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Cephalopoda Loliginidae) : a Scanning Electron Microscopical Study A

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Cephalopoda Loliginidae) : a Scanning Electron Microscopical Study A DEVELOPMENTAL ASPECTS OF EMBRYONIC INTEGUMENT IN ALLOTEUTHIS MEDIA (CEPHALOPODA LOLIGINIDAE) : A SCANNING ELECTRON MICROSCOPICAL STUDY A. Scharenberg To cite this version: A. Scharenberg. DEVELOPMENTAL ASPECTS OF EMBRYONIC INTEGUMENT IN ALLO- TEUTHIS MEDIA (CEPHALOPODA LOLIGINIDAE) : A SCANNING ELECTRON MICROSCOP- ICAL STUDY. Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, 1997, pp.149-153. hal-03103548 HAL Id: hal-03103548 https://hal.sorbonne-universite.fr/hal-03103548 Submitted on 8 Jan 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. VIE MILIEU, 1997, 47 (2) : 149-153 DEVELOPMENTAL ASPECTS OF EMBRYONIC INTEGUMENT IN ALLOTEUTHIS MEDIA (CEPHALOPODA LOLIGINIDAE) : A SCANNING ELECTRON MICROSCOPICAL STUDY A. SCHARENBERG Geologisch-Palaontologisch.es Institut und Muséum Universitàt Hamburg, Bundesstrafie 55, 20146 Hamburg, Germany CEPHALOPODS ABSTRACT. - The embryonic integument of teuthoid cephalopods shows two EMBRYONIC DEVELOPMENT obvious features. First the development of an elaborate pattern of ciliated cells CILIATURE PATTERN and second the differentiation of a dense cover of glandular cells. Thèse epithelial GLANDULAR CELLS structures are illustrated by scanning électron microscopy in hatchlings of the midsize squid Alloteuthis média. Squid embryos have three différent sets of locomotory multiciliated cells. The cells of the outer yolk sac carry a uniform ciliation. On the embryo proper cilia are arranged in separated tufts, and finally a System of ciliary bands forms on the dorsal and ventral mantle surface. A further type of cilia in the epidermal lines of the head and the arms serves as a mechanoreceptor. The development of epithelial glandular cells in the form of goblet cells reaches its highest amount in the hatching stage. The ciliature pattern as well as the glandular cells occur in a functional context of development inside the chorion and of the mode of hatching through the envelopes of the egg mass. CEPHALOPODES RÉSUMÉ. - Le tégument embryonnaire des Calmars présente deux caractéristiques DÉVELOPPEMENT EMBRYONNAIRE évidentes : d'une part une structure ciliaire complexe et d'autre part la STRUCTURE CILIAIRE différenciation d'une couche dense constituée de cellules glandulaires. Ces GLANDES structures épithéliales sont mises en évidence à l'aide d'un microscope électronique à balayage sur des Calmars de taille moyenne Alloteuthis média (L.) au moment de Féclosion. Les embryons de Calmars présentent trois séries différentes de cellules multiciliaires locomotrices. Les cellules du sac vitellin externe présentent une structure ciliaire uniforme. Sur l'embryon, les cils sont disposés en touffes séparées et les surfaces dorsale et ventrale présentent un système ciliaire disposé en bandes. Un autre type de cils implantés sur les lignes épidermiques de la tête et des bras a une fonction mécanoréceptrice. Le développement des glandes muqueuses atteint son degré maximal lors de l'éclosion. La formation de la structure ciliaire et des glandes est imposée par la structure des enveloppes de la masse des œufs dans un contexte fonctionnel déterminé par le développement à l'intérieur du chorion et la manière d'éclore. INTRODUCTION hatching. Arnold and Williams-Arnold (1980) des- cribed in détail the embryonic development of this The integument of embryos and larvae can be ciliature pattern in Loligo pealei. As Boletzky considered a multifunctional organ system, which (1982) reported, this ciliature is not as well ela- serves as a turn-table for the interaction between borated in sepiid embryos. In sepiolid embryos the organism and the external médium. Therefore the entire ciliary band system is missing. In the ciliary Systems are common and responsible for incirrate octopods a dense embryonic ciliature oc- movement, feeding, protection or sensory fonc- curs only on the outer yolk sac. tions (Nielson 1987). A dense pattern of motile Beside the numerous locomotory cilia a further cilia is an obvious feature in the embryonic epi- type of cilia has been described by Sundermann thelia of teuthoid squids during post-cleavage de- (1983) in the epidermal lines, the so-called "Drii- velopment. Thèse multiciliated cells are shed after senlinien" of Naef (1928) on the head and arms. 150 A.SCHARENBERG Budelmann and Bleckmann (1988) demonstrated at the mantle apex is the so called Hoyles organ. that thèse cells serve as a sensory receptor System It is notable that the system of ciliary bands for detecting water movements. radiâtes from this organ (Fig. 5). A further integumental differentiation is the In the system of epidermal lines, which forms development of glandular cells, which cover the on the head and partly on the arms sensory cilia whole embryo. A comparative description was gi- are best visible in the dorsal Ll and L2 line on ven by Fioroni (1978). each side of the head (Fig. 7). Most of thèse hair This short contribution will represent some of cells are elongated in the antherior-posterior axis the morphological features of the squid integu- of the embryo and the cilia are standing in one ment from an A. média hatchling by scanning row. Further détails of thèse sensory cells, as well électron microscopy and will discuss the functio- as the latéral and ventral lines were not examined nal morphology of this organ system. here. MATERIALS AND METHODS DISCUSSION Egg strands of Alloteuthis were obtained from sam- The gênerai integumental differentiation, the ples collected off the shore of Laboratoire Arago, Ba- development and placement of the ciliature pattern nyuls-sur-Mer (France). They were maintained under in Alloteuthis correspond to those reported for running sea-water at a mean température of 15°C. Em- Loligo pealei by Arnold and Williams-Arnold bryonic development was observed from early organo- (1980). The ciliature of the outer yolk sac enve- genetic stages to hatching. The embryonic stages lope générâtes a first constant circulation of the referred to are those of Naef (1928) in combination intrachorionic fluid and a slow movement of the with those of Arnold (1965) given in brackets. Embryos embryo inside the egg case. In the incirrate octo- were taken from the chorion, washed in seawater and fixed in 2,5 % glutaraldehyd/seawater at 4°C. They were pods thèse cilia are responsible for the first em- dehydrated through a graded séries of ethanol and cri- bryonic inversion (Boletzky and Fioroni 1990). tical-point-dried with CO2. The examination was car- The ventilation guarantees the necessary gradient ried out with a CamScan 44 scanning électron for an effective O2/C02 respiration and the meta- microscope at 15 KV at the University of Hamburg, bolic exchange through the chorion. The cover of Geological and Paleontological Institute. multiciliated ectodermic cells of the outer yolk sac is the only cilia system, which appears in ail main lines of the Coleoidea and also in Nautilus RESULTS (Arnold and Carlson 1986). It resembles the uns- pecific uniform ciliation in early free swimming The onset of organogenesis at the end of gas- planula-like gastrula stages of bivalve larvae trulation is also the onset of differentiation of (Bandel 1988, pers. obs.). Most probably this is integumental structures. When the outer yolk sac based on the same genetic larval program for envelope is nearly closed, a shallow dépression ectodermic ciliation. forms the boundary between the embryonic area The ciliature on the integument of the embryo of blastoderm and the extra-embryonic area (fu- proper supports the movement of the intrachorio- ture external yolk sac). Organ rudiments morpho- nic fluid. Arnold and Williams-Arnold (1980) ob- logically arise first as thickened placodes, foldings served the gênerai direction of particle flow cau- or contractions of the embryo proper at stage VII sed by the beating cilia on the embryonic (16) (Fig. 1). The formation of the various organ integument. The ciliary tufts were described by primordia like shell gland, mantle, optic vesicles, them as so called "paddle-type cilia", because of gills, arms and statocysts defines the following their tendency to form plasma membrane swel- developmental stages. lings at the distal end of the cilia. The investiga- Two différent types of cilia can be recognized tion of Alloteuthis média could not confirm thèse from stage VII (16) onward. First, a uniform pat- observations in any type of cilia. tern of cilia appears on ail cells of the future outer The phenomenon of paddle cilia or discocilia yolk sac (Fig. 2). By hatching stage XX (30) has been reported in ciliary Systems of différent (Fig. 4) they develop into an elaborate system of invertebrate larvae (cf. Campos and Mann 1988). partly branched bands with a mean width of Sundermann (1991) observed similar membrane 9.5 |0.mm (Fig. 6). swellings in a hitherto not further described type The glandular cells, which cover the whole of cilia at Sepia hatchlings. Haszprunar (1985) embryo in the form of goblet cells are most ob- found thèse kinds of cilia also in the chemorecep- vious by their partly empty vacuoles (Fig. 6) in tor epithelia of the molluscan osphradium. Since the hatching stage XX (30). A further glandular the discovery of this type of cilia there has been system, which develops in a Y-shape arrangement a continuing discussion whether this phenomenon DEVELOPMENTAL ASPECTS OF EMBRYONIC INTEGUMENT 151 Pl. I. - Scanning électron micrographs of Alloteuthis média illustrating the development of the integument at différent embryonic stages. Fig. I, ventral view of stage VII (16) with organ primordia. Note ciliary tufts, visible as small light patches on mantle margin and optic vesicles.
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