Thriving at high hydrostatic pressure: the example of ammonoids (extinct cephalopods)

Ammonoids are a group of extinct mollusks belonging to the same class of the living genus Nautilus (cephalopoda). In both Nautili and ammonoids, the (usually planospiral) shell is divided into chambers separated by septa that, during their lifetime, are filled with gas at atmospheric pressure. The intersection of septa with the external shell generates a curve called the suture line, which in living and most fossil Nautili is fairly uncomplicated. In contrast, suture lines of ancient ammonoids were gently curved and during the evolution of the group became highly complex, in some cases so extensively frilled as to be considered as fractal curves. Numerous theories have been put forward to explain the complexity of suture ammonoid lines. Calculations presented here lend support to the hypothesis that complex suture lines aided in counteracting the effect of the external water pressure. Additionally, it is suggested that complex suture lines diminished shell shrinkage caused by water pressure, and thus aided in improving buoyancy. Understanding the reason for complex sutures in ammonoids represents an important issue in paleobiology with potential applications to the problem of the resistance of hollow mechanical structures subjected to high pressure.     

Morphostructural constraints and phylogenetic overprint on sutural frilling in Late Jurassic ammonites

The functional significance of frilled septa and complex sutures in ammonoids has generated ongoing debate. The 'classic' hypothesis envisages ammonoid shells and septa as designed for resisting ambient hydrostatic pressure, complex sutures being the evidence of strength in shells for colonization of deep habitats. Here we address the 'suture problem', focusing on the analysis and interpretation of variables in our database of Late Jurassic ammonites not included in previous studies, such as whorl height ( W h ), whorl shape ( S ), shell coiling ( WD ), taxonomic grouping and basic planispiral shell shape. The results indicate that sutural complexity, as measured by the fractal dimension ( D f ) value of the suture line, is positively correlated with W h , and that the sutures of oceanic shells tend to provide, for a given W h value, lower D f estimates than do those of neritic shells. No general trend of increase in sutural complexity was noted for specimens recovered from swell areas belonging to oceanic fringes with respect to those that inhabited epicontinental shelves. In fact, Perisphinctoidea, the clade best represented in the database analysed, shows a higher D f mean value in neritic species than in epioceanic ones. Significant differences in sutural complexity were detected for groups of ammonites classified according to shell shapes ( WD , S ). Oxycones and discocones, streamlined potential swimmers, show the highest D f mean values, while spherocones and cadicones, which were presumably vertical vagrants, present the lowest ones. This indicates that sutural complexity was more related to shell geometry than to bathymetry.     

Mechanische Simulation und funktionelle Evolution des Ammoniten-Septums

Simulation of nautiloid and ammonoid septa and suture lines illustrates the fabricational constraints and possibilities that controlled their evolution towards the paradigm of a pressure resistant structure.     

Buckman's Paradox: variability and constraints on ammonoid ornament and shell shape

Buckman's Law of Covariation states that ammonoid shell shape and ornamentation are typically correlated, such that compressed, involute forms have light ornament while more inflated, evolute forms have heavier ornament. Such covariation has been observed in many ammonoid groups, and implies a link between the morphogenesis of shell shape and ornamentation. However, other evidence suggests that while ornament growth is controlled by the genetic‐developmental program of the ammonoid, shell shape is strongly influenced by environmental factors. These differing viewpoints lead to Buckman's Paradox – are ornamentation and shell shape tightly linked, as implied by Buckman's covariation, or is the morphogenesis of ornament controlled genetically, while shell shape is controlled environmentally? To address this issue, the variability of shell shape and rib morphology has been compared for a group of endemic acanthoceratid ammonites from the Cretaceous Western Interior Seaway of North America. If Buckman's Law holds due to a morphogenetic connection between shell shape and ornamentation, we would expect taxa with more variable shell shapes to also show more variable rib features and growth. Morphometric analysis of seven shell shape and two rib characters for the Western Interior acanthoceratids finds no such correlation, suggesting that shell shape and rib growth are controlled by different processes. Indeed, rib growth appears to be more constrained than shell shape, consistent with the view that ornamentation is more tightly controlled by the developmental‐genetic growth program of the ammonoid. These results emphasize the complexity of ammonoid morphogenesis and highlight our limited understanding of the causes underlying Buckman's Law.     

Buoyancy of some Palaeozoic ammonoids and their hydrostatic properties based on empirical 3D‐models

The interpretation of the function of the ammonoid phragmocone as a buoyancy device is now widely accepted among ammonoid researchers. During the 20^th century, several theoretical models were proposed for the role of the chambered shell (phragmocone); accordingly, the phragmocone had hydrostatic properties, which enabled it to attain neutral buoyancy, presuming it was partially filled with gas. With new three‐dimensional reconstructions of ammonoid shells, we are now able to test these hypothetical models using empirical volume data of actual ammonoid shells. We investigated three Palaeozoic ammonoids (Devonian and Carboniferous), namely Fidelites clariondi, Diallagites lenticulifer and Goniatites multiliratus, to reconstruct their hydrostatic properties, their syn vivo shell orientation and their buoyancy. According to our models, measurements and calculations, these specimens had aperture orientations of 19°, 64° and 125° during their lives. Although none of our results coincide with the aperture orientation of the living Nautilus, they do verify the predictions for shell orientations based on published theoretical models. Our calculations also show that the shorter the body chamber, the poorer was the hydrodynamic stability of the animal. This finding corroborates the results of theoretical models from the 1990s. With these results, which are based on actual specimens, we favour the rejection of hypotheses suggesting a purely benthonic mode of life of ammonoids. Additionally, it is now possible to assess hydrodynamic properties of the shells through ontogeny and phylogeny, leading to insights to validate theoretical modes of life and habitat through the animal's life.     

Large‐scale evolutionary trends of Acrochordiceratidae Arthaber, 1911 (Ammonoidea,Middle Triassic) and Cope’s rule

Abstract: Directed evolution of life through millions of years, such as increasing adult body size, is one of the most intriguing patterns displayed by fossil lineages. Processes and causes of such evolutionary trends are still poorly understood. Ammonoids (externally shelled marine cephalopods) are well known to have experienced repetitive morphological evolutionary trends of their adult size, shell geometry and ornamentation. This study analyses the evolutionary trends of the family Acrochordiceratidae Arthaber, 1911 from the Early to Middle Triassic (251–228 Ma). Exceptionally large and bed‐rock‐controlled collections of this ammonoid family were obtained from strata of Anisian age (Middle Triassic) in north‐west Nevada and north‐east British Columbia. They enable quantitative and statistical analyses of its morphological evolutionary trends. This study demonstrates that the monophyletic clade Acrochordiceratidae underwent the classical evolute to involute evolutionary trend (i.e. increasing coiling of the shell), an increase in its shell adult size (conch diameter) and an increase in the indentation of its shell suture shape. These evolutionary trends are statistically robust and seem more or less gradual. Furthermore, they are nonrandom with the sustained shift in the mean, the minimum and the maximum of studied shell characters. These results can be classically interpreted as being constrained by the persistence and common selection pressure on this mostly anagenetic lineage characterized by relatively moderate evolutionary rates. Increasing involution of ammonites is traditionally interpreted by increasing adaptation mostly in terms of improved hydrodynamics. However, this trend in ammonoid geometry can also be explained as a case of Cope’s rule (increasing adult body size) instead of functional explanation of coiling, because both shell diameter and shell involution are two possible paths for ammonoids to accommodate size increase.     

<Emphasis Type="Italic">Goniatites sphaericus</Emphasis> (Sowerby, 1814), the archetype of Palaeozoic ammonoids: a case of decreasing phenotypic variation through ontogeny

The Late Viséan (Early Carboniferous) ammonoid species Goniatites sphaericus (Sowerby, 1814) is revised with the use of the type material. With respect to conch morphology, suture line and particularly shell ornament, it is regarded as a senior synonym of the species Goniatites fimbriatus (Foord and Crick, 1897) and must therefore be re-established as an important index fossil for the ammonoid stratigraphy of the Rhenohercynian and Subvariscan shelves. The Goniatites fimbriatus Zone has been re-named Goniatites sphaericus Zone on this basis. The study of ontogenetic changes in the conch parameters shows that intraspecific variation occurs within a wide range. In the whorl profile, variation is very high in small juveniles, while in the coiling rate, intermediate growth stages are more strongly affected.     

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.     

Meta-analysis of character utility and phylogenetic information content in cladistic studies of ammonoids

While previous workers have argued persuasively that ammonoid workers should use cladistic approaches to reconstruct phylogeny, relatively few cladistic studies have been published to date. An essential yet challenging part of cladistic analysis is the selection of characters. Are certain types of characters more likely to show homoplasy? Are certain aspects of shell anatomy more likely to contain phylogenetically informative characters? Are datasets with more characters inherently better? To answer these questions, a meta-analysis of character data from published ammonoid phylogenies was performed. I compiled 14 datasets, published between 1989 and 2007, representing parsimony-based phylogenetic analyses of ammonoids. These studies defined a combined total of 323 characters, which were grouped into categories reflecting different aspects of anatomy: shell size and shape, ornament, suture, early ontogeny, body chamber and apertural modifications. Tree searches were re-run to determine overall tree statistics, parsimony permutation tail probability (PTP) tests were calculated to assess the phylogenetic information content of the matrices, and retention and rescaled consistency indices for each character were calculated. My analyses revealed that studies with higher character/taxon ratios did not necessarily produce trees with more information content and less homoplasy, as measured by retention or rescaled consistency indices, because additional characters were often parsimony-uninformative. Rather, studies with relatively few characters could produce high-quality trees if the characters were well-chosen and character states carefully defined. Characters related to the body chamber and adult aperture typically had retention indices of either 0 or 1, rarely in between, indicating that they either worked perfectly or not at all. Suture characters tended to have higher indices than shell shape or ornament characters, suggesting more phylogenetic information and less homoplasy in the suture line than in shell traits. These results should aid in the selection of characters for future cladistic studies of ammonoids.     

The development of ammonoid septa: An epithelial invagination process controlled by morphogens?

Suture lines are important in ammonoid taxonomy. Their complex morphologies, caused by iterated invaginations of the posterior body wall, can be explained using a mechano‐chemical model inspired by modem developmental models for epithelial folding in kidneys, lungs, teeth, mammary glands and other organs. A morphogen, organized to form a regular spacing pattern by reaction‐diffusion dynamics or similar processes, induces changes in cell shape and/or rate of proliferation, causing invagination and the formation of lobes. Interactions between mechanical and chemical effects, combined with expanding size due to overall growth, produce a “fractal”; pattern of smaller (secondary) invaginations superimposed on larger (primary) ones. The pattern of increasing sutural complexity that is observed in ammonoid evolution may be a simple heterochronic effect, that allowed iterated invagination to be extended to higher and higher levels of folding. In contrast with some earlier theories, the present model is based on the view that the development of ammonoid septa must have been under relatively strict genetic control.     

Calvarial suture interdigitation in hadrosaurids (Ornithischia: Ornithopoda): Perspectives through ontogeny and evolution

Lambeosaurine hadrosaurids exhibited extreme modifications to the skull, where the premaxillae, nasals, and prefrontals were modified to form their iconic supracranial crests. This morphology contrasts with their sister group, Hadrosaurinae, which possessed the plesiomorphic arrangement of bones. Although studies have discussed differences between lambeosaurine and hadrosaurine skull morphology and ontogeny, there is little information detailing suture modifications through ontogeny and evolution. Suture morphology is of particular interest due to its correlation with the mechanical loading of the skull in extant vertebrates. We quantify and contrast the morphology of calvarial sutures in iguanodontians and ontogenetic series of Corythosaurus and Gryposaurus to test whether the evolution of lambeosaurine crests impacted the mechanical loading of the skull. We found that suture interdigitation (SI) increases through ontogeny in hadrosaurids, although this increase is more extreme in Corythosaurus than Gryposaurus, and overall suture complexity (i.e., overall shape) remained constant. Lambeosaurines also have higher SI than other iguanodontians, even in crestless juveniles, suggesting that increased sinuosity is unrelated to the structural support of the crest. Hadrosaurines and basal iguanodontians did not differ. Similarly, lambeosaurines have more complexly shaped sutures than hadrosaurines and basal iguanodontians, while the latter two groups do not differ. Taken together, these results suggest that lambeosaurine calvarial sutures are more interdigitated than other iguanodontians, and although suture sinuosity increased through ontogeny, the suture shape remained constant. These ontogenetic and evolutionary patterns suggest that increased suture complexity in lambeosaurines coincided with crest evolution, and corresponding modifications to their facial skeleton altered the distribution of stress while feeding.     

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.     

Sutural complexity and bathymetry in ammonites: fact or artifact?

The widespread assumption that sutural complexity in ammonites is mainly proportional to water depth is revisited. Fractal analysis has been used for the precise morphometric evaluation of sutural complexity in 131 Upper Jurassic ammonites. Suture lines belonging to twelve families have been analyzed, account being taken of shell structure (coiling, shape of whorl section), sculpture and paleoenvironments. Fractal dimensions obtained in epicontinental and epioceanic ammonites show the unlikelihood of precise relationships between suture complexity and depth, and/or the absence of major differences in habitat depth if bathymetry played any significant role in the configuration of intricate septa. Suture complexity appears to be better related to shell structural types. □ Fractal analysis, ammonite sutures, Upper Jurassic.     

Shell features, main colonized environments, and fractal analysis of sutures in Late Jurassic ammonites

A precise approach to the quantification of relationships between suture complexity, as measured by fractal analysis (step-line procedure), the architecture of shells, and the main colonized environments, has been made in a set of Late Jurassic ammonites ( N =507). Statistically significant differences between fractal-dimension ( D _f) mean values of evolute and involute shells are interpreted as caused by differences in the surface:volume ( S:V ) ratio. Suture complexity is also related to the shape of whorl section. The lowest D _f values correspond to subcircular whorl sections (low S:V ratio) and the highest ones to acute sections (high S:V ratio). The shape of flanks shows correlation with suture complexity. The highest values of D _f are found in planulate shells and the lowest ones in whorl cross sections with convex flanks. Highly significant differences appear between D _f mean values from unsculptured shells and those from ammonites with ribs and/or tubercles of medium to large size. Multivariate analysis shows a combined variation of shell features and suture complexity, resulting in a heterogeneous distribution of D _f values within the ammonite morphospace, mainly according to structural (shell architecture) and ornamental (sculpture strength rather than density) factors. Finally, the data obtained on relationships between suture complexity and the colonized environments (epicontinental vs. epioceanic inhabitants) suggest that suture complexity is not primarily related to bathymetry, and/or that no major differences in habitat depths existed between epicontinental and epioceanic ammonites.     

Post-hatching early life history of Cretaceous Ammonoidea

Post-hatching early life histories in Cretaceous Ammonoidea are discussed on the basis of density calculations of the shells in 71 species belonging to four separate suborders. The calculation was made under the assumption that a newly hatched ammonoid had a gas-filled chamber and a succeeding body-filled whorl terminating at the primary constriction. The results show that the density of the species examined at the hatching stage is almost constant and is relatively smaller than that of seawater, i.e. the animals are positively buoyant. This fact strongly suggests a planktic mode of life. In all species, the density increases gradually with growth and attains neutral buoyancy at 2.C2.5 mm in shell diameter. Thus, most ammonoids probably changed their mode of life from planktic to nektoplanktic or nektobenthic at this critical point. The rare occurrence of newly hatched specimens (ammonitellas) in many ammonoid assemblages may also support this interpretation. Planktic duration of a newly hatched ammonoid might be regulated by the animal's density at hatching, shell growth pattern, cameral volume (or hatching size), and rate of cameralliquid removal (or siphuncle diameter). The latter two seem to be very important factors in determining the biogeographical framework of species, as demonstrated in the Tetragonitaceae.□ Cretaceous, Ammonoidea, density calculation, early life history .     

Sutural amplitude of ammonite shells as a paleoenvironmental indicator

The Sutural Amplitude Index (SAI), obtained by measuring the maximum height of sutural elements and the length of the suture pattern on ammonoid shells, provides a useful indicator of relative habitat depth for ammonoids with similar shell morphotypes. A higher SAI indicates greater septal support for the shell wall against implosion under increased hydrostatic pressures in deeper waters. Relating the sutural amplitude indices of ammonites found in a well-studied depositional basin, such as the Cretaceous Western Interior Seaway, to morphotype distributions illustrates the utility of this index in bathymetric interpretations. □ Ammonoidea, sutures, Sutural Amplitude Index, Cretaceous, Greenhorn Cyclothem. Western Interior.     

L’évolution chez les Phyllocerataceae,la variabilité des paramètres dimensionnels et relatifs. Variabilité de la complexité de la ligne cloisonnaire: Variabilité et paedomorphose

Evolution of the Phyllocerataceae, the variability of the dimensional and relative parameters. Variability of the complexity of the suture line. Variability and paedomorphosis. A recent study has shown the importance of heterochronies in the development of Phyllocerataceae. It was attractive to estimate with precision the variability of some morphological characters of the shell and of the suture line in order to study how this variability changed in the course of time (from Jurassic to terminal Cretaceous). This note gives the averages of the calculations of variability in dimensional and relative variables in the shell of Phylloceratidae and variability in the complexity C of their suture lines. Coefficient of variation V is the statistical parameter used here, because it allows the comparison between the dispersions of different populations. This study shows that the variability of the complexity in the suture line and h₁ + h₂ is more fluctuating among the taxa (usually subfamilies, genera and species) in which heterochrony is evident. On the other hand, the variability of other parameters (V₁, V₂, D) first grows and then slowly decreases till the branch or the lineage is extinct. This schema is mostly acceptable down to the Lower Cretaceous-Upper Cretaceous in the Tethys and in the marine shelf of Gondwana. In the family of Neophylloceratidae, very clearly in the Tethys, less clearly in marine shelf of Gondwana (it is less obvious in the genus Phyllopachyceras), the variability grows as far as the terminal Cretaceous. The extinction of this family may result from a catastrophic event and not from internal causes. In short, the decrease of variability comes before the extinction of the taxa and consequently it agrees with a Darwinian classic schema. On the other hand, the extinction of Neophylloceratidae that occurs when the variability is maximal probably takes place in another perspective, an external « catastrophic » event. To cite this article, B. Joly, C.R. Palevol 2 (2003).     

Cranial Suture Morphology and its Relationship to Diet in Cebus

Cranial sutures are complex morphological structures. Four Cebus species (C. albifrons, C. apella, C. capucinus, C. olivaceus) are used here to test the hypothesis that sagittal suture complexity is enhanced in animals that eat materially challenging foods. These primates are ideal for such comparative studies because they are closely related and some are known to exhibit differences in the material properties of the foods they ingest and masticate. Specifically, Cebus apella is notable among members of this genus for ingesting food items of high toughness as well as consistently demonstrating a relatively robust cranial morphology. Consistent with previous studies, C. apella demonstrates significantly more robust mandibular and temporal fossa morphology. Also, C. apella possesses sagittal sutures that are more complex than congenerics. These data are used to support the hypothesis that cranial suture complexity is increased in response to consuming diets with more obdurate material properties. One interpretation of this hypothesis is that, compared to non-apelloids, total strain in the apelloid cranial suture connective tissue environment is elevated due to increased jaw muscle activity by increases in either force magnitudes or the number of chewing events. It is argued that greater masticatory function enhances the growth and modeling of cranial suture interdigitation. These data show that cranial suture complexity is one more hard tissue feature from the skull that might be used to inform hypotheses of dietary functional morphology.     

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.