The structure of the chambered nautilus siphuncle: The siphuncular epithelium

The siphuncle of the chambered nautilus (Nautilus macromphalus) is composed of a layer of columnar epithelial cells resting on a vascularized connective tissue base. The siphuncular epithelium taken from chambers that have not yet begun to be emptied of cameral liquid has a dense apical brush border. The great number of apical cell junctions (zonula adherens) compared to the number of nuclei suggests extensive interdigitation of these cells. The perinuclear cytoplasm of these preemptying cells is rich in rough endoplasmic reticulum. The siphuncular epithelium of both emptying and “old” siphuncle (which has already completed emptying its chamber) both show little rough endoplasmic reticulum but do contain extensive systems of mitochondria-lined infoldings of the basolateral plasma membranes. Active transport of NaCl into the extracellular space of this tubular system probably entrains the water transport involved in the chamber-emptying process. Both emptying and old siphuncular epithelium also show large basal infoldings (canaliculi) continuous with the hemocoel, which appear to be filled with hemocyanin. The apical cell junctions of emptying and old siphuncular epithelium contain septate desmosomes that may help to prevent back-flow of cameral liquid into the chambers.     

Cameral membranes in prolecanitid and goniatitid ammonoids from the Permian Arcturus Formation, Nevada, USA

We describe cameral membranes in prolecanitid and goniatitid ammonoids from the Lower Permian Arcturus Formation, Nevada, USA. The membranes are preserved as phosphatic sheets and were originally composed of organic material such as conchiolin. Because the phragmocones are filled with micritic calcite, the cameral membranes can be exposed by etching with weak acetic acid. The membranes are associated with the siphuncle and also coat the septal faces and chamber walls. The siphuncular membranes are much more extensive in the prolecanitids than in the goniatites. These membranes appear in the prolecanitids at the beginning of the third whorl, corresponding to a shell diameter of 3-4 mm, and become more complex through ontogeny. Additional membranes, called transverse membranes, appear in some of the septal saddles on the ventrolateral side. The siphuncular membranes in prolecanitids are very similar to those in the Ceratitina plus Mesozoic Ammonoidea, suggesting that such membranes are widely distributed in this group. However, the origin and function of these membranes are unclear. We argue that the siphuncular membranes were sequentially secreted by the rear mantle during forward movement of the body and were not produced by desiccation of cameral liquid after the formation of the chambers. The most compelling arguments for this interpretation are the abrupt appearance of these membranes at a shell diameter of approximately 3-4 mm in prolecanitids, ceratites, and ammonitids, coincident with the end of the neanic stage, and the uniform increase in complexity of the membranes through ontogeny. The shape of the siphuncular membranes in prolecanitids suggests the presence of an invagination on the dorsal side of the siphuncle during part of the chamber formation cycle. Cameral membranes may have served a variety of functions including stabilizing the cameral liquid to reduce rocking motion during swimming, anchoring the siphuncle to the chamber wall, and facilitating cameral liquid removal, permitting a faster rate of growth.     

SIPHUNCULAR STRUCTURE IN SOME FOSSIL COLEOIDS AND RECENT SPIRULA

Abstract: In Jurassic Phragmoteuthis huxleyi Donovan (Order Phragmoteuthida) the siphuncular wall shows unique structural and morphological features. The septal neck is short, about one‐eighth of chamber length, but the connecting ring is extremely long, extending through 5–6 chambers. The permeable siphuncular wall in each chamber is, therefore, unusually thick and consists of 5–6 consecutive connecting rings. Each connecting ring is calcified and has a highly porous structure in being composed of bundles of spicular crystallites, orientated more or less at right angles to the siphuncular wall, and separated by smaller or larger interspaces. A restudy of the belemnoid Megateuthis gigantea (Schlotheim) and the aulacoceratid Mojsisovicsteuthis? shows that the connecting rings in these taxa are also calcified. Each ring has a length of two chambers and consists of several calcified lamellae that are traversed by minute pores. The permeable siphuncular wall in each chamber therefore consists of two consecutive connecting rings separated by a porous prismatic layer. In Recent Spirula the connecting ring is composed of two layers: an outer spherulitic‐prismatic layer and an inner glycoprotein layer, of which the latter is not preserved in dry shells. The connecting ring structure is here similar to that in Recent Nautilus. Our study shows that at least three different structural types of siphuncular wall occur in coleoids. The phragmoteuthid connecting ring has a primitive structure, unknown in other cephalopods. This indicates that this taxon has no closer relationship with other coleoid taxa. The belemnitid‐aulacoceratid connecting ring is calcified and traversed by numerous pore canals. It shows a certain structural similarity to that in fossil actinoceratid and orthoceratid nautiloids. The spirulid connecting ring is structurally similar to that in Recent Nautilus and fossil nautilitid and tarphyceratid nautiloids. Thus the connecting ring structure indicates that coleoids include several, phylogenetically clearly separated lineages.     

Soft-part anatomy of the siphuncle in Permian prolecanitid ammonoids

Exceptionally well-preserved remains of phosphatized siphuncles were discovered in four specimens of a Permian prolecanitid ammonoid Akmilleria electraensis (Plummer and Scott) from Buck Mountain, Nevada. These structures occur as truncated segments within the siphuncular tube. The outer surface of the siphuncle is sculptured by numerous equally spaced longitudinal ridges and furrows; the ridges represent an infolded basement membrane of epithelial cells which corresponds to the distal ends of individual canaliculi between epithelial cells. In cross-section, the siphuncle of A. electraensis consists of a large central vein, possibly two pairs of arteries, porous connective tissue with reticulate hemocoelic spaces, and a thin epithelium. In the presence of two pairs of arteries and porous connective tissue, the siphuncle of A. electraensis is more like that of Nautilus pompilius than that of Spirula spirula, which has nine arteries and dense connective tissue. However, Nautilus possesses relatively smaller and more numerous epithelial cells around the siphuncle than does Akmilleria. These observations strongly suggest that the siphuncular epithelium of Akmilleria served as the salt-­concentrating organ for buoyancy regulation of the living animal, just as in Nautilus and Spirula.     

Post-mortem behaviour of Early Paleozoic nautiloids and paleobathymetry

It is unlikely that the intact or commonly preserved varieties of Ordovician-Silurian nautiloid shells were able to drift for any distance at the surface of the sea even if they died there. Their cameral capacity was much larger than the volume of the extracted or decayed body, and it would have contained a partial vacuum and cameral liquid when they were alive. The closely spaced and thin septa of the shallow-water adapted species were liable to buckle in compression and then implode in local tension during reverse hydrostatic loading by water pressure. This reverse loading and internal implosion of the septa was probably initiated by the sudden cameral refilling of an apical chamber caused by the depositional rupture of the apical siphuncle at or near the maximum habitat depth of these species. The instantaneous buckling of the more adorai septa was potentially terminated by variations in the septum thickness and cameral fill-fractions at that time, and they imply that some of the Silurian nautiloids from Bohemia were deposited at a minimum depth of about 65 m. Alternative interpretations involving the breakage of the same septa in tension, or buckling due to the difference in pressure between adjacent flooded chambers, set a maximum depth limit of about 160 m for the same facies. Many of the smaller Silurian nautiloids were unlikely to buckle during refilling, and they were potentially flooded faster than they could sink, below a depth of 100–300 m.     

Origin of intracameral sheets in ammonoids

The distribution, morphology and mutual relationships of cameral sheets in ammonoids are revised and re-evaluated. Taking into account recent models of ammonoid septum and chamber formation, three different origins can be attributed to the morphological types of sheets: (1) membranes replicated by the rear mantle (pseudosepta and septal linings), (2) membranes secreted sequentially and/or stretched across the chamber (horizontal membranes and chamber linings) and (3) products of desiccation of the cameral liquid (transverse and siphuncular sheets), presumably a cameral hydrogel. Sheets are always preserved near the siphuncular area, because as the cameral liquid was pumped out from the chamber it became progressively richer in dissolved mucus. In the last-formed drops, or menisci, this mucus adhered to the surface of the previously secreted sheets and, on dehydration, it also replicated the surface of the residual reservoirs, producing desiccation sheets. On the basis of the new evidence, changes in the shape of the rear mantle in Triassic ammonoids can be reconstructed. In general, deformations affected the rounded or bottle-neck saddles, which deflated after detachment of the last-formed septum and reinflated when the position of the next septum was reached. The rest of the elements of the septal epithelium were affected to a much lesser extent. One of the functions of those cameral sheets secreted by the rear body was related to a more efficient transport of the cameral liquid upon decoupling from the siphuncular tube. Ammonoids, Triassic, septum, chamber growth, cameral sheets.     

Function of calcium phosphate renal concrements in extant Nautilus: a paradigm for Cambrian-relict short-term mineral reserve equivalent to vertebrate bone

Renal uroliths (concrements) of calcium phosphate have long been known to exist in both growing and mature (non-growing) Nautilus specimens, but to date no evidence-based explanation for their existence has been available. The currently favored speculation is that they function as a calcium reserve for shell and septal calcification. Here we present new observational and experimental data that are consistent with the hypothesis that they serve as a mineral/ion reserve, allowing short-term (<1 day) addition of ionized calcium and phosphorus to blood and other body fluids, in a way analogous to that of vertebrate bone. In both in-ocean experiments and during long-term observation of captive nautiluses, concrements disappear during two different, energy-intensive activities involving removal of anions and cations from newly secreted cameral liquid in the chamber formation cycle, and during dives to depths requiring high osmotic pressures within the canaliculi of the siphuncular epithelium to keep previously emptied chambers from flooding due to suddenly increased ambient hydrostatic pressure. New concrements reappear at other points in the chamber formation cycle and when normal living depth is restored. The use of concrements as an ion reserve and the Cambrian ancestry of nautiloids indicate that Nautilus may exemplify a solution to the problem of energy supply in newly evolved swimmers of the Cambrian radiation independent of that seen in fish.     

Biological response to experimental damage of the phragmocone and siphuncle in Nautilus pompilius Linnaeus

Tsujino, Y & Shigeta, Y. 2012: Biological response to experimental damage of the phragmocone and siphuncle in Nautilus pompilius Linnaeus. Lethaia, Vol. 45, pp. 443–449. Three adult specimens of Nautilus pomplilius Linnaeus from the Philippines were experimented on to estimate the biological response to damage of the phragmocone and siphuncle in this cephalopod mollusc. In addition, the data obtained from the experiments were used for discussion of shell damage in ammonoids and in other extinct cephalopods. Specimen’s phragmocone and siphuncle were perforated and severed artificially, followed by observations in the laboratory tank during periods of 75 and 132 days. For at least 2 or 3 months, all individuals survived after damage to the phragmocone and siphuncle despite loss of neutral buoyancy. Based on our observations after completion of the experiments, the severed adoral remaining part of siphuncle healed by the siphunclar epithelium. In addition, perforation of the phragmocone was partly repaired by shell secretion from the dorsally extending mantle due to subsequent volution of shell growth. Our experiments revealed that damage to the phragmocone and siphuncle in Nautilus was not necessarily a lethal injury. It may be possible that such biological response also applies to extinct ammonoids and nautiloids. In a similar case of extinct ammonoids and nautiloids, damage to their phragmocone and siphuncle may also not have been a lethal injury as with Nautilus. However, some factors leading to death are likely to be dependent on the degree of damage to the phragmocone and siphuncle and influence of hydraulic pressure. □Ammonoids, injury, nautiloids, Nautilus, phragmocone, repair, siphuncle.     

Sutural inversion in a heteromorph ammonite and its implication for septal formation

The first known sutural inversion in ammonoids occurred in the adolescent stage of a late Cretaceous Glyptonoceras subcompressum (Forbes). Inversion has affected all folioles and lobules which are convex adapically instead of adorally, but not the tie-points from which they are 'suspended' and which shape the principal saddle and lobes. The ventral median saddle is also normal due to its proximity to the siphuncle. The partially inverted sutures are also strongly approximated. This suggests that, in this instance, body advance was mainly by muscular pull against a negative pressure differential of cameral liquid to 'ambient' body pressure across the septal mantle, owing to insufficient liquid in the newly forming chamber. Conversely, a slightly positive pressure differential is inferred for normal ammonitic septum formation. In spite of reversal, the length of folioles and lobules remains constant, indicating the existence of a 'permanent' sinuous attachment band resembling the posterior aponeurosis of Nautilus , with tie-points for primary wall attachment.     

河北秦皇岛地区奥陶纪奇壁角石科分子的发现及意义

奇壁角石科（Ａｌｌｏｔｒｉｏｃｅｒａｔｉｄａｅ）分子在我华北东部属首次发现。它产于马家沟组下部。界于Ｄｅｆｏｒｍｏｎ－ｃｅｒａｓ－Ｐｅｒｉｐａｔｏｃｅｒａｓ与Ｐｏｌｙｄｅｓｍｉａ－Ｗｕｔｉｎｏｃｅｒａｓ－Ｅｏｓｉｏｔｅｌｕｓ组合带之间偏下。奇壁角石科是Ｆｌｏｗｅｒ,Ｒ．Ｈ．１９９５年创立的,至今科内已建立６属１３种和３个相似种。但以往所描述标本绝大多数仅保存有部分内体管,对其它特征所知甚少。文中描     

On the efficiency of the buoyancy apparatus in ammonoids: evidences from sublethal shell injuries

The five greatest sublethal injuries were selected from a collection of more than 12,000 predominantly Mesozoic injured or otherwise pathological ammonoids. The loss of shell mass from these survived injuries was calculated and compared with comparable tolerances in the recent Nautilus . These ammonoids tolerated a shell loss up to four times greater than in Nautilus . The maximum tolerated shell loss indicates an unexpected buoyancy compensation mechanism. The buoyancy of the selected specimens was calculated. The results show that the buoyancy of all the observed ammonoid shells was positive. In order to maintain neutral buoyancy after injury, these ammonoids had to fill the phragmocone with a volume of mass. Nautilus compensated a maximum mass loss requiring a liquid refill of 3% of the cameral capacity, the ammonoids compensated a maximum of observed mass loss requiring a liquid refill of more than 10% of cameral capacity. The ratio of chamber volume/siphuncular surface area in the ammonoid Lithacoceras is 0.043, indicating that the relative area of the siphuncular epithelium in Lithacoceras is significantly higher when compared with a ratio of 0.12-0.14 in the adult Nautilus . The phragmocone in ammonoids offered the ability of a much more active buoyancy regulation than in Nautilus .     

Characterization of actinoceratoid cephalopods by their siphuncular structure

Partially phosphatized connecting rings show well-preserved structural details in the actinoceratoid Adamsoceras holmi (Ormoceratidae) from the Lower Ordovician (Kundan) of Estonia. Each connecting ring is composed of an outer, thin, spherulitic-prismatic layer, and an inner, thick, calcareous, lamellar layer, the latter being traversed by numerous large pores. The calcareous lamellar inner layer occurs in the connecting rings of three other actinoceratoids: Eushan-tungoceras pseudoimbricatum, Rayonnoceras solidiforme , and Huroniella sp. In Huroniella sp. and R. solidiforme , this layer is traversed by similar large pores as in Adamsoceras holmi , but in E. pseudoimbricatum the pores were probably too narrow to be recognized. The described structural type of the connecting rings, together with well-developed annular endosiphuncular deposits, are here considered as characteristic for actinoceratoids. The inflated connecting ring in actinoceratoids had a great surface area, which increased the number of pores across it. The permeability and emptying rates of the cameral liquid through the connecting ring could therefore have been as high or higher than that in Nautilus . In being composed of numerous calcified lamellae, the mechanical strength of the connecting ring against hydrostatic pressure could have also been the same or higher than that in Nautilus.     

Post-mortem descent with septal implosion in Silurian nautiloids

Late Silurian nautiloids from Bohemia have either (1) thin and densely spaced septa of which many are broken and internally accumulated, or (2) thick and widely spaced septa wnich are all intact. Since the latest chamber (s) and the shell wall are undamaged, septal fragmentation occurred by implosion during postmortem sinking, with sea water rushing in through the siphuncle. The latest connecting ring(s) were more permeable than the immature ones, permitting pressure compensation in the latest chamber(s). Septal debris accumulated adapically indicating the (ultimate) sinking orientation. Depth (maxima) of the nautiloid habitats and of the Bohemian basin are estimated from the strength parameters of the broken and intact septa: brevicones — epipelagic, weak longicones — moderately shallow pelagic, strong longicones — nektobenthic, sea floor depth — several 100 m. Silurian-Nautiloids-Shell-Connecting rings-Bathymetry.     

Early growth-stages and classification of orthoceridan Cephalopods of the Darriwillian (Middle Ordovician) of Baltoscandia

Five apices of orthoceridan cephalopods from the early Middle Ordovician Holen Limestone of Öland, Sweden that where collected in the late 19th Century by G. Holm provide information on cephalopod evolution in the early Palaeozoic. The apices belong to specimens of the genus Hedstroemoceras Foerste, 1930 and Archigeisonoceras Chen, 1984. The apices are small in comparison with apices of other cephalopods of the Ordovician; the initial chambers of the shells of both genera are hemispherical and approximately 1 mm and 1.5 mm in cross-section diameter, respectively. The apical 2–3 mm of the shell are free from growth-lines and possess no cicatrix, though distinct longitudinal wrinkles are present. There is a slight variability of siphuncle position during early growth in Archigeisonoceras. It can be shown that the structure of the connecting ring of Hedstroemoceras is similar to that of other Orthocerida. Additionally, the hemispherical apex of Lituites perfectus Wahlenberg, 1821 gives evidence for the orthoceridan affinity of lituitidans. The investigation shows that early Middle Ordovician Orthocerida display a characteristic connecting ring structure, a characteristic apex morphology and variable siphuncular positions that differs significantly from other cephalopods of the Ordovician. Based on this evidence it is concluded that a small spherical apex is an autapomorphy of the Orthocerida. Moreover, this evidence supports a splitting of the order Orthocerida in two taxa of different affinities. The Orthocerida sensu stricto comprises orthocones with a tubular siphuncle nearly without endospiphuncular deposits, and a spherical apex. Embryonic shell, orthoceridan ancestry, orthoceridan classification.     

The connecting rings of Nautilus and Mesozoic ammonoids: implications for ammonoid bathymetry

The fresh conchiolinous ('horny') connecting rings of Nautilus pompilius decrease ontogcnctically in the strength index (100 times; wall thicknessh/inner radius r), i.e. from ≥ 16 to – 12. A similar decrease of 100 h/ r is the rule in Ammonitina. This may reflect depth migration but, more likely and in analogy with Nautilus, is compensated for by increased conchiolin strength. The mature ammonoid siphunclc, therefore, provides the more reliable indicator for depth limits. No marked shrinkage of connecting rings is evident in fossil nautiloids, but Mesozoic nautilid connecting rings are rarely preserved. Post-mortem alteration of the abundantly preserved ammonoid connecting rings entails mechanical distortion and fragmentation by differential filling of the siphunclc and camerac with sediment, and probable microbial decomposition, proceeding from the body chamber and resulting in pitting and perforation; shrinkage occurred rarely. This is probably related to the high phosphate content as here documented for Haplo-phylloceras. If the phosphate prevalent in ammonoid connecting rings is a primary constituent, rather than of early diagenetic origin, calibration of the ammonoid strength index on the non-phosphatic Nautilus connecting rings may not be justified. The strength indices of ammonoid connecting rings would thus provide only a relative scale of depth limits. Another example of a phylloccratid, Ptychophylloceras, has been found with a connecting ring extending well into the body chamber. D Connecting rings, ammonoids. Nautilus, bathymetry.     

The siphuncle in Georginidae and other Ordovician actinoceroid cephalopods

The lower Middle Ordovician carbonate sediments of the Georgina Basin in Australia contain many and varied Actinoceratida, including an endemic family, Georginidae Wade (1977), with siphuncular calcification consisting of radial lamellae separated by spaces (now sediment-filled) enclosed within calcified annulus walls. In each segment a distinct series of more massive calcareous engrafts grows inward from the inside of the connecting ring and is engrafted into adjacent annuli across the interannulus; this divides the perispatium into longitudinal perispatial sinuses. At each extremity each perispatial sinus is connected with passages leading through the segments to the axial space and, nearer to, or at the interannulus, with radial canals. Axial canals are few, but more than one is normal. Good preservation of Armenoceras and Actinoceras allows recognition of similar structures in the annuli of normal Actinoceratida.     

Connecting stripes: An organic skeletal structure in Sepia from Red Sea

The skeletal structure, herein termed “connecting stripes”, is demonstrated in dried cuttlebones of Sepia (Acanthosepion) savignyi de Blainville from the Gulf of Aqaba, Red Sea, Eilat, Israel. This structure consists of segmented chitinous strip-like sheets covering the outside opening to the cuttlebone chambers. Scanning electron microscope images demonstrate that the connecting stripes are tightly attached to the neighbouring septa along the septal edges and do not continue from one chamber to the next. When broken, they leave band-like remnants along the attachment sites. The connecting stripes consist of fibrous, organic, possibly mainly chitinous, laminas. Chemical analysis using energy dispersive spectrometry shows that the connecting stripes contain C, O, Na, K but lack Ca and P. The connecting stripes show perceptible, usually barely visible micropores with diameter of ca. 0.1 μm; distances between the micropores are 0.2 to 0.3 μm. The connecting stripes in Sepia are similar to connecting rings in bactritoids and ammonoids in having a segmented structure and a non-mineralized, organic composition. The microporosity of connecting stripes observed in Sepia has been also recorded in three genera of Mesozoic ammonoids. The connecting stripes may serve as a transport route of the cameral liquid in and out of the chambers and are considered to be a homologue of the connecting rings in cephalopods with a fully developed siphonal tube.     

Septal implosion in Late Carboniferous coiled nautiloids from Ohio

Mapes, R.H. & McComas, G.A. 2010: Septal implosion in Late Carboniferous coiled nautiloids from Ohio. Lethaia, 10.1111/j.1502–3931.2009.00213.x More than 200 relatively mature coiled nautiloid specimens, assigned to Metacoceras mcchesneyi, were recovered from an Upper Carboniferous shale in northeastern Ohio. Twenty‐seven undistorted specimens reveal that the septa in every specimen were collapsed and/or telescoped. This septal collapse without external shell distortion could only have been accomplished by limited implosion due to excessive pressure. Analysis of the fossils, sediment and the depositional environment indicate that after burial, the nautiloid cameral spaces were probably filled with both liquid and gas, and the body chamber was filled with semi‐solid thixotropic mud. To prevent conch collapse at the time of septal implosion, the thixotropic mud filling the nautiloid body chamber acted as a liquid at the time of stress release during septal failure. The stress was produced by combined lithostatic and hydrostatic pressures, which fluidized the unlithified thixotropic mud that flowed from the body chamber into the phragmocone during septal collapse. After the septal implosion and when flowage ceased, the thixotropic mud quickly resolidified into a solid state providing internal conch support that prevented the collapse of the conch. □Carboniferous, nautiloids, septal implosion, taphonomy, thixotropic mud.     

Eridites undulatum壳体微细构造

利用偏光显微镜及扫描电子显微镜观察了假直角石类Ｅｒｉｄｉｔｅｓｕｎｄｕｌａｔｕｍ的体管沉积及气室沉积微细构造特征,体管沉积内部有机质层及矿物晶体层形态及厚度较稳定。气室沉积中有机质层及矿物晶体层形态及厚度变化大,晶体层内部具有柱状晶体。基于内部微细构造特征,推测体管沉积由软体上皮细胞直接分泌而成,气室沉积由体液渗透连接环在气室内表面上形成矿化基质后通过有机质层及矿物晶体层不断加积而成。另外,通过与石炭纪其它假直角石类内部沉积微细构造特征的比较,认为假直角石类内部沉积的微细构造特征不具有分类学意义。