A. M. Penny

Ediacaran metazoan reefs from the Nama Group, Namibia

Building coral reefs in ancient times 540 million years ago, in the dawn before the Cambrian explosion, evolution was setting the stage for the global rise of animals. Before they took over the seas, the earliest animals developed strategies to defend themselves against predators. These strategies, which remain common today, include forming skeletons and building reefs. Penny et al. discovered a massive fossil reef deposit in Namibia made up of tiny coneshaped early animals known as Cloudina. The reef, which is 20 million years older than other ancient reefs, was probably formed as the Cloudina adapted to benefit from reefs, which protect the animals and allow them to feed more efficiently. Science, this issue p. 1504 Animal reefs from 550 million years ago suggest a complex ecosystem before the Cambrian explosion. Reef-building in metazoans represents an important ecological innovation whereby individuals collectively enhance feeding efficiency and gain protection from competitors and predation. The appearance of metazoan reefs in the fossil record therefore indicates an adaptive response to complex ecological pressures. In the Nama Group, Namibia, we found evidence of reef-building by the earliest known skeletal metazoan, the globally distributed Cloudina, ~548 million years ago. These Cloudina reefs formed open frameworks without a microbial component but with mutual attachment and cementation between individuals. Orientated growth implies a passive suspension-feeding habit into nutrient-rich currents. The characteristics of Cloudina support the view that metazoan reef-building was promoted by the rise of substrate competitors and predators.

Low-oxygen waters limited habitable space for early animals.

The oceans at the start of the Neoproterozoic Era (1,000–541 million years ago, Ma) were dominantly anoxic, but may have become progressively oxygenated, coincident with the rise of animal life. However, the control that oxygen exerted on the development of early animal ecosystems remains unclear, as previous research has focussed on the identification of fully anoxic or oxic conditions, rather than intermediate redox levels. Here we report anomalous cerium enrichments preserved in carbonate rocks across bathymetric basin transects from nine localities of the Nama Group, Namibia (∼550–541 Ma). In combination with Fe-based redox proxies, these data suggest that low-oxygen conditions occurred in a narrow zone between well-oxygenated surface waters and fully anoxic deep waters. Although abundant in well-oxygenated environments, early skeletal animals did not occupy oxygen impoverished regions of the shelf, demonstrating that oxygen availability (probably >10 μM) was a key requirement for the development of early animal-based ecosystems.

Ediacaran skeletal metazoan interpreted as a lophophorate

While many skeletal biomineralized genera are described from Ediacaran (635–541 million years ago, Ma) strata, none have been suggested to have an affinity above the Porifera–Cnidaria metazoan grade. Here, we reinterpret the widespread terminal Ediacaran (approx. 550–541 Ma) sessile goblet-shaped Namacalathus as a triploblastic eumetazoan. Namacalathus has a stalked cup with radially symmetrical cross section, multiple lateral lumens and a central opening. We show that the skeleton of Namacalathus is composed of a calcareous foliated ultrastructure displaying regular concordant columnar inflections, with a possible inner organic-rich layer. These features point to an accretionary growth style of the skeleton and an affinity with the Lophotrochozoa, more specifically within the Lophophorata (Brachiopoda and Bryozoa). Additionally, we present evidence for asexual reproduction as expressed by regular budding in a bilateral pattern. The interpretation of Namacalathus as an Ediacaran total group lophophorate is consistent with an early radiation of the Lophophorata, as known early Cambrian representatives were sessile, mostly stalked forms, and in addition, the oldest known calcareous Brachiopoda (early Cambrian Obolellida) and Bryozoa (Ordovician Stenolaemata) possessed foliated ultrastructures.

Flexible and responsive growth strategy of the Ediacaran skeletal Cloudina from the Nama Group, Namibia

The Ediacaran skeletal tubular putative metazoan Cloudina occurs globally in carbonate settings, which both provided lithified substrates and minimized the cost of skeletonization. Habitat and substrate preferences and the relationship of Cloudina to other metazoans have not been fully documented, so we know little as to its ecological demands or community dynamics. In situ Cloudina from the Nama Group, Namibia (ca. 550–541 Ma), formed mutually attached reefs composed of successive assemblages in shallow, high-energy environments, and also communities attached to either stromatolites in storm-influenced deep inner-ramp settings or thin microbial mats in lower-energy habitats. Each assemblage shows statistically distinct tube diameter cohorts, but in sum, Cloudina shows an exponential frequency distribution of diameter size. In reefs, we document a periodicity of size variation, where mean, minimum, and maximum tube diameters vary together and show a systematic increase toward the top of each assemblage. We conclude that most Nama Group Cloudina represent one ecologically generalist taxon with highly variable size, that size was environmentally mediated, and that Cloudina could respond rapidly to periodic environmental changes. While Nama Group skeletal metazoans coexisted with soft-bodied biota, there was no apparent ecological interaction, as they were segregated into lithified carbonate and non-lithified clastic microbial mat communities, respectively. We infer that ecological flexibility allowed Cloudina to form varied communities that colonized diverse carbonate substrates under low levels of interspecific substrate competition. This is in notable contrast to the earliest Cambrian skeletal epibenthos that formed biodiverse reef communities with specialist niche occupancy.

Substrate growth dynamics and biomineralization of an Ediacaran encrusting poriferan

The ability to encrust in order to secure and maintain growth on a substrate is a key competitive innovation in benthic metazoans. Here we describe the substrate growth dynamics, mode of biomineralization and possible affinity of Namapoikia rietoogensis, a large (up to 1 m), robustly skeletal, and modular Ediacaran metazoan which encrusted the walls of synsedimentary fissures within microbial–metazoan reefs. Namapoikia formed laminar or domal morphologies with an internal structure of open tubules and transverse elements, and had a very plastic, non-deterministic growth form which could encrust both fully lithified surfaces as well as living microbial substrates, the latter via modified skeletal holdfasts. Namapoikia shows complex growth interactions and substrate competition with contemporary living microbialites and thrombolites, including the production of plate-like dissepiments in response to microbial overgrowth which served to elevate soft tissue above the microbial surface. Namapoikia could also recover from partial mortality due to microbial fouling. We infer initial skeletal growth to have propagated via the rapid formation of an organic scaffold via a basal pinacoderm prior to calcification. This is likely an ancient mode of biomineralization with similarities to the living calcified demosponge Vaceletia. Namapoikia also shows inferred skeletal growth banding which, combined with its large size, implies notable individual longevity. In sum, Namapoikia was a large, relatively long-lived Ediacaran clonal skeletal metazoan that propagated via an organic scaffold prior to calcification, enabling rapid, effective and dynamic substrate occupation and competition in cryptic reef settings. The open tubular internal structure, highly flexible, non-deterministic skeletal organization, and inferred style of biomineralization of Namapoikia places probable affinity within total-group poriferans.