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Development of the Embryonic Shell Structure in Nautilus
Abstract
Microstructural features of embryonic shells of Nautilus macromphalus and N. pompilius at different stages of development were observed by optical and scanning electron microscopy on the basis of specimens recovered from the Kasai and Toba Aquaria, Japan. The results of our observations reveal that the early embryonic shell development of Nautilus can be divided into two major stages with different shell structure and ornamentation. In the first stage, a low cap-shaped shell with a distinct median depression (= cicatrix) is secreted by the shell gland in the sequence of outer conchiolin and inner spherulitic prismatic layers. In the second stage, a new shell consisting of outermost conchiolin, outer prismatic, middle nacreous, and inner prismatic layers appears at the outer margin of the cicatrix, marked by a discontinuity in the shell structure (constriction) at the boundary. It is ornamented with longitudinal growth lines and radial undulations, indicating shell secretion at the mantle margin. During the second stage, a protoseptum, which comprises outer prismatic, middle nacreous, and inner prismatic layers, is also added on the adorai side of the cicatrix by the rear mantle. These early embryonic shell features of Nautilus are similar to those of Carboniferous orthocerids, but are clearly distinguished from those of coleoids and ammonoids, both starting with a spherical initial chamber.
... It is generally cap-shaped with a prominent medial depression. In Nautilus, the cicatrix is composed of an outer conchiolin, and inner spherulitic-prismatic layer, later underlain by the proseptum (Tanabe and Uchiyama 1997). The outer edge of the cicatrix may be marked by a weak constriction beyond which the conch wall consists of an outer conchiolin layer, an outer prismatic layer, a middle nacreous layer, and inner prismatic layer (Tanabe and Uchiyama 1997, fig. ...
... In Nautilus, the cicatrix is composed of an outer conchiolin, and inner spherulitic-prismatic layer, later underlain by the proseptum (Tanabe and Uchiyama 1997). The outer edge of the cicatrix may be marked by a weak constriction beyond which the conch wall consists of an outer conchiolin layer, an outer prismatic layer, a middle nacreous layer, and inner prismatic layer (Tanabe and Uchiyama 1997, fig. 8). ...
High-level classification of the nautiloid cephalopods has been largely neglected since the publication of the Russian and American treatises in the early 1960s. Although there is broad general agreement amongst specialists regarding the status of nautiloid orders, there is no real consensus or consistent approach regarding higher ranks and an array of superorders utilising various morphological features has been proposed. With work now commencing on the revision of the Treatise Part K, there is an urgent need for a methodical and standardised approach to the high-level classification of the nautiloids. The scheme proposed here utilizes the form of muscle attachment scars as a diagnostic feature at subclass level; other features (including siphuncular structures and cameral deposits) are employed at ordinal level. We recognise five subclasses of nautiloid cephalopods (Plectronoceratia, Multiceratia, Tarphyceratia nov., Orthoceratia, Nautilia) and 18 orders including the Order Rioceratida nov. which contains the new family Bactroceratidae. This scheme has the advantage of relative simplicity (it avoids the use of superorders) and presents a balanced approach which reflects the considerable morphological diversity and phylogenetic longevity of the nautiloids in comparison with the ammonoid and coleoid cephalopods. To avoid potential confusion arising in the higher levels of nautiloid classification employed in the revision of the Treatise Part K, we propose herein to replace the suffix ‘-oidea’ at subclass level with the suffix ‘-ia’. Apart from removing ambiguity and clarifying the nomenclature, this approach also brings greater consistency and affinity with modern zoological classification schemes used for cephalopods. The original Treatise Part K adopted an ‘abbreviated’ form of name for nautiloid orders using the ending ‘-cerida’ rather than ‘-ceratida’ (e.g., Order Actinocerida rather than Actinoceratida). For the revision of Treatise Part K, we propose using the ‘full’ version of the ordinal names. This approach re-employs several order names in their original form, e.g., Ellesmeroceratida, Oncoceratida, and Tarphyceratida. For reasons of consistency, we also apply the same to ordinal names created since the original Treatise Part K; therefore, Order Bisonocerida becomes Bisonoceratida.
... Well preserved embryonic shells of Arbuckleoceras tricamerae were documented by Ristedt (1971) and Tanabe and Uchiyama (1997) as "Orthoceras" sp. A and by Blind (1987Blind ( , 1988Blind ( , 1991 as Orthoceras sp. ...
... Cephalopods of the Buckhorn Asphalt Lagerstätte have been investigated for biogeochemistry (Crick, 1982;Brand, 1987Brand, , 1989Sadd, 1991;Seuss et al., 2012a), shell ultrastructure (Ristedt, 1971;Blind, 1988Blind, , 1991, ultrastructure of organic remnants (Grégoire, 1988), apical shell characters (Ristedt, 1971;Blind, 1987Blind, , 1988Tanabe and Uchiyama, 1997), and the structure of cameral and endosiphuncular deposits (Fischer and Teichert, 1969;Crick, 1982;Seuss et al., 2012b). However, the taxonomy of the cephalopods analyzed in these papers has never been revised or treated in detail. ...
Nine longiconic cephalopod species of Desmoinesian (Middle Pennsylvanian; upper Carboniferous) pseudorthoceratid orthocerids are described from the Buckhorn Asphalt Lagerstätte (Boggy Formation) in Southcentral Oklahoma, Midcontinent North America. The fauna consists of Pseudorthoceras knoxense (McChesney), Arbuckleoceras tricamerae (Smith), Bitaunioceras buckhornense (Smith), Cyrtothoracoceras? sp., Dolorthoceras boggyense sp. nov., Smithorthoceras unicamera (Smith), Sueroceras oklahomense (Smith), Sulphurnites taffi sp. nov. and Unklesbayoceras striatulum sp. nov. Bitaunioceras buckhornense represents the first Pennsylvanian and therefore the oldest record of this genus. Arbuckleoceras gen. nov. differs from a comparable genus, Shikhanoceras, in possessing a weak exogastric curvature with a circular cross section of the conch and in lacking a conspicuous inflation at the embryonic shell. Smithorthoceras gen. nov. resembles orthoceratids rather than pseudorthoceratids in characters of camerae and siphuncle; however it refers to the Pseudorthoceratidae by having endosiphuncular deposits. These similarities seem to be the result of convergent evolution. Endosiphuncular deposits in Sulphurnites gen. nov. initiate at apical and adoral junctions between septal neck and connection ring, whose characters are unique for pseudorthoceratids. Unklesbayoceras gen. nov. differs from Mitorthoceras in having the endogastric conch, longer camerae and a less eccentric siphuncle. Taxonomic status of these orthoceratids was uncertain in previous biogeochemical and morphological studies. Sediments in the Buckhorn Asphalt Lagerstätte were deposited in a tropical epeiric sea (the Midcontinent Sea). Small, restricted marine basins, like that in this Oklahoma occurrence, probably provided an orthocerid refuge habitat as indicated by the high diversity and provincialism in comparison with other Middle Pennsylvanian (= Moscovian) faunas in other regions of the world.
... The embryonic shell of a lechritrochoceratid shows three morphologically discernible growth stages. The first stage is represented by a small elliptical, dorsoventrally elongated cicatrix with a central bar similar to that in Nautilus and fossil nautilids (Schindewolf 1933;Arnold et al. 1987;Tanabe and Uchiyama 1997;Chirat and von Boletzky 2003). The flattened area of the cicatrix is inclined towards the dorsum (P. ...
The family Lechritrochoceratidae Flower, 1950 includes the earliest cephalopods acquiring a lateral pair of retractor muscles—a diagnostic character of the Nautilida. The embryonic shell of Silurian lechritrochoceratids is minute, with a diameter of 2–4 mm, a length of 4.5–7.5 mm and consists of three growth stages: (1) elliptical, dorsoventrally elongated and flattened cicatrix with a central bar, (2) a short, rapidly expanding shell part and (3) a gradually expanding, very slightly curved shell. The sculpture consists of longitudinal lirae, and faintly distinct growth lines or ridges. A ventral lobe formed by ridges corresponds in its course to post-hatching ribs. This lobe indicates the early development of the hyponome in the egg capsule. The hatching is indicated by the appearance of ribs and sometimes also by a change in shell curvature. The juvenile stage is characterised by the prolongation of the body chamber, a change in the shape of the cross section, increasing expansion rate, and by a deepening of the hyponomic sinus. The juveniles were probably demersal with the aperture oriented more or less towards the sea floor. The dorsoventrally elongated cicatrix with a central bar and a depression corresponding to the caecum position and the appearance of longitudinal lirae near the cicatrix margin support systematic position of the lechritrochoceratids among the Nautilida. The hemispherical apex and the very slightly curved embryonic shell, ribbed juvenile shell and narrow annular elevation around the body chamber base, however, call for the definition of a new suborder Lechritrochoceratina.
... Nautilida. Authors as Stenzel in Sweet (1964), Arnold et al. (1987) or Tanabe and Uchiyama (1997) have reported on a 'caecum' in Nautilus (Fig. 4d). Unlike other cephalopods, the Nautilus type of caecum cannot penetrate the first septum as it lacks a siphuncular foramen. ...
Homoplasy is a common phenomenon in the evolution of the Cephalopoda. Many homology problems accordingly light up phylogenetic debates. The initial segment of the siphuncle, the so-called ‘caecum’, is one of these characters difficult to be unambiguously evaluated. Although rarely discussed, the caecum of the endocochleate decabrachian Spirula is traditionally seen as a plesiomorphy directly inherited from its ectocochleate ancestors. However, the Spirula caecum must be—according to recent phylogenetic analyses—derived from a substructure of the belemnoid protoconch. Here, I review the morphology of different types of ectocochleate and endocochleate protoconchs. Detailed comparisons show that belemnoid protoconchs are structurally closer to the bactritoid/ammonoid protoconch than to the spiruloid protoconch. The most striking difference between the caecum of Spirula and bactritoids or ammonoids concerns its ultrastructure, which is lamello-fibrillar nacre (Spirula nacre or nacre type II) in the former and organic in the latter. The Spirula caecum is consequently equivalent to the first septum, while in bactritoids/ammonoids, the caecum is a separate structure independent of the proseptum. To conclude, the spiruloid protoconch (including caecum) has been derived either from a belemnitid or diplobelid protoconch. Similarities between the bactritoid/ammonoid and spiruloid caecum are superficial and only concern its shape.
... In species with a rudimentary shell, shell gland development ceases during dorsal ectoderm invagination, and the shell field never forms. In cephalopods with an internal shell, the shell gland is also internalised forming a 'shell sac', whereas Nautilus retains an external shell throughout embryogenesis (Kniprath, 1981;Tanabe & Uchiyama, 1997;Hohagen & Jackson, 2013). However, cephalopod eggs differ from those of other molluscs in the presence of large yolk stocks, strongly impacting embryonic development, therefore there might be underlying cephalopod-specific developmental patterns. ...
An exhaustive study of existing data on the relationship between egg size and maximum size of embryonic shells in 42 species of extant cephalopods demonstrated that these values are approximately equal regardless of taxonomy and shell morphology. Egg size is also approximately equal to mantle length of hatchlings in 45 cephalopod species with rudimentary shells. Paired data on the size of the initial chamber versus embryonic shell in 235 species of Ammonoidea, and 1 Spirulida demonstrated that, although there is a positive relationship between these parameters in some taxa, initial chamber size cannot be used to predict egg size in extinct cephalopods; the size of the embryonic shell may be more appropriate for this task. The evolution of reproductive strategies in cephalopods in the geological past was marked by an increasing significance of small-egged taxa, as is also seen in simultaneously evolving fish taxa.
... However, mainly because of poor preservation, the shell ultrastructure at early ontogenetic stages was still inadequately known. Among orthoconic forms the shell ultrastructure had been mainly studied in Pennsylvanian (Upper Carboniferous) ortho-and pseudorthocerids of the Buckhorn Asphalt of the USA (ERBEN et al., 1969;RISTEDT, 1971;MUTVEI, 1972;BLIND, 1988;TANABE & UCHIYAMA, 1997). The shell ultrastructure of the Palaeozoic orthoceroids and ammonoids is better known than that of bactritoids. ...
... The cephalic compartment is situated at the most anterior, and the tentacle buds are arranged along each lateral side of the embryonic bodies. Following these findings, a more detailed analysis was conducted on the embryonic shell (Arnold et al., 1987;Tanabe and Uchiyama, 1997). recently, the unknown earlier stages of Nautilus pompilius were analyzed, and the outline of developmental sequence was finally described (Figure 3A-C; Shigeno et al., 2008). ...
... The cephalic compartment is situated at the most anterior, and the tentacle buds are arranged along each lateral side of the embryonic bodies. Following these findings, a more detailed analysis was conducted on the embryonic shell (Arnold et al., 1987; Tanabe and Uchiyama, 1997). recently, the unknown earlier stages of Nautilus pompilius were analyzed, and the outline of developmental sequence was finally described (Figure 3A-C; Shigeno et al., 2008). ...
... Their summary is based on four lines of evidence, namely, the microstructure of the shell wall, the ornamentation, the presence of the primary varix, and the shape of the proseptum (Landman et al. 1996, Fig. 19). These observations, in analogy with studies of the early ontogeny of modern cephalopods, especially modern nautilids (Arnold et al. 1987;Landman 1988;Tanabe and Uchiyama 1997), suggest that ammonites developed directly without a larval stage, which is also in line with their larger size compared to other mollusks (more yolk?). According to this theory of direct development in ammonoids, the ammonitella, consisting of the initial chamber and the whorl terminating at the primary varix, formed within the egg capsule. ...
A great number of new studies have been carried out on ammonoid embryonic development in the last two decades. We focus here on novel developments and interpretations in the description of the embryonic shell (including terminology, shape, size, ornamentation, microstructure, septa, siphuncle and muscle scars), the sequence of embryonic development, reproductive strategy and post-hatching mode of life, followed by conclusions and possible future areas of research.
... The cephalic compartment is situated at the most anterior, and the tentacle buds are arranged along each lateral side of the embryonic bodies. Following these findings, a more detailed analysis was conducted on the embryonic shell (Arnold et al., 1987;Tanabe and Uchiyama, 1997). recently, the unknown earlier stages of Nautilus pompilius were analyzed, and the outline of developmental sequence was finally described (Figure 3A-C; Shigeno et al., 2008). ...
Nautilus macromphalus is the species of nautilus characteristic of the New Caledonian Archipelago, which comprises the islands of New Caledonia, the Isle of Pines, and the Loyalty Group. I took up my residence on the shores of Sandal Bay, Lifu, in August, 1896. Having collected a number of Nautilus, I placed them in captivity in a large native fish-trap, specially fitted up, fed them twice or three times a week with fish, land-crabs, Palinurus, and Scyllarus, and on December 5,1896, commenced to obtain the fertilised ova. It is not necessary at present to describe the details of manipulation, and I therefore proceed at once to give a brief account of the more obvious features of the eggs as illustrated by the accompanying figures.
This paper discusses postembryonic early mode of life in Carboniferous goniatites based on analysis of ammonoid assemblages and calculation. of total shell densities of actual specimens. Co-occurrence of embryonic and postembryonic shells appears common in. Carboniferous Goniatitina, as confirmed in Home ceras, Homoceratoides, Vallites, and Reticuloceras from the Middle Carborziferous (Namurian) of west Ireland and England, in Tumulites, Cravenoceras and Eumorphoceras from the Upper Mississippian. (Chesteran) of Texas, and in Aristoceras and Vidrioceras from the Upper Pennsylvanian (Virgilian) of Kansas. Embryonic and postembryonic shells of these genera occur in ammonoid-packed calcium carbonate concretions (bullions) or in black bituminous limestone beds, together with rare shells of bactritoid cephalopods, brachiopods, bivalves and gastropods. They appear to not have been transported a long distance because of the absence of a preferred orientation, size sorting and apparent shell abrasion. or fragmentation. Buoyancy calculation. of specimens of 12 species belonging to 8 genera including Homoceras, Aristoceras, and Vidrioceras from several fossil localities shows that the total shell densities at hatching remain almost constant among these species and can be approximated to that of seawater (=neutral buoyancy). These lines of evidence strongly suggest a similarity in the biostratinomic properties of empty shells between post-hatching juvenile stage and middle-late ontogeny. In all probability, in most Carboniferous Goniatitina, a newly hatched ammonoid had a nektobenthic or nektic mode of life, as has been postulated for adult animals.
Morphologic analysis was made on early whorls of two Paleozoic and 43 Mesozoic ammonoid species to obtain basic data on early life history. A positive linear relationship between protoconch and ammonitella sizes is recognized among the species examined. Total rotation angle of the ammonitella (ammonitella angle) seems to be independent of ammonitella size but has a significant negative linear relation with whorl expansion rate. This supports the model that the embryonic shell of ammonoids consists of gas-filled protoconch and the succeeding body whorl up to the primary varix. Growth analysis of siphuncle diameter in the early post-embryonic stage also indicates that the shell growth rates of the species hatched from large-sized eggs were smaller than those of species hatched from small-sized eggs. Authors
Records of Nautilus pompilius trapped in the Taon Strait, Negros Oriental, Philippines were kept for a 1 year period from August 1971 through August 1972, and ovaries of mature females collected from August 1971 through March 1972. Females averaged only 8% of the catch during the year of study, but were more abundant in catches from January through May. The male:female ratio was not markedly altered at any depth in the trapping range (61 to 300 m). During the 8 month period, there was no trend apparent in the changes in average size of the ovaries collected; however, oocytes within varied markedly in their maximum weight. Encapsulated spermatophores are stored above the buccal cone on the male, and are attached unencapsulated below the ventral cirri of the female. N. pompilius pairs kept at 80 m remained healthy but laid no eggs from September 1971 through May 1972.
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.