Ediacaran marine animal forests and the ventilation of the oceans.

The rise of animals across the Ediacaran-Cambrian transition marked a step-change in the history of life, from a microbially dominated world to the complex macroscopic biosphere we see today.1,2,3 While the importance of bioturbation and swimming in altering the structure and function of Earth systems is well established,4,5,6 the influence of epifaunal animals on the hydrodynamics of marine environments is not well understood. Of particular interest are the oldest "marine animal forests,"7 which comprise a diversity of sessile soft-bodied organisms dominated by the fractally branching rangeomorphs.8,9 Typified by fossil assemblages from the Ediacaran of Mistaken Point, Newfoundland,8,10,11 these ancient communities might have played a pivotal role in structuring marine environments, similar to modern ecosystems,7,12,13 but our understanding of how they impacted fluid flow in the water column is limited. Here, we use ecological modeling and computational flow simulations to explore how Ediacaran marine animal forests influenced their surrounding environment. Our results reveal how organism morphology and community structure and composition combined to impact vertical mixing of the surrounding water. We find that Mistaken Point communities were capable of generating high-mixing conditions, thereby likely promoting gas and nutrient transport within the "canopy." This mixing could have served to enhance local-scale oxygen concentrations and redistribute resources like dissolved organic carbon. Our work suggests that Ediacaran marine animal forests may have contributed to the ventilation of the oceans over 560 million years ago, well before the Cambrian explosion of animals.

Reconstructing the feeding ecology of Cambrian sponge reefs: the case for active suspension feeding in Archaeocyatha.

Sponge-grade Archaeocyatha were early Cambrian biomineralizing metazoans that constructed reefs globally. Despite decades of research, many facets of archaeocyath palaeobiology remain unclear, making it difficult to reconstruct the palaeoecology of Cambrian reef ecosystems. Of specific interest is how these organisms fed; previous experimental studies have suggested that archaeocyaths functioned as passive suspension feeders relying on ambient currents to transport nutrient-rich water into their central cavities. Here, we test this hypothesis using computational fluid dynamics (CFD) simulations of digital models of select archaeocyath species. Our results demonstrate that, given a range of plausible current velocities, there was very little fluid circulation through the skeleton, suggesting obligate passive suspension feeding was unlikely. Comparing our simulation data with exhalent velocities collected from extant sponges, we infer an active suspension feeding lifestyle for archaeocyaths. The combination of active suspension feeding and biomineralization in Archaeocyatha may have facilitated the creation of modern metazoan reef ecosystems.

The role of iron in the formation of Ediacaran 'death masks'.

The Ediacara biota are an enigmatic group of Neoproterozoic soft-bodied fossils that mark the first major radiation of complex eukaryotic and macroscopic life. These fossils are thought to have been preserved via pyritic "death masks" mediated by seafloor microbial mats, though little about the chemical constraints of this preservational pathway is known, in particular surrounding the role of bioavailable iron in death mask formation and preservational fidelity. In this study, we perform decay experiments on both diploblastic and triploblastic animals under a range of simulated sedimentary iron concentrations, in order to characterize the role of iron in the preservation of Ediacaran organisms. After 28 days of decay, we demonstrate the first convincing "death masks" produced under experimental laboratory conditions composed of iron sulfide and probable oxide veneers. Moreover, our results demonstrate that the abundance of iron in experiments is not the sole control on death mask formation, but also tissue histology and the availability of nucleation sites. This illustrates that Ediacaran preservation via microbial death masks need not be a "perfect storm" of paleoenvironmental porewater and sediment chemistry, but instead can occur under a range of conditions.

The rangeomorph Pectinifrons abyssalis: Hydrodynamic function at the dawn of animal life.

Rangeomorphs are among the oldest putative eumetazoans known from the fossil record. Establishing how they fed is thus key to understanding the structure and function of the earliest animal ecosystems. Here, we use computational fluid dynamics to test hypothesized feeding modes for the fence-like rangeomorph Pectinifrons abyssalis, comparing this to the morphologically similar extant carnivorous sponge Chondrocladia lyra. Our results reveal complex patterns of flow around P. abyssalis unlike those previously reconstructed for any other Ediacaran taxon. Comparisons with C. lyra reveal substantial differences between the two organisms, suggesting they converged on a similar fence-like morphology for different functions. We argue that the flow patterns recovered for P. abyssalis do not support either a suspension feeding or osmotrophic feeding habit. Instead, our results indicate that rangeomorph fronds may represent organs adapted for gas exchange. If correct, this interpretation could require a dramatic reinterpretation of the oldest macroscopic animals.

Ancient life and moving fluids.

Over 3.7 billion years of Earth history, life has evolved complex adaptations to help navigate and interact with the fluid environment. Consequently, fluid dynamics has become a powerful tool for studying ancient fossils, providing insights into the palaeobiology and palaeoecology of extinct organisms from across the tree of life. In recent years, this approach has been extended to the Ediacara biota, an enigmatic assemblage of Neoproterozoic soft-bodied organisms that represent the first major radiation of macroscopic eukaryotes. Reconstructing the ways in which Ediacaran organisms interacted with the fluids provides new insights into how these organisms fed, moved, and interacted within communities. Here, we provide an in-depth review of fluid physics aimed at palaeobiologists, in which we dispel misconceptions related to the Reynolds number and associated flow conditions, and specify the governing equations of fluid dynamics. We then review recent advances in Ediacaran palaeobiology resulting from the application of computational fluid dynamics (CFD). We provide a worked example and account of best practice in CFD analyses of fossils, including the first large eddy simulation (LES) experiment performed on extinct organisms. Lastly, we identify key questions, barriers, and emerging techniques in fluid dynamics, which will not only allow us to understand the earliest animal ecosystems better, but will also help to develop new palaeobiological tools for studying ancient life.

Increase in metazoan ecosystem engineering prior to the Ediacaran-Cambrian boundary in the Nama Group, Namibia.

The disappearance of the soft-bodied Ediacara biota at the Ediacaran-Cambrian boundary potentially represents the earliest mass extinction of complex life, although the precise driver(s) of this extinction remain unresolved. The 'biotic replacement' model proposes that an evolutionary radiation of metazoan ecosystem engineers in the latest Ediacaran profoundly altered marine palaeoenvironments, resulting in the extinction of Ediacara biota and setting the stage for the subsequent Cambrian Explosion. However, metazoan ecosystem engineering across the Ediacaran-Cambrian transition has yet to be quantified. Here, we test this key tenet of the biotic replacement model by characterizing the intensity of metazoan bioturbation and ecosystem engineering in trace fossil assemblages throughout the latest Ediacaran Nama Group in southern Namibia. The results illustrate a dramatic increase in both bioturbation and ecosystem engineering intensity in the latest Ediacaran, prior to the Cambrian boundary. Moreover, our analyses demonstrate that the highest-impact ecosystem engineering behaviours were present well before the onset of the Cambrian. These data provide the first support for a fundamental prediction of the biotic replacement model, and evidence for a direct link between the early evolution of ecosystem engineering and the extinction of the Ediacara biota.

Biomineralization by particle attachment in early animals.

Crystallization by particle attachment (CPA) of amorphous precursors has been demonstrated in modern biomineralized skeletons across a broad phylogenetic range of animals. Precisely the same precursors, hydrated (ACC-H2O) and anhydrous calcium carbonate (ACC), have been observed spectromicroscopically in echinoderms, mollusks, and cnidarians, phyla drawn from the 3 major clades of eumetazoans. Scanning electron microscopy (SEM) here also shows evidence of CPA in tunicate chordates. This is surprising, as species in these clades have no common ancestor that formed a mineralized skeleton and appear to have evolved carbonate biomineralization independently millions of years after their late Neoproterozoic divergence. Here we correlate the occurrence of CPA from ACC precursor particles with nanoparticulate fabric and then use the latter to investigate the antiquity of the former. SEM images of early biominerals from Ediacaran and Cambrian shelly fossils show that these early calcifiers used attachment of ACC particles to form their biominerals. The convergent evolution of biomineral CPA may have been dictated by the same thermodynamics and kinetics as we observe today.

Gregarious suspension feeding in a modular Ediacaran organism.

Reconstructing Precambrian eukaryotic paleoecology is pivotal to understanding the origins of the modern, animal-dominated biosphere. Here, we combine new fossil data from southern Namibia with computational fluid dynamics (CFD) to test between competing feeding models for the Ediacaran taxon Ernietta. In addition, we perform simulations for multiple individuals, allowing us to analyze hydrodynamics of living communities. We show that Ernietta lived gregariously, forming shallow marine aggregations in the latest Ediacaran, 548 to 541 million years (Ma) ago. We demonstrate enhanced vertical mixing of the water column above aggregations and preferential redirection of current into body cavities of downstream individuals. These results support the reconstruction of Ernietta as a macroscopic suspension feeder and also provide a convincing paleoecological advantage to feeding in aggregations analogous to those recognized in many extant marine metazoans. These results provide some of the oldest evidence of commensal facilitation by macroscopic eukaryotes yet recognized in the fossil record.