrne pores with a short cilium, and the ultrastructureof their and Barker, 1991), and Asterias rubens (Gondolf, 2000; secretory granules (contents, size and shape) remain re- Haesaertset al., 2005a). This arrangementalso differs from markably constant from one species to another. In other that of the triradiatetripod complex of other benthic devel- benthic developers, the presence of such cells can easily be opers, in which the three arms are equally developed inferred from their characteristicpores with associated ci- (Byrne, 1995). However, this bilobed shape seems to have lium at the surface of the brachiolar arms (see, e.g., P. evolved from an ancestral larval type with three brachiolar exigua; Byrne et al., 2001). In pelagic developers, the arms; indeed, we observed a typical three-armattachment secretion released by type A cells is muccopolysaccharidic complex in a few larvae. This phenomenonwas recurrentin and cross-reacts with antibodies raised against the tempo- our rearing conditions and was already pointed out by rary adhesive of the tube feet (Haesaerts et al., 2005a). On Luwig (1882) and McBride (1898), who compared the the other hand, type B cells are typical echinoderm de- "occasional bifurcation"of the smallest lobe with the three- adhesive cells (Flammang, 1996). The occurrenceof a duo- arm attachment complex of other asteroids. It can be hy- gland adhesive system in the larval arms of benthic devel- pothesized, therefore, that this smallest lobe resulted from opers is also confirmed by their behavior. Indeed, in A. fusion of the two lateral arms present in the ancestral-type gibbosa, larvae are able to move over short distances by brachiolaria.Yet there is no indication whether the imme- repeatedly attaching and detaching their arms, as do the diate ancestor was a benthic or a planktonic lecithotrophic tripod larvae of P. exigua (Byrne, 1995). The occurrenceof brachiolaria. A benthic tripod form seems unlikely, as it type A and B secretory cells in the adhesive disc epidermis would requirereversal from equally sized to unequally sized indicates that this structureis involved not only in perma- arms. The evolution of a bilobed attachmentcomplex thus nent attachment but also in temporary attachmentbefore seems specific to larvae of the Atlantic Asterina, which metamorphosis, an ability already observed by MacBride interestingly were found by molecular methods to be sister (1896). The very wide distribution of type A and type B to all Pacific asterinidspossessing tripod larvae (Hart et al., cells over the brachiolar arms and the adhesive disc in- 1997, 2004; Byrne, 2006). creases the adhesive surface area in contact with the sub- THE ATTACHMENT COMPLEX OF A BENTHIC ASTEROID LARVA 181 stratum.The resulting sole-like attachmentpresumably pro- developed, as is the case in other benthic larvae (Byrne et vides more efficient adhesion for the organism, thus al., 2001). In the larvae of P. exigua, for example, an reducing the possibility that the larva will be dislodged by extensive peptidergic nerve plexus was demonstratedin the water motion before metamorphosis.The larvae of A. gib- attachmentcomplex, especially at the level of the adhesive bosa, like other benthic brachiolariae(Byrne, 1995), spend disc (Byrne et al., 2001). 4 to 6 days attached temporarily by the brachiolar arms, to brachiolariaethat remain in this contrary planktotrophic Characteristics of asteroid benthic development phase of temporaryattachment for not more than one hour, after which they either resume swimming or attach by the During its ontogeny, A. gibbosa keeps an almost uninter- disc and metamorphose(Barker, 1977). rupted relation with the substratumon which it lives. We The main function of the disc is to cement the larva to the have discerned four benthic developmental stages, each substratumduring metamorphosis.The disc secretory cells relying on particularadhesive structuresor organs: (1) the (type D cells) dominate in the disc epidermis and are re- embryonic stage, during which the embryos are attachedto sponsible for permanent attachment. Ultrastructurallythe the substratumin clusters by their jelly coat; (2) the bra- secretorygranules of the type D cells are remarkablysimilar chiolaria stage, when the brachiolararms provide temporary to those of asteroids with planktotrophic larvae (Barker, adhesion; (3) the metamorphicstage, which correspondsto 1978; Haesaertset al., 2005a), suggesting that the secretion the fixation by the adhesive disc; and (4) the post-metamor- of type D cells is probably proteinaceous (Barker, 1978). phic stage, when the first tube feet take over the role of In A. gibbosa, the sensory cells observed in the secretory attachment to the substratum,while enabling locomotion. areas of the brachiolararms and in the adhesive disc were This sequence of stages, each possessing its own adhesive identical to those distributedall over the larval epidermis. strategy, seems to be characteristicof all asteroid species This is different from what is seen in planktotrophicbra- having a benthic development (Komatsuet al., 1979; Byrne, chiolariae, in which a unique type of serotonergic sensory 1995). In A. gibbosa, a turbulentchannel flow apparatushas cell, presumablyinvolved in the detection of cues associated been used to evaluate the attachment strength of three of with the substratum,appears to be restrictedto the papillae these developmental stages (Haesaerts et al., 2005b). The of the brachiolar arms (Barker, 1978; Chee and Byrne, results showed that the flows needed to dislodge brachio- 1999; Haesaertset al., 2005a). Once a suitable substratumis lariae attached by the arms and postmetamorphicindividu- found, the stimulationof these specialized cells presumably als attachedby the tube feet are similar and much lower than triggers the behavioral sequence leading to larval fixation the flow needed to detach metamorphicindividuals attached and metamorphosis(Barker, 1978; Haesaerts et al., 2005a). by the disc. The larval fixation is considered to be a per- In A. gibbosa, the sensory cells of the attachmentcomplex manent attachment because the disc remains cemented differ in ultrastructurefrom the ones found in the papillae of when the organism detaches and assumes a free benthic life. planktotrophiclarvae. Moreover, their homogeneous distri- Such a feature is also observed in planktotrophic larvae bution over the entire larval body suggests that they are (Gemmill, 1914; Strathmann,1978; Barker, 1978). unrelated to settlement or metamorphosis, which is not The attachment complex of A. gibbosa presents some surprising since larvae of this species move only short characteristicstypical of the benthic mode of development, distances; in fact, they develop and metamorphose on the but it also has some unique characteristics.The hypertrophic same spot where the fertilized eggs are laid by the adults, development of the complex is a feature that evolved inde- making the search for a suitable metamorphosissite unnec- pendently several times in phylogenetically distant asteroid essary. The loss of the sensory cells required for surface lineages that have benthic development, while the bilobed testing is significant from the evolutionary point of view. shape seems to have evolved only once, in the genus Aste- Indeed, McEdward and Janies (1997) proposed that, con- rina (Kubo, 1951; Komatsu et al., 1979; Byrne, 1995; traryto the evolutionarytransition from feeding to nonfeed- 2006). At the ultrastructurallevel, the wide distribution of ing development which would be irreversible because it the secretorycells involved in temporaryattachment to form involves marked changes in larval morphology, the transi- an almost complete adhesive sole at the anterior surface of tion between pelagic and benthic development would be an the attachment complex (see above) is presumably corre- ecological change independent of changes in morphogene- lated to this bilobed shape. The lack of sensory cells in- sis and thus should be reversible. Regression of the sensory volved in the detection of settlement-associatedcues, on the equipmentin A. gibbosa suggests that reversal from benthic other hand, is described for the first time in a benthic lecithotrophy to pelagic lecithotrophy would probably be developer. More ultrastructuraldata from species with tri- more difficult than previously thought. pod larvae are needed to determinewhether this feature has Regression of sensory abilities does not mean regression also evolved in other benthic developers. of the nervous system altogether and, in A. gibbosa, the Another common feature of the benthic development nerve plexus associated with the attachmentcomplex is well pattern is the floating behavior of juveniles. In our rearing 182 D. HAESAERTS ET AL. conditions, we observed this behavior a few days after and ecology of the two British species of Asterina. Field Stud. 5: metamorphosiswhen the juveniles went to the water surface 867-882. Flammang, P. 1996. Adhesion in echinoderms. 1-60 in Echinoderm upside down. Such behavior was previously observed in Pp Studies, Vol 5, M Jangoux and J. M Lawrence, eds. Balkema, Rot- other asteroid species with benthic development-i.e. in terdam. Asterina phylactica, A. minor, P. exigua, and Patiriella Gemmill, J. F. 1914. The development and certain points in the adult pseudoexigua-and suggested to be a means of dispersal structureof the starfishAsterias rubens, L. Philos. Trans.R. Soc. Lond. (Marthy, 1980; Soliman and Nojima, 1984; Byrne, 1995; B 205: 213-294. A. L. 2000. and electron obser- Chen and Chen, 1992). This is likely to be Gondolf, Light scanning microscopic juvenile rafting vations on the of the common an mechanism for flow in developmental biology starfishAsterias important enhancing gene species rubens (Echinodermata:Asteroidea). Ophelia 52: 153-170 an benthic Wa- Linn6 having entirely development (Byrne, 1995; Goto, S. 1898. Some points in the metamorphosisof Asterina gibbosa. ters and Roy, 2004). J. Sc. Coll. Imp. Univ. Tokyo. Vol XII, Pt III. Haesaerts, D., M. Jangoux, and P. Flammang. 2003. Study of the Acknowledgments perimetamorphicperiod of the sea star Astertas rubens by scanning electron microscopy. Pp. 155-159 in EchinodermResearch 2001, J.-P. This work was supportedby a FRIA (Belgium) grant to F6ral and B David, eds. Swets & Zeitlinger, Lisse. DH. PF is a Research Associate of the National Fund for Haesaerts, D., M. Jangoux, and P. Flammang. 2005a. The attachment Scientific Research (FNRS, This is a con- complex of the brachiolana larvae of the starfish Asterias rubens L. Belgium). study an ultrastructuraland tribution of the 'Centre Interuniversitairede Ma- (Echinodermata): immunocytochemical study. Biologie Zoomorphology124: 67-78. rine' (CIBIM; http://www.ulb.ac.be/sciences/biomar/). Haesaerts, D., J. A. Finlay, M. E. Callow, J. A. Callow, Ph. Grosjean, M. Jangoux, and P. Flammang. 2005b. 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