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Shell ultrastructure and ontogenetic growth in Nautilus pompilius L. (Mollusca: Cephalopoda)

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Abstract

Ontogenetic growth of the Nautilus shell is here reconstructed on the basis of structural studies of the initial, apical parts of adult shells. The results of these studies are compared with those obtained previously by studies on embryonic shells. The following four early growth stages can be distinguished: (1) formation of initial plate of organic matrix (periostracum) with cicatrix, (2) formation of initial calcified shell, composed of the initial organic plate and outer prismatic layer, (3) formation of three-layered shell-wall around the initial calcified shell, and (4) formation of three-layered protoseptum on the inner surface of the initial calcified shell-wall. The protoseptum differs from ordinary septa in that it lacks the siphonal tube and in that it is firmly attached to the inner surface of the initial shell-wall in order to make it less fragile, without forming a shell-chamber. During subsequent growth, two thin but distinct prismatic layers, separated by an organic sheet, are secreted on the inner surface of the ventral and lateral sides of the shell-wall. The outer of the two prismatic layers is the mantle-attachment layer. In adult shells, this layer is considerably thickened on the ventral and lateral sides of the shell aperture, and perforated by vertical canals, which in all probability housed finger-shaped epithelial extensions from the mantle. Thus, the mantle seems to be firmly attached to the apertural region of the shell during the entire ontogenetic growth of the animal. The inner of the two prismatic layers is the myostracal layer, secreted by the myo-adhesive mantle epithelium in front of the last septum. The caecum is the sac-shaped apical end of the siphonal tube. Its structure is extremely variable. Occasionally, the caecum is formed by a regularly developed connecting ring of the first septum and consists of the outer porous spherulitic layer and the inner conchiolin layer. In this case, it has the same structure as the connecting rings in the subsequent septa. Usually, however, the connecting ring of the first septum is structurally modified and heavily calcified. In the latter case, the wall of the caecum is impermeable to cameral fluid, which means that empting of the cameral fluid form the first chamber cannot take place in the majority of animals.
... The Late Carboniferous Shimanskya from Western Texas, Brewster Country, Marathon Basin; USA, has a Spirula/Sepia shell-wall type characterized by absence of nacreous layer. This shell-wall type has been earlier known in the fossil spirulid genus Adygeya from the Early Cretaceous of north-western Caucasus [13] and is atypical for the externally shelled cephalopods, in which a nacreous layer forms the bulk of the shell-wall thickness [14][15][16][17][18][19][20]. Thus, Shimanskya demonstrates the evolutionary stability of the Spirula/Sepia shell-wall type through a period of about 330 million years. ...
... The extant Sepia secretes an ultra-lightweight, high-stiffness organic-rich biomaterial that efficiently maintains neutral buoyancy at considerable habitation depths [23][24][25][26][27] . In various ectocochleate cephalopods, irrespective of their systematic affiliation, the wall typically consists of the outer prismatic, nacreous and inner prismatic layers [14][15][16][17][18][19][20]but rare forms among them have additional layers on the standard shell wall [28][29][30]. These layers imply a capability to stretch the mantle onto the external shell surface, producing an internally shelled condition that, at first glance, is similar to that in Spirula and Sepia. ...
... Scanning Electron Microscopy/Energy Dispersive Spectrometry (SEM/ EDS) Analyses of A. nordenskjoeldi under SEM/EDS revealed a unique combination of morphological , ultrastructural and chemical traits; they are: (1, 2) chambered, longiconic conch; (3, 4, 5) thin microlaminated shell wall, having no nacreous layer; (6, 7) a central/or slightly sub-central , broadly expanded siphuncle; (8) notably large (0.6 shell diameter) septal foramen, 2–6 times wider than that of all other known cephalopods; (9, 10, 11) deep, thin, organic septa; (12, 13) thin suborthochoanitic septal necks; (14, 15) thin non-mineralized connecting rings; (16) inorganic-organic mural, epi-and hyposeptal cameral deposits; (17) hyposeptal cameral soft tissues; (18) lack of endosiphuncular deposits; (19, 20) lack of a rostrum and pro-ostracum; (21) irregular mineralization of the shell wall evidenced by the variable content of calcium (5.4% -27.8%); (22) inorganic-organic shell wall composition indicated by high content of nitrogen (up to 7. 8%) and additionally by lower (less than 1%) content of manganese, iron, nickel, copper, zinc, barium, thallium and lead (Figs 1A–1G, 2A–2C, 3, 4A–4C, 5A–5C and 6A–6G; S1, S2A, S2B, S3, S4A, S4B, S6A, S6B and S8A–S8H Figs; Table 1). The prismatic mural, epi-and hyposeptal cameral deposits have, in comparison with the shell wall, higher average values of calcium (24% and 16.6%, respectively), carbon (27.6% and 18. 4%), nitrogen (7.05% and 4. 7%), magnesium (0.9% and 0.4%), potassium (0.9% and 0.2%), approximately similar values of oxygen (55.2% and 59.9%) and strontium (0.2% and 0.2%), but lower average values of copper (0.1% and 0.5%), zinc (0.5% and 0.7%), and lead (0.2% and 0.4%) (Fig 6A–6H; Table 1). ...
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Background The Subclass Coleoidea (Class Cephalopoda) accommodates the diverse present-day internally shelled cephalopod mollusks (Spirula, Sepia and octopuses, squids, Vampyroteuthis) and also extinct internally shelled cephalopods. Recent Spirula represents a unique coleoid retaining shell structures, a narrow marginal siphuncle and globular protoconch that signify the ancestry of the subclass Coleoidea from the Paleozoic subclass Bactritoidea. This hypothesis has been recently supported by newly recorded diverse bactritoid-like coleoids from the Carboniferous of the USA, but prior to this study no fossil cephalopod indicative of an endochochleate branch with an origin independent from subclass Bactritoidea has been reported. Methodology/Principal findings Two orthoconic conchs were recovered from the Early Eocene of Seymour Island at the tip of the Antarctic Peninsula, Antarctica. They have loosely mineralized organic-rich chitin-compatible microlaminated shell walls and broadly expanded central siphuncles. The morphological, ultrustructural and chemical data were determined and characterized through comparisons with extant and extinct taxa using Scanning Electron Microscopy/Energy Dispersive Spectrometry (SEM/EDS). Conclusions/Significance Our study presents the first evidence for an evolutionary lineage of internally shelled cephalopods with independent origin from Bactritoidea/Coleoidea, indicating convergent evolution with the subclass Coleoidea. A new subclass Paracoleoidea Doguzhaeva n. subcl. is established for accommodation of orthoconic cephalopods with the internal shell associated with a broadly expanded central siphuncle. Antarcticerida Doguzhaeva n. ord., Antarcticeratidae Doguzhaeva n. fam., Antarcticeras nordenskjoeldi Doguzhaeva n. gen., n. sp. are described within the subclass Paracoleoidea. The analysis of organic-rich shell preservation of A. nordenskjoeldi by use of SEM/EDS techniques revealed fossilization of hyposeptal cameral soft tissues. This suggests that a depositional environment favoring soft-tissue preservation was the factor enabling conservation of the weakly mineralized shell of A. nordenskjoeldi.
... Esta simplificación nos recuerda y hace pensar en la conjunción entre la espiral longitudinal y la transversal observada en el análisis resumen realizado en el capítulo primero. Y esa perspectiva se refleja claramente en la sección de dicha concha embrionaria correspondiente a esa fase preseptal (Figura 2.6) donde la parte dorsal embrionaria bien podremos catalogarla como el septo cero o inicial (Mutvei & Doguzhaeva, 1997 , indican que el protosepto o capa interior sobre la concha inicial es un septo que carece de tubo sifuncular). Precisamente es en la constricción de la cicatriz (C 1 en la Figura 2.6) donde la concha adopta la curvatura cordobesa en la pared ventral e inicia el cambio de concavidad en la pared dorsal, iniciándose el labio dorsal. ...
... Apoyándonos en que en una espiral cordobesa el ángulo que forma el radio vector con la recta tangente es de tenemos que (ver el detalle en la Figura 3.4) el ángulo que forma la recta tangente a la pared dorsal en con la recta tangente al septo en ese mismo punto es de , es decir el septo no interseca a la pared dorsal perpendicularmente, si no formando con respecto a esa perpendicular un ángulo de Eso concuerda con lo indicado por Mutvei & Doguzhaeva (1997) , que ya reflejamos en la Figura 2.31, y la depresión septal dorsal en el área media -sección o corte que es el que estamos analizando en este estudio-lo que hace es corregir dicha desviación respecto a la perpendicular buscando aportar y lograr, quizás, una mayor consistencia (eso es lo que puede interpretarse de este hecho aportado por la matemática). ...
Book
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La concha del Nautilus es el reflejo de la bitácora vital de este ser vivo y, en general, los seres vivos dentro de la homogeneidad de formas que mantienen durante su ciclo vital presentan ciertas particularidades en las etapas embrionaria, juvenil y adulta, es la denominada ontogenia biológica. En este libro analizamos la ontogenia del Nautilus y construimos el modelo ontogénico matemático de su concha.
... The pores contain small, finger-shaped extensions from the mantle epithelium that are attached to the inner shell surface on the body-shell attachment band (Stenzel 1964;Doguzhaeva & Mutvei 1986, fig. 5D; Mutvei & Doguzhaeva 1997, fig. 10). ...
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The structure of the shell wall in the Ordovician Orthoceras differs from that in the extant Nautilus. It consists of two equal thick layers: an outer probably nacreous layer and an inner prismatic layer. The two layers are separated from each other by a thin intermediate sub-layer that is rich in organic substance and has indistinct boundaries. The intermediate sub-layer and the inner prismatic layer contain a hitherto undetected pore-canal network that consists of vertical and horizontal canals. Horizontal canals are arranged in a single layer in the outermost part of the intermediate sub-layer. The vertical canals are arranged in parallel rows, and the canals in each row open into one of the horizontal canals. The canals have thin walls of calcified organic fibres. The walls are preserved in the intermediate sub-layer, whereas in the inner prismatic layer, they are partially dissolved. The canal network is absent in the shell wall of the extant Nautilus, but the horizontal canals occur in the shell wall of the Carboniferous orthocerid-like coleoid Mitorthoceras and the bactritid-like coleoid Shimanskya. Thus, the pore-canal network had an important, still unknown, function for the animal, and it existed, without changes, at least 150 ma.
... Tarphycerids (Early Ordovician-late Silurian) with tightly coiled conchs are the oldest cephalopods with a supposedly nektonic mode of life resembling extant Nautilus (Kröger 2005, Kröger & Landing 2008. The time of hatching can be determined in fossil nautiloids by applying an actualistic approach using information from the early embryonic development of extant Nautilus (Stenzel 1964, Mutvei et al. 1993, Mutvei & Doguzhaeva 1997). It appears to work well for post-Palaeozoic nautilids, in which freshly hatched juveniles look like miniature adults. ...
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Our study of the early ontogeny of the Silurian Ophioceras has led to the revision of the current concept that many juvenile tarphycerids possessed a coiled conch upon hatching and thus resembled adults in habit as is in extant Nautilus. In fact, there is no evidence that any Early Palaeozoic coiled nautiloid possessed an embryonic conch exceeding half a whorl. A change in conch coiling, occasionally accentuated by a dorsolateral groove analogous to the nepionic constriction and the appearance of conspicuous growth anomalies indicate that, after hatching, Ophioceras possessed a cap-shaped, slightly curved conch, usually approximately a quarter whorl long. A hatchling thus differed substantially from the likely nektonic late juveniles with coiled conchs and their obliquely oriented aperture as in Nautilus. A relatively large first phragmocone chamber and very short body chamber possibly resulted in positive buoyancy and a planktonic habit of hatchlings. The embryonic conch size is highly variable and the height of the first chamber varies between 1.2-2.6 mm. Changes in sculpture across the embryonic/juvenile conch boundary are sometimes gradual, but frequently, hatching is manifested by an abrupt increase in growth line spacing and the appearance of longitudinal ridges. The cicatrix is here documented in the Tarphycerida for the first time. A distinct chamber length decrease, commonly present close to the end of the first whorl, is not linked with hatching. Anomalous conch structures in Ophioceras including healed injuries, atypical shapes of ribs, atypical courses of septa and pits occurring in late juvenile growth stages are described in the light of the autecology of Ophioceras and the determination of early post-embryonic growth anomalies.
... The interspaces between the plates may have been formed from post-mortem destruction of the perishable organic matter between the plates. Mutvei and Doguzhaeva 1997). Schematic presentation of the body to show mantle surface ( m), sites of the origin of the retractor muscles ( rm) and the mantle and septal attachment zones ( aa, pa), mantle attachment zone to the shell aperture ( exp) with finger like epithelial extensions ( p) layers separated with a thick, additional prismatic layer. ...
Chapter
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The present chapter is a review on the aberrant shell wall structures of some ammonoids characterized by additional external layers. Secondary deposits of shell on the outside of the conchs of some ammonoid species suggest that the body exceeded the body chamber volume and the mantle coated the shell.
Article
Orthocerid-like coleoids with mixed orthocerid-coleoid characteristics are described for the first time from the Carboniferous of USA. The appearance of these coleoids represents transitional morphology between the orthoconic nautiloid and coleoid lineages. This transitional state is based on the new genus Colorthoceras n. gen. with three assigned new species (C. inflata n. sp., C. tubulata n. sp. and C. concavus n. sp.) in the new family Colorthoceridae of the new order Colorthocerida. Orthocerid nautiloid characteristics include a longiconic phragmocone with a well-developed body chamber, and a central, sub-central or sub-ventral siphuncle with endosiphuncular deposits. The shell wall in the new order Colorthocerida is characterized by the coleoid characteristics of a lack of the nacreous layer, with a high content of chitin that created a somewhat semi-elastic shell. The connecting rings are uni-layered, directly continuous from the septal neck, and have a mixed chitinous-calcareous composition similar to that in order Mixosiphonata. The shell wall structure in these unique orthocerid-like coleoids is similar to that in the previously described Carboniferous bactritoid-like coleoids. The evolution of these coleoid characteristics appears to represent an unsuccessful evolutionary experiment, as the diversity of this nautiloid lineage was in gradual decline in the Upper Paleozoic. https://zoobank.org/urn:lsid:zoobank.org:pub:84AF55EC-9A8D-4237-A2AE-185BBFA9C3EA
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The ultrastructure of pristine shells of Jurassic and Cretaceous lytoceratid and perisphinctid ammonoids indicates that flares and parabolae represent homologous structures. Both mark an interruption of shell growth. We dismiss earlier interpretations of parabolae as actual aperture, relics of resorbed apophyses or superstructure of the musculature associated to a semi-internal shell. Instead we propose an episodic growth model including several growth stops at the aperture during the formation of a frill-like aperture for parabolae and flares. Such an aperture is composed of the outer prismatic layer, the nacreous layer and an apertural prismatic coating. Here, we observed the apertural prismatic coating for the first time as an integral part of flares and parabolae. The apertural prismatic coating covers only the inner surface of the frill and was secreted by a permanent mantle cover indicating a prolonged period without the production of new shell material. Parabolae differ from flares by their general shape and the presence of ventro-lateral parabolic notches and nodes. The notches were formed by folding of the frill and had the potential to form semi-open spines. The corresponding parabolic nodes are caused by an outward swelling of the shell-secreting mantle tissue producing new shell material at the position of the folding. New shell material that belongs to the conch tube is attached to the base of flares and parabolae after withdrawal of the mantle edge representing the continuation of shell growth. Usually, the frilled aperture associated with flares and parabolae were removed during lifetime. This study reports on flares in Argonauticeras for the first time. In this genus they are typically associated with varices.
Chapter
The varying body chamber lengths and the different attachment of muscles and mantle to conch wall belong to the major adaptations to their diverse modes of locomotion. Therefore, these traits are indirect indicators of different life styles. The sparse record of ammonoid body chamber lengths and attachment marks has impeded the understanding of this aspect of ammonoid paleobiology. The examination of body chamber length revealed that the decrease of the ammonitella body chamber lengths shows is the long-term trend characterizing the evolutionary development of the Goniatitida–Prolecanitida–Ceratitida–Phylloceratida branch of the Ammonoidea. The analysis of the body chamber lengths and the attachment marks leads to conclusion that a precondition for the jet-powered swimming of ammonoids is less than one whorl body chamber length and the position of the attachment marks in sites from where the cephalic retractor and funnel retractor muscles would be able to extend straight across to the head and to the funnel. This is the case of goniatitids and ammonitids possessing moved forward large ventrolateral muscle marks; jet-powered swimming is highly probable for them. None of the universal small dorsal, umbilical and ventral marks may be left in the attachment sites of the cephalic retractor and funnel retractor muscles. In the hook-shaped terminal body chambers of heteromorph ammonoids, like Audouliceras, the long tongue-like umbilical marks perhaps indicate the moved forward strong umbilical muscles adapted for regular change of the mantle cavity volume for sucking and filtering seawater. This suggests that such ammonoids fed on fine plankton or suspended organic rich substance. Their irregular coiled spiral shells, best suited to floating and perhaps vertical (diurnal) migrations, support the view above. The fossilized mantle so far described in the ceratitid ammonoid Austrotrachyceras has a laminated structure fibrous seen in internally shelled Jurassic belemnotheutis and Loligosaepia.
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The parabola-bearing shells of the Callovian ammonite Indosphinctes (Elatmites) submutatus Nikitin from Ryazan Region, Central Russia, are examined using morphological, ultrastructural and chemical approaches to clarify the functional significance of the parabola. The parabolae are missing in the embryonic shell that is comparatively large (about 1.5 mm in diameter) and has a prismatic shell wall, with the exception of the nacreous primary varix. There are no parabolae at the early post-hatching stage at which the shell wall consists of the outer prismatic, middle nacreous and inner prismatic layers. The parabolae are observed in small and medium-sized shells (about 15-30 mm in diameter) in which the bulk of the lateral and ventral portions of the shell wall are formed by the nacreous layer, and the outer prismatic layer seems to be missing. The thin dorsal wall lacks the nacreous layer, and the adjacent whorls are connected via a structureless layer showing a nano-granular ultrastructure. Beyond the contact of the whorls, the broken rolled ends of this layer are only preserved at the corners between the neighboring whorls. This perishable layer contains N (an indicator of organic ingredient preserved), C, O, Mg, Ca, Fe, Zn, and Sr. The same elements are detected in the structureless shell material from repaired injuries of the shell wall. There are about seven parabolae in a whorl. The parabolae are commonly exhibited on the exposed dorsal wall when the next whorl is broken. The parabolae are also observed on the outer shell surface not yet covered with the dorsal wall of the next whorl. The body chamber is about 330° in spiral length. The paired adorally 'opened' parabolic 'notches' are expressed either as small knobs on internal moulds, as nodes on the dorsal wall, or as a contour reinforced with minor relief on outer surface of the body chamber. A parabolic node represents a lens-like inclusion into the nacreous layer of the shell wall and is composed of flattened, loosely packed spherulites and nacreous micro-chips. Based on these observations it is suggested that (1) the shell of I. (E.) submutatus, excepting early ontogenetic stages, was coated with an organic-rich layer, possibly secreted from the outside like the outer plate in the shell wall of extant Spirula; (2) the parabolae served as attachment structures related to the mantle attachment inside and outside the body chamber.
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Nautilus, long recognized as the most primitive living cephalopod, provides insight into molluscan evolution. Despite many attempts, embryos have not been observed until now. This report details the surface morphology and extraembryonic circulatory pattern. It was found that development, as in other extant cephalopods, is direct, without larval stages. There appears to be no embryonic protoconch associated with shell ontogeny.