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.     

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 .     

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.     

Chamber growth in ammonites inferred from colour markings and naturally etched surfaces of Cretaceous vascoceratids from Nigeria

Cretaceous Vascoceras and Jurassic Lytoceras show colour markings and etched surfaces representing original organic membranes between the septa. The main difference between the formation of ammonite and Nautilus chambers involved the continuous secretion of a gelatinous cameral liquid to support the ammonite mantle when it moved forward. The gel containing cyclically secreted membranes. here named pseudosepta, resembled the intra-cameral structures of the cuttlebone in Sepia. Pseudoscpta are attached to the shell wall in pseudosutures (Pseudoloben) which are particularly visible in the saddles of the septal suture and tend to mimic them. Their shape suggests reconstruction of posterior mantle shape during translocation. Drag-bands (Schleppstreifen) are spiral markings formed by the overlapping pseudosepta along the axial traces of the foliole folds. The chamber of ammonites was formed by a locally muscular mantle in a tripartite cycle: (1) the mantle initially remained attached to the saddles of the completed septal suture while muscular tissue within the umbilical lobes was contracted and rapidly reattached to the side of the lateral saddles; (2) the whole mantle subsequently crept forward by secreting a gelatinous matrix which contained telescoped membranes, with an adhesive function on pseudolobc flanks; (3) the mantle almost ceased to move within the sites of future lobules, but expanded and crept on before forming the mural and 'gutter' ridges of the septum. □ Ammonites, chamber growth, vascoceratids, LYTOCERAS, Nigeria.     

LATE CAMBRIAN PLECTRONOCERID NAUTILOIDS AND THEIR ROLE IN CEPHALOPOD EVOLUTION

Abstract:  Numerous plectronocerid nautiloids appear in the Upper Cambrian of China. We have restudied their siphuncular structure, first described some 20 years ago. The siphuncle is characterized by: (1) long and holochoanitic septal necks dorsally but short and recurved necks laterally and ventrally; (2) strongly expanded connecting rings laterally; (3) two calcified layers in each connecting ring, outer spherulitic-prismatic and inner compact, the latter perforated by numerous pore canals; and (4) highly oblique siphuncular segments. The strongly expanded lateral sides of the connecting rings, together with the highly oblique course of the siphuncular segments, considerably enlarged the surface area of the connecting rings in each chamber, thereby increasing the transport capacity of cameral liquid. Thus, from their first appearance, plectronocerid nautiloids had developed a siphuncle for the replacement of cameral liquid with gases, and this system had a better and a more sophisticated design than that seen in stratigraphically younger nautiloids. However, their small orthoconic or slightly cyrtoconic shells were not well adapted for jet-powered swimming.     

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.     

Integrating 2D and 3D shell morphology to disentangle the palaeobiology of ammonoids: a virtual approach

Based on data derived from computed tomography, we demonstrate that integrating 2D and 3D morphological data from ammonoid shells represents an important new approach for investigating the palaeobiology of ammonoids. Characterization of ammonite morphology has long been constrained to 2D data, with only a few studies collecting ontogenetic data in 180° steps. Here we combine this traditional approach with 3D data collected from high‐resolution nano‐computed tomography. Ontogenetic morphological data on the hollow shell of a juvenile ammonite Kosmoceras (Jurassic, Callovian) was collected. 2D data was collected in 10° steps and show significant changes in shell morphology. Preserved hollow spines show multiple mineralized membranes never reported before, representing temporal changes in the ammonoid mantle tissue. 3D data show that chamber volumes do not always increase exponentially, as was generally assumed, but may represent a proxy for life events, such as stress phases. Furthermore, chamber volume cannot be simply derived from septal spacing in forms comparable to Kosmoceras. Vogel numbers represent a 3D parameter for chamber shape, and those for Kosmoceras are similar to other ammonoids (Arnsbergites, Amauroceras) and modern cephalopods (Nautilus, Spirula). Two methods to virtually document the suture line ontogeny, used to document phylogenetic relationships of larger taxonomic entities, were applied for the first time and present a promising alternative to hand drawings. The curvature of the chamber surfaces increases during ontogeny due to increasing strength of ornamentation and septal complexity. As this may allow for faster handling of cameral liquid, it could compensate for decreasing SA/V ratios through ontogeny.     

Soft‐tissue imprints in fossil and Recent cephalopod septa and septum formation

Several soft‐tissue imprints and attachment sites have been discovered on the inside of the shell wall and on the apertural side of the septum of various fossil and Recent ectocochleate cephalopods. In addition to the scars of the cephalic retractors, steinkerns of the body chambers of bactritoids and some ammonoids from the Moroccan and the German Emsian (Early Devonian) display various kinds of striations; some of these striations are restricted to the mural part of the septum, some start at the suture and terminate at the anterior limit of the annular elevation. Several of these features were also discovered in specimens of Mesozoic and Recent nautilids. These structures are here interpreted as imprints of muscle fibre bundles of the posterior and especially the septal mantle, blood vessels as well as the septal furrow. Most of these structures were not found in ammonoids younger than Middle Devonian. We suggest that newly formed, not yet mineralized (or only slightly), septa were more tightly stayed between the more numerous lobes and saddles in more strongly folded septa of more derived ammonoids and that the higher tension in these septa did not permit soft‐parts to leave imprints on the organic preseptum. It is conceivable that this permitted more derived ammonoids to replace the chamber liquid faster by gas and consequently, new chambers could be used earlier than in other ectocochleate cephalopods, perhaps this process began even prior to mineralization. This would have allowed faster growth rates in derived ammonoids.     

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.     

Composition and ontogeny ofDictyoconites (aulacocerida,cephalopoda)

Dictyoconites from the middle Triassic Cassian Formation is a characteristic representative of the Aulacocerida. Embryonic development and construction of the phragmocone is like that of Jurassic belemnites. The siphuncular tube is double-walled with a long retrochoanitic mineralized septal neck continuing into an organic tube. The extended decoupling zone resembles that ofSpirula. Characteristic ofDictyoconites are the tubular »living chamber« and two layered deposits of the muscular mantle on the phragmocone. The Triassic coleoid was a slender squid with visceral mass and mantle cavity encapsuled in shell and the whole conch covered by muscular mantle extending in two lateral apical fins attached to the aragonitic rostrum.     

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.     

The Evolution and Development of Cephalopod Chambers and Their Shape

The Ammonoidea is a group of extinct cephalopods ideal to study evolution through deep time. The evolution of the planispiral shell and complexly folded septa in ammonoids has been thought to have increased the functional surface area of the chambers permitting enhanced metabolic functions such as: chamber emptying, rate of mineralization and increased growth rates throughout ontogeny. Using nano-computed tomography and synchrotron radiation based micro-computed tomography, we present the first study of ontogenetic changes in surface area to volume ratios in the phragmocone chambers of several phylogenetically distant ammonoids and extant cephalopods. Contrary to the initial hypothesis, ammonoids do not possess a persistently high relative chamber surface area. Instead, the functional surface area of the chambers is higher in earliest ontogeny when compared to Spirula spirula. The higher the functional surface area the quicker the potential emptying rate of the chamber; quicker chamber emptying rates would theoretically permit faster growth. This is supported by the persistently higher siphuncular surface area to chamber volume ratio we collected for the ammonite Amauroceras sp. compared to either S. spirula or nautilids. We demonstrate that the curvature of the surface of the chamber increases with greater septal complexity increasing the potential refilling rates. We further show a unique relationship between ammonoid chamber shape and size that does not exist in S. spirula or nautilids. This view of chamber function also has implications for the evolution of the internal shell of coleoids, relating this event to the decoupling of soft-body growth and shell growth.     

Irregular calcareous sheets preserved in a conch of the Cretaceous ammonoid Hypophylloceras from Hokkaido,Japan

The mantle tissue is essential for understanding the diverse ecology and shell morphology of ammonoid cephalopods. Here, we report on irregular calcareous sheets in a well-preserved shell of a Late Cretaceous phylloceratid ammonoid Hypophylloceras subramosum from Hokkaido, Japan, and their significance for repairing the conch through the mantle inside the body chamber. The sheets are composed of nacreous layers arranged parallel to the irregularly distorted outer whorl surface. The nacreous sheets formed earlier are unevenly distributed and attached to the outer shell wall locally, whereas the last formed sheet covers a wide area of the outer shell wall. The absence of any interruption of ribbing around the irregular area suggests that these sheets were secreted inside the body chamber from the inner mantle. Gross morphological and X-ray computed tomography observations revealed that the spacing of septal formation was not affected by this event. The complex structure of the irregular sheets suggests a highly flexible mantle inside the body chamber.     

Empirical 3D model of the conch of the Middle Jurassic ammonite microconch Normannites: its buoyancy,the physical effects of its mature modifications and speculations on their function

A 3D model of the Middle Jurassic ammonoid Normannites with an apertural modification from Thürnen, Switzerland, was constructed using physical–optical tomography. It was tested to determine whether the formation of the apertural modification affected shell orientation, to estimate buoyancy regulation and to reconstruct the mode of life of this ammonoid. No drastic postural changes occurred between the 3D models that excluded and included lappets, suggesting that the lappets were not formed to change the syn vivo shell orientation and, in turn, locomotion. We speculate that these adult shell modifications served to protect the soft parts during the reproduction period. Buoyancy calculations based on the model assume that ammonoids were positively buoyant when the phragmocone was devoid of liquid. When 31% of the entire phragmocone was filled with liquid, the living animal would have reached neutral buoyancy in contrast to 27% of cameral liquid filling when the weight of the aptychi is included. Provided that smaller ammonoids had more cameral liquid than bigger ammonoids, such as the modern Nautilus, Normannites examined in this study would have been able to maintain neutral buoyancy and might have had a demersal, nektobenthic or nektonic habitat somewhere in the water column.     

Model for origin,function and fabrication of fluted cephalopod septa

The model supposes that sub-hemispheric septa of deep-water cephalopods evolved transverse pillars by meridional fluting in order to support flat and therefore weak areas of the shell wall. Several trends toward reduction of sutural spacing for improved wall support resulted in rise of fluting and finally, marginal crenulation. During ontogeny, the function of the ammonite septum as complex vault system against ”normal“ pressure from the body was succeeded by compound-pillar function for wall support. Fabrication of ammonitic septa probably involved positive pressure differential of new ”cameral“ liquid, orientation of mantle fibers along stress lines, and successively affixed tie-points which lay on an aponeurosislike mantle structure.     

The black layer in cephalopods from the German Muschelkalk (Triassic)

Thin, dark, probably phosphatic coatings were found on the dorsum in front of and sometimes behind the aperture of 50 specimens of Paraceratites and Ceratites (Ammonoidea) belonging to 14 species and subspecies and in three specimens of Germanonautilus , all from the Middle Triassic of Germany. The proportions, occurrences, position, outline, and preservation in fossil Nautiloidea and Ammonoidea (originally organic matter) of this structure support the hypothesis that it is homologous with the black layer in Recent Nautilus and Allonautilus . It is not yet possible to test whether these cephalopods show homologous styles of the development of these structures or whether the black layer can be identified in a common ancestor. In contrast to many ammonoids, Ceratites and Paraceratites , most Palaeozoic ammonoids, and some Mesozoic ammonoids probably did not have lower mandibles that were suitable for the closure of the aperture. They probably possessed a dorsally extending mantle (supracephalic mantle fold) and a hood, as in Recent Nautilus and Allonautilus , that was attached to the black layer. This interpretation is corroborated by a similar morphology of the black layer in an adult specimen of the nautilid Cenoceras from the South German Middle Jurassic and three specimens of Germanonautilus from the South German Middle Triassic (both Nautiloidea).     

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.     

Dark bands on pyritic internal moulds of the Early Jurassic ammonites Oxynoticeras and Cheltonia from Gloucestershire,England: interpretation and significance to ammonite growth analysis

Abstract: Thin, radiating, darker bands occur on pyritic internal moulds of the Early Jurassic ammonites Oxynoticeras and Cheltonia from Bishop’s Cleeve, Gloucestershire. They closely resemble true colour patterns preserved in Early Jurassic Calliphylloceras from Kutch, India, and false colour patterns reported in Carboniferous and Triassic ammonoids. Up to five dark bands occur within the body chamber, suggesting that they do not represent serially repeated anatomical structures, but the same feature repeatedly formed during growth. Dark bands are interpreted as traces of black bands deposited on the inside of the shell at the aperture during pauses in growth. The angles between dark bands and between septa correlate strongly in Cheltonia, suggesting that pauses in growth coincided with septal secretion during the chamber formation cycle. There are, however, no other indications that growth was episodic in either genus.