Ontogeny of highly variable ceratitid ammonoids from the Anisian (Middle Triassic).

Ammonoids reached their greatest diversity during the Triassic period. In the early Middle Triassic (Anisian) stage, ammonoid diversity was dominated by representatives of the family Ceratitidae. High taxonomic diversity can, however, be decoupled from their morphologic disparity. Due to its high phenotypic variability, the high diversity of ceratitids of the Anisian of Nevada was initially assumed to be caused by artificial over-splitting. This study aims to contribute data to settle this issue by applying geometric morphometrics methods, using landmarks and semi-landmarks, in the study of ontogenetic cross-sections of ammonoids for the first time. The results reveal that alterations in ontogenetic trajectories, linked to heterochronic processes, lead to the morphologic diversification of the species studied herein. Our knowledge, based on these ontogenetic changes, challenge the traditional treatment of species using solely adult characters for their distinction. This study furthermore demonstrates that the high diversity of the Anisian ammonoid assemblages of Nevada based on the traditional nomenclatoric approach is regarded to be reasonably accurate.

Suppressed competitive exclusion enabled the proliferation of Permian/Triassic boundary microbialites.

During the earliest Triassic microbial mats flourished in the photic zones of marginal seas, generating widespread microbialites. It has been suggested that anoxic conditions in shallow marine environments, linked to the end-Permian mass extinction, limited mat-inhibiting metazoans allowing for this microbialite expansion. The presence of a diverse suite of proxies indicating oxygenated shallow sea-water conditions (metazoan fossils, biomarkers and redox proxies) from microbialite successions have, however, challenged the inference of anoxic conditions. Here, the distribution and faunal composition of Griesbachian microbialites from China, Iran, Turkey, Armenia, Slovenia and Hungary are investigated to determine the factors that allowed microbialite-forming microbial mats to flourish following the end-Permian crisis. The results presented here show that Neotethyan microbial buildups record a unique faunal association due to the presence of keratose sponges, while the Palaeotethyan buildups have a higher proportion of molluscs and the foraminifera Earlandia. The distribution of the faunal components within the microbial fabrics suggests that, except for the keratose sponges and some microconchids, most of the metazoans were transported into the microbial framework via wave currents. The presence of both microbialites and metazoan associations were limited to oxygenated settings, suggesting that a factor other than anoxia resulted in a relaxation of ecological constraints following the mass extinction event. It is inferred that the end-Permian mass extinction event decreased the diversity and abundance of metazoans to the point of significantly reducing competition, allowing photosynthesis-based microbial mats to flourish in shallow water settings and resulting in the formation of widespread microbialites.

Spatial distribution of oncocerid cephalopods on a Middle Devonian bedding plane suggests semelparous life cycle.

Reproductive strategies of extinct organisms can only be recognised indirectly and hence, they are exceedingly rarely reported and tend to be speculative. Here, we present a mass-occurrence with common preservation of pairs of late Givetian (Middle Devonian) oncocerid cephalopods from Hamar Laghdad in the Tafilalt (eastern Anti-Atlas, Morocco). We analysed their spatial occurrences with spatial point pattern analysis techniques and Monte Carlo simulations; our results shows that the pairwise clustering is significant, while ammonoids on the same bedding plane reveal a more random distribution. It is possible that processes such as catastrophic mass mortality or post-mortem transport could have produced the pattern. However, we suggest that it is more likely that the oncocerids were semelparous and died shortly after mating. These findings shed new light on the variation and evolution of reproductive strategies in fossil cephalopods and emphasise that they cannot be based on comparisons with extant taxa without question.

Eutrophication, microbial-sulfate reduction and mass extinctions.

In post-Cambrian time, life on Earth experienced 5 major extinction events, likely instigated by adverse environmental conditions. Biodiversity loss among marine taxa, for at least 3 of these mass extinction events (Late Devonian, end-Permian and end-Triassic), has been connected with widespread oxygen-depleted and sulfide-bearing marine water. Furthermore, geochemical and sedimentary evidence suggest that these events correlate with rather abrupt climate warming and possibly increased terrestrial weathering. This suggests that biodiversity loss may be triggered by mechanisms intrinsic to the Earth system, notably, the biogeochemical sulfur and carbon cycle. This climate warming feedback produces large-scale eutrophication on the continental shelf, which, in turn, expands oxygen minimum zones by increased respiration, which can turn to a sulfidic state by increased microbial-sulfate reduction due to increased availability of organic matter. A plankton community turnover from a high-diversity eukaryote to high-biomass bacterial dominated food web is the catalyst proposed in this anoxia-extinction scenario and stands in stark contrast to the postulated productivity collapse suggested for the end-Cretaceous mass extinction. This cascade of events is relevant for the future ocean under predicted greenhouse driven climate change. The exacerbation of anoxic "dead" zones is already progressing in modern oceanic environments, and this is likely to increase due to climate induced continental weathering and resulting eutrophication of the oceans.

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.

Flourishing ocean drives the end-Permian marine mass extinction.

The end-Permian mass extinction, the most severe biotic crisis in the Phanerozoic, was accompanied by climate change and expansion of oceanic anoxic zones. The partitioning of sulfur among different exogenic reservoirs by biological and physical processes was of importance for this biodiversity crisis, but the exact role of bioessential sulfur in the mass extinction is still unclear. Here we show that globally increased production of organic matter affected the seawater sulfate sulfur and oxygen isotope signature that has been recorded in carbonate rock spanning the Permian-Triassic boundary. A bifurcating temporal trend is observed for the strata spanning the marine mass extinction with carbonate-associated sulfate sulfur and oxygen isotope excursions toward decreased and increased values, respectively. By coupling these results to a box model, we show that increased marine productivity and successive enhanced microbial sulfate reduction is the most likely scenario to explain these temporal trends. The new data demonstrate that worldwide expansion of euxinic and anoxic zones are symptoms of increased biological carbon recycling in the marine realm initiated by global warming. The spatial distribution of sulfidic water column conditions in shallow seafloor environments is dictated by the severity and geographic patterns of nutrient fluxes and serves as an adequate model to explain the scale of the marine biodiversity crisis. Our results provide evidence that the major biodiversity crises in Earth's history do not necessarily implicate an ocean stripped of (most) life but rather the demise of certain eukaryotic organisms, leading to a decline in species richness.

Extinction space--a method for the quantification and classification of changes in morphospace across extinction boundaries.

Three main modes of extinction are responsible for reductions in morphological disparity: (1) random (caused by a nonselective extinction event); (2) marginal (a symmetric, selective extinction event trimming the margin of morphospace); and (3) lateral (an asymmetric, selective extinction event eliminating one side of the morphospace). These three types of extinction event can be distinguished from one another by comparing changes in three measures of morphospace occupation: (1) the sum of range along the main axes; (2) the sum of variance; and (3) the position of the centroid. Computer simulations of various extinction events demonstrate that the pre-extinction distribution of taxa (random or normal) in the morphospace has little influence on the quantification of disparity changes, whereas the modes of the extinction events play the major role. Together, the three disparity metrics define an "extinction-space" in which different extinction events can be directly compared with one another. Application of this method to selected extinction events (Frasnian-Famennian, Devonian-Carboniferous, and Permian-Triassic) of the Ammonoidea demonstrate the similarity of the Devonian events (selective extinctions) but the striking difference from the end-Permian event (nonselective extinction). These events differ in their mode of extinction despite decreases in taxonomic diversity of similar magnitude.

Quantification of ontogenetic allometry in ammonoids.

Ammonoids are well-known objects used for studies on ontogeny and phylogeny, but a quantification of ontogenetic change has not yet been carried out. Their planispirally coiled conchs allow for a study of "longitudinal" ontogenetic data, that is data of ontogenetic trajectories that can be obtained from a single specimen. Therefore, they provide a good model for ontogenetic studies of geometry in other shelled organisms. Using modifications of three cardinal conch dimensions, computer simulations can model artificial conchs. The trajectories of ontogenetic allometry of these simulations can be analyzed in great detail in a theoretical morphospace. A method for the classification of conch ontogeny and quantification of the degree of allometry is proposed. Using high-precision cross-sections, the allometric conch growth of real ammonoids can be documented and compared. The members of the Ammonoidea show a wide variety of allometric growth, ranging from near isometry to monophasic, biphasic, or polyphasic allometry. Selected examples of Palaeozoic and Mesozoic ammonoids are shown with respect to their degree of change during ontogeny of the conch.

Early evolutionary trends in ammonoid embryonic development.

During the Devonian Nekton Revolution, ammonoids show a progressive coiling of their shell just like many other pelagic mollusk groups. These now extinct, externally shelled cephalopods derived from bactritoid cephalopods with a straight shell in the Early Devonian. During the Devonian, evolutionary trends toward tighter coiling and a size reduction occurred in ammonoid embryonic shells. In at least three lineages, descendants with a closed umbilicus evolved convergently from forms with an opening in the first whorl (umbilical window). Other lineages having representatives with open umbilici became extinct around important Devonian events whereas only those with more tightly coiled embryonic shells survived. This change was accompanied by an evolutionary trend in shape of the initial chamber, but no clear trend in its size. The fact that several ammonoid lineages independently reduced and closed the umbilical window more or less synchronously indicates that common driving factors were involved. A trend in size decrease of the embryos as well as the concurrent increase in adult size in some lineages likely reflects a fundamental change in reproductive strategies toward a higher fecundity early in the evolutionary history of ammonoids. This might have played an important role in their subsequent success as well as in their demise.

Morphological disparity of ammonoids and the mark of Permian mass extinctions.

The taxonomic diversity of ammonoids, in terms of the number of taxa preserved, provides an incomplete picture of the extinction pattern during the Permian because of a strongly biased fossil record. The analysis of morphological disparity (the variety of shell shapes) is a powerful complementary tool for testing hypotheses about the selectivity of extinction and permits the recognition of three distinct patterns. First, a trend of decreasing disparity, ranging for about 30 million years, led to a minimum disparity immediately before the Permian-Triassic boundary. Second, the strongly selective Capitanian crisis fits a model of background extinction driven by standard environmental changes. Third, the end-Permian mass extinction operated as a random, nonselective sorting of morphologies, which is consistent with a catastrophic cause.