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.     

Growth trajectories of some major ammonoid sub‐clades revealed by serial grinding tomography data

Molluscs such as ammonoids record their growth in their accretionary shells, making them ideal for the study of evolutionary changes in ontogeny through time. Standard methods usually focus on two‐dimensional data and do not quantify empirical changes in shell and chamber volumes through ontogeny, which can possibly be important to disentangle phylogeny, interspecific variation and palaeobiology of these extinct cephalopods. Tomographic and computational methods offer the opportunity to empirically study volumetric changes in shell and chamber volumes through ontogeny of major ammonoid sub‐clades in three dimensions (3‐D). Here, we document (1) the growth of chamber and septal volumes through ontogeny and (2) differences in ontogenetic changes between species from each of three major sub‐clades of Palaeozoic ammonoids throughout their early phylogeny. The data used are three‐dimensional reconstructions of specimens that have been subjected to grinding tomography. The following species were studied: the agoniatitid Fidelites clariondi and anarcestid Diallagites lenticulifer (Middle Devonian) and the Early Carboniferous goniatitid Goniatites multiliratus. Chamber and septum volumes were plotted against the septum number and the shell diameter (proxies for growth) in the three species; although differences are small, the trajectories are more similar among the most derived Diallagites and Goniatites compared with the more widely umbilicate Fidelites. Our comparisons show a good correlation between the 3‐D and the 2‐D measurements. In all three species, both volumes follow exponential trends with deviations in very early ontogeny (resolution artefacts) and near maturity (mature modifications in shell growth). Additionally, we analyse the intraspecific differences in the volume data between two specimens of Normannites (Middle Jurassic).     

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.     

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.     

First direct evidence of ammonoid ovoviviparity

Ammonoids had high evolutionary rates and diversity throughout their entire history and played an important role in the high‐resolution sub‐division of the Mesozoic, but much of their palaeobiology remains unclear, including the brooding habitat. We present our study of the first recorded ammonite embryonic shell clusters preserved with calcified embryonic aptychi in situ within the body chambers of mature macroconch shells of the Early Aptian (Early Cretaceous) ammonite Sinzovia sazonovae. The following support the idea that the clusters are egg masses, which developed inside ammonite body chambers: the absence of post‐embryonic shells and any other fossils in these clusters, the presence of the aptychi in all embryonic shell apertures and peculiarities of adult shells preservation. These facts confirm earlier speculations that at least some ammonoids could have been ovoviviparous and that, like many modern cephalopods, they could have reproduced in mass spawning events. The aptychi of ammonite embryonic shells are observed here for the first time, indicating that they were already formed and calcified before hatching. Our results are fully congruent with the peculiar modes of ammonoid evolution: quick recovery after extinctions, distinct evolutionary rates, pronounced sexual dimorphism and the nearly constant size of embryonic shells through ammonoid history. We assume that adaptation to ovoviviparity may be the reason for the presence of these features in all post‐Middle Devonian ammonoids.     

Covariation of morphological characters in the Triassic ammonoid Czekanowskites rieberi

The Triassic ammonoid Czekanowskites rieberi displays a covariation of morphological charac ters, which is rather common in ammonoids. Its morphological spectrum ranges from laterally compressed, involute, weakly ribbed forms to depressed, semiinvolute, strongly ribbed forms. In order to study this covariation, fifteen axially cut specimens have been analyzed by means of image analysis, which allows us to obtain the ontogenetic record of radii, area and perimeter of the individual whorl cross-sections. A logarithmic model of growth has been applied. Our data indicate that, owing to the covariation, the radii from the origin to the venter and to the umbil ical seam of a given whorl section vary inversely in order to maintain the relative position of the center of gravity of the whorl cross-section both throughout the ontogeny of single specimens and within the population. This influences hydrostatic parameters, such as the position of the center of mass and the orientation and stability of the shell. Since the ontogenetic record of the angular length of the body chamber is not known, we have calculated those hydrostatic varia bles using two mutually exclusive assumptions: (1) the angular length of the body chamber was constant throughout ontogeny and (2) the volume of the body chamber grew monotonically with the revolution angle. Fluctuations of the three hydrostatic variables were always less important in the first assumption. In any case, the spectrum of, for example, theoretical orien tations is comparable to those observed in the species of present-day Nautilus. The range of adult body-chamber length observed in C. rieberi is much narrower than the theoretical adult body-chamber length calculated under the second assumption which indicates that a certain control over this parameter existed in the natural population, probably in order to maintain a narrow range in orientation and stability. The excess or deficit in soft-body weight was probably compensated by inverse variations in shell-wall weight. The main conclusion is that, despite the extreme morphological variability, hydrostatic and, possibly, hydrodynamic properties of the population remained within narrow limits.     

Iterative ontogenetic development of ammonoid conch shapes from the Devonian through to the Jurassic

We measured longitudinal growth in conch cross‐sections of 177 Devonian to Jurassic ammonoid species to test whether conch ontogenetic development parallels the iterative evolution of pachyconic or globular conch shapes. Ontogenetic trajectories of two cardinal conch parameters, conch width index and umbilical width index, show a few common recurring ontogenetic pathways in terms of the number of ontogenetic phases. The most common, with three phases in the conch width index (decrease–increase–decrease) and umbilical width index (increase–decrease–increase), is termed here C‐mode ontogeny (after the Carboniferous genus Cravenoceras). Many of the studied globular Palaeozoic and Triassic species (of the latter, particularly the arcestid ammonoids) share principal patterns in the triphasic C‐mode conch ontogeny in closely related groups but also between unrelated groups as well. The repetition of conch growth patterns is an example of convergent evolution of the entire life history of globular ammonoids. The studied Jurassic globular shaped ammonoids deviate from the growth patterns seen in earlier groups showing less pronounced ontogenetic trajectories with nearly isometric or weakly asymmetric growth without distinct phases. This trajectory is termed here M‐mode ontogeny (after the Jurassic genus Macrocephalites). No major change in the ontogenetic modes of pachyconic and globular ammonoids occurred moving from the Palaeozoic into the Mesozoic; the survivors of the end‐Permian extinction event iteratively developed conch ontogenies similar to those of Palaeozoic forms. In contrast, the Triassic–Jurassic boundary marks the major event with the evolution of some cardinal conch parameters relating to globular ammonoid ontogeny.     

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.     

Key innovations in Mesozoic ammonoids: the multicuspidate radula and the calcified aptychus

A nearly complete radula with seven elements per row preserved inside of an isolated, bivalved, calcitic lower jaw (= aptychus) of the Late Jurassic ammonite Aspidoceras is described from the Fossillagerstätte Painten (Bavaria, southern Germany). It is the largest known ammonite radula and the first record for the Perisphinctoidea. The multicuspidate tooth elements (ctenodont type of radula) present short cusps. Owing to significant morphological differences between known aptychophoran ammonoid radulae, their possible function is discussed, partly in comparison with modern cephalopod and gastropod radulae. Analogies between the evolution of the pharyngeal jaws of cichlid fishes and the ammonoid buccal apparatus raise the possibility that the evolution of a multicuspidate radula allowed for a functional decoupling of the aptychophoran ammonoid jaw. The radula, therefore, represents a key innovation which allowed for the evolution of the calcified lower jaws in Jurassic and Cretaceous aptychophoran ammonites. Possible triggers for this morphological change during the early Toarcian are discussed. Finally, we hypothesize potential adaptations of ammonoids to different feeding niches based on radular tooth morphologies.     

New representatives of the family Melagathiceratidae (Ammonoidea) from the Lower Triassic of South Primorye

A new ammonoid genus, Ussurijuvenites (Melagathiceratidae), is described from the early Olenekian of South Primorye, represented by two new species (U. popovi sp. nov. and U. artyomensis sp. nov.); data on the inner shell structure of melagathiceratid ammonoids (based on U. artyomensis sp. nov.) are presented for the first time.     

Untangling phylogenetic,geometric and ornamental imprints on Early Triassic ammonoid biogeography: a similarity‐distance decay study

Ammonoids are diverse and widespread fossil, externally shelled cephalopods that flourished for more than 300 Myr before their total extinction 65 Ma ago. In spite of two centuries of intensive scientific studies, their mode(s) of life and long‐distance dispersal abilities remain poorly known. Here, we address this by focusing on the latitudinal distribution of Early Triassic (approximately 250 Myr) ammonoids through similarity‐distance decay analyses. We examine and compare rates of similarity‐distance decay between various groups with respect to systematics, shell geometry and ornamentation to untangle phylogenetic, geometric and ornamental imprints on the observed biogeographical pattern. Our data do not support any phylogenetic and shell ornamentation influence, but rather demonstrate the significant effect of (sub‐)adult shell geometry on the similarity–distance decay: most evolute morphs tend to have been more endemic than most involute forms. This contrasts with the classic hypothesis that long‐distance ammonoid dispersal mainly occurred during the earliest planktonic stages, and thus that (sub‐)adult morphological characteristics should not constrain large‐scale biogeographical patterns of ammonoids. Although direct control by Sea Surface Temperature can be discarded, this result may indicate that at least some adult Triassic ammonoid morphs were skilled active swimmers capable of achieving long‐distance migration, as observed for some present‐day coleoid cephalopods. □Ammonoid, dispersal, similarity‐distance decay, morphology, phylogeny, biogeography, Triassic.     

Recent advances in heteromorph ammonoid palaeobiology

Heteromorphs are ammonoids forming a conch with detached whorls (open coiling) or non-planispiral coiling. Such aberrant forms appeared convergently four times within this extinct group of cephalopods. Since Wiedmann's seminal paper in this journal, the palaeobiology of heteromorphs has advanced substantially. Combining direct evidence from their fossil record, indirect insights from phylogenetic bracketing, and physical as well as virtual models, we reach an improved understanding of heteromorph ammonoid palaeobiology. Their anatomy, buoyancy, locomotion, predators, diet, palaeoecology, and extinction are discussed. Based on phylogenetic bracketing with nautiloids and coleoids, heteromorphs like other ammonoids had 10 arms, a well-developed brain, lens eyes, a buccal mass with a radula and a smaller upper as well as a larger lower jaw, and ammonia in their soft tissue. Heteromorphs likely lacked arm suckers, hooks, tentacles, a hood, and an ink sac. All Cretaceous heteromorphs share an aptychus-type lower jaw with a lamellar calcitic covering. Differences in radular tooth morphology and size in heteromorphs suggest a microphagous diet. Stomach contents of heteromorphs comprise planktic crustaceans, gastropods, and crinoids, suggesting a zooplanktic diet. Forms with a U-shaped body chamber (ancylocone) are regarded as suspension feeders, whereas orthoconic forms additionally might have consumed benthic prey. Heteromorphs could achieve near-neutral buoyancy regardless of conch shape or ontogeny. Orthoconic heteromorphs likely had a vertical orientation, whereas ancylocone heteromorphs had a near-horizontal aperture pointing upwards. Heteromorphs with a U-shaped body chamber are more stable hydrodynamically than modern Nautilus and were unable substantially to modify their orientation by active locomotion, i.e. they had no or limited access to benthic prey at adulthood. Pathologies reported for heteromorphs were likely inflicted by crustaceans, fish, marine reptiles, and other cephalopods. Pathologies on Ptychoceras corroborates an external shell and rejects the endocochleate hypothesis. Devonian, Triassic, and Jurassic heteromorphs had a preference for deep-subtidal to offshore facies but are rare in shallow-subtidal, slope, and bathyal facies. Early Cretaceous heteromorphs preferred deep-subtidal to bathyal facies. Late Cretaceous heteromorphs are common in shallow-subtidal to offshore facies. Oxygen isotope data suggest rapid growth and a demersal habitat for adult Discoscaphites and Baculites. A benthic embryonic stage, planktic hatchlings, and a habitat change after one whorl is proposed for Hoploscaphites. Carbon isotope data indicate that some Baculites lived throughout their lives at cold seeps. Adaptation to a planktic life habit potentially drove selection towards smaller hatchlings, implying high fecundity and an ecological role of the hatchlings as micro- and mesoplankton. The Chicxulub impact at the Cretaceous/Paleogene (K/Pg) boundary 66 million years ago is the likely trigger for the extinction of ammonoids. Ammonoids likely persisted after this event for 40–500 thousand years and are exclusively represented by heteromorphs. The ammonoid extinction is linked to their small hatchling sizes, planktotrophic diets, and higher metabolic rates than in nautilids, which survived the K/Pg mass extinction event.     

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.     

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 .     

Desmoceras (Pseudouhligella) intrapunctatum n. sp. (Ammonoidea) aus dem Unter-Albium von NW-Madagaskar mit Ritzstreifen

The new ammonoid speciesDesmoceras (Pseudouhligella) intrapunctatum (DesmoceratoideaZittel, 1895) is described and figured from the dark glauconitic marls of the Lower Albian of Ambatolafia (Mahajanga Basin of northwestern Madagascar). On the molds of its body chamber a well developed system of dotted lines is visible originally described from Palaeozoic ammonoids and nautiloids (= ?Ritzstreifen“Sandberger & Sandberger 1850 sensuTozer 1972). These internal shell structures have been originated by small ridges of the inner prismatic layer as the result of an incomplete mineralization. “Ritzstreifen” could not have observed in any other ammonoid species accompanied withDesmoceras (Pseudouhligella) intrapunctatum, despite of the same excellent aragonitic shell preservation. Therefore, this unique character is interpreted as taxonomically significant on species level.     

Ammonoid palaeobiology

This, the second in the series of virtual issues of Palaeontology, charts the development of concepts in ammonoid palaeobiology, with reference to nine selected papers published in this journal from 1965 onwards. These cover a broad range of topics: goniatite bed palaeoecology, systematics and evolution in Scaphites, flow dynamics of cephalopod shells, shell growth and differential geometry, septal function, ammonoid assemblage analysis, evolutionary trends, stratocladistics, and soft part preservation. Despite the growth and success of palaeobiological interpretations of ammonoid evolution, life, morphology and environments over the last 50 years, ammonoid research retains a great potential for the future.     

Intraspecific variation of hatchling size in Late Cretaceous ammonoids from Hokkaido,Japan: implication for planktic duration at early ontogenetic stage

Tajika, A. & Wani, R. 2011: Intraspecific variation of hatchling size in Late Cretaceous ammonoids from Hokkaido, Japan: implication for planktic duration at early ontogenetic stage. Lethaia, Vol. 44, pp. 287–298. Intraspecific variations of the early shell dimensions (ammonitella and protoconch diameters) of two Late Cretaceous (earliest Campanian) ammonoid species (Gaudryceras tenuiliratum and Hypophylloceras subramosum) from the Haboro and Ikushumbetsu areas, Hokkaido, Japan, show no significant difference between these areas that are approximately 110 km apart. The geographic distributions of G. tenuiliratum and H. subramosum are supposed to be mainly controlled by the flotation and transportation during the embryonic stage within floating egg masses and/or post‐embryonic stage because of their small hatchling sizes (1.18–1.46 mm in diameter for G. tenuiliratum, and 0.91–1.13 mm in diameter for H. subramosum), suggesting these two ammonite species at the embryonic and/or post‐embryonic stages were transported at least 110 km. Postulating that the velocity of palaeocurrent around the Haboro and Ikushumbetsu areas during the Cretaceous Period was 0.25 m/s, similar to those in the modern ocean current flowing off the eastern Pacific coast of Hokkaido, the egg masses and/or hatchlings of G. tenuiliratum and H. subramosum were buoyant and transported more than 5 days. The preliminary comparison of hatchling size through time suggests that the hatching sizes of H. subramosum in Hokkaido increased slightly from the Middle Turonian until the earliest Campanian (during about 7 Myr). □ammonoid, hatchling, paleoecology, variation, Cretaceous.     

Ontogenetic trajectories of septal spacing in Early Jurassic belemnites from Germany and France,and their palaeobiological implications

Based on well‐preserved belemnites, the ontogenetic trajectories of septal spacing between succeeding chambers were analysed. In the examined species (Passaloteuthis laevigata, Parapassaloteuthis zieteni and Pseudohasitites longiformis) that come from Buttenheim, Germany, and Lixhausen, France, the ontogenetic trajectories of septal spacing follow exponentially increasing trends with no decreasing phase of septal crowding during the earliest ontogenetic stage. The absence of a decreasing trend at the earliest ontogenetic stage is a unique character in contrast with those in modern cuttlefish and ancient and modern nautiloids, in which the decreasing trends are related to hatching events. These ontogenetic septal spacing trends suggest that the belemnite hatchlings had only a protoconch with no chamber. These belemnite hatchlings with no chamber and therefore small embryonic shell diameter are similar to those of ammonoids. Significant difference in a statistical test that compared the protoconch size between the two localities, might suggest that there was limited transportation at the embryonic stage, although it could also just indicate differences in regional environmental conditions, age and/or degree of time averaging which might differ between the examined taxa.     

Phylogenetic relationships of Early Triassic ammonoids (new data on the inner shell structure of some Olenekian ammonoids of Southern Primorye)

The inner shell structure for several ammonoid taxa (Inyoceras singularis, Anasibirites simanenkoi, A. nevolini, Yvesgalleticeras proximus, and Koninckitoides popovi) from the Olenekian of Southern Primorye is studied. The family-group level taxonomy of ammonoids is discussed.