A late-Ediacaran crown-group sponge animal.

Sponges are the most basal metazoan phylum1 and may have played important roles in modulating the redox architecture of Neoproterozoic oceans2. Although molecular clocks predict that sponges diverged in the Neoproterozoic era3,4, their fossils have not been unequivocally demonstrated before the Cambrian period5-8, possibly because Precambrian sponges were aspiculate and non-biomineralized9. Here we describe a late-Ediacaran fossil, Helicolocellus cantori gen. et sp. nov., from the Dengying Formation (around 551-539 million years ago) of South China. This fossil is reconstructed as a large, stemmed benthic organism with a goblet-shaped body more than 0.4 m in height, with a body wall consisting of at least three orders of nested grids defined by quadrate fields, resembling a Cantor dust fractal pattern. The resulting lattice is interpreted as an organic skeleton comprising orthogonally arranged cruciform elements, architecturally similar to some hexactinellid sponges, although the latter are built with biomineralized spicules. A Bayesian phylogenetic analysis resolves H. cantori as a crown-group sponge related to the Hexactinellida. H. cantori confirms that sponges diverged and existed in the Precambrian as non-biomineralizing animals with an organic skeleton. Considering that siliceous biomineralization may have evolved independently among sponge classes10-13, we question the validity of biomineralized spicules as a necessary criterion for the identification of Precambrian sponge fossils.

Lithium isotopic constraints on the evolution of continental clay mineral factory and marine oxygenation in the earliest Paleozoic Era.

The evolution of oxygen cycles on Earth's surface has been regulated by the balance between molecular oxygen production and consumption. The Neoproterozoic-Paleozoic transition likely marks the second rise in atmospheric and oceanic oxygen levels, widely attributed to enhanced burial of organic carbon. However, it remains disputed how marine organic carbon production and burial respond to global environmental changes and whether these feedbacks trigger global oxygenation during this interval. Here, we report a large lithium isotopic and elemental dataset from marine mudstones spanning the upper Neoproterozoic to middle Cambrian [~660 million years ago (Ma) to 500 Ma]. These data indicate a dramatic increase in continental clay formation after ~525 Ma, likely linked to secular changes in global climate and compositions of the continental crust. Using a global biogeochemical model, we suggest that intensified continental weathering and clay delivery to the oceans could have notably increased the burial efficiency of organic carbon and facilitated greater oxygen accumulation in the earliest Paleozoic oceans.

The cluster digging behavior of larvae confers trophic benefits to fitness in insects.

Collective behaviors efficiently impart benefits to a diversity of species ranging from bacteria to humans. Fly larvae tend to cluster and form coordinated digging groups under crowded conditions, yet understanding the rules governing this behavior is in its infancy. We primarily took advantage of the Drosophila model to investigate cooperative foraging behavior. Here, we report that Drosophila-related species and the black soldier fly have evolved a conserved strategy of cluster digging in food foraging. Subsequently, we investigated relative factors, including larval stage, population density, and food stiffness and quality, that affect the cluster digging behavior. Remarkably, oxygen supply through the posterior breathing spiracles is necessary for the organization of digging clusters. More importantly, we theoretically devise a mathematical model to accurately calculate how the cluster digging behavior expands food resources by diving depth, cross-section area, and food volume. We found that cluster digging behavior approximately increases 2.2 fold depth, 1.7-fold cross-section area, and 1.9 fold volume than control groups, respectively. Amplification of food sources significantly facilitates survival, larval development, and reproductive success of Drosophila challenged with competition for limited food resources, thereby conferring trophic benefits to fitness in insects. Overall, our findings highlight that the cluster digging behavior is a pivotal behavior for their adaptation to food scarcity, advancing a better understanding of how this cooperative behavior confers fitness benefits in the animal kingdom.

A Great late Ediacaran ice age.

The emergence of the Ediacara biota soon after the Gaskiers glaciation ca. 580 million years ago (Ma) implies a possible glacial fuse for the evolution of animals. However, the timing of Ediacaran glaciation remains controversial because of poor age constraints on the ∼30 Ediacaran glacial deposits known worldwide. In addition, paleomagnetic constraints and a lack of convincing Snowball-like cap carbonates indicate that Ediacaran glaciations likely did not occur at low latitudes. Thus, reconciling the global occurrences without global glaciation remains a paradox. Here, we report that the large amplitude, globally synchronous ca. 571-562 Ma Shuram carbon isotope excursion occurs below the Ediacaran Hankalchough glacial deposit in Tarim, confirming a post-Shuram glaciation. Leveraging paleomagnetic evidence for a ∼90° reorientation of all continents due to true polar wander, and a non-Snowball condition that rules out low-latitude glaciations, we use paleogeographic reconstructions to further constrain glacial ages. Our results depict a 'Great Ediacaran Glaciation' occurring diachronously but continuously from ca. 580-560 Ma as different continents migrated through polar-temperate latitudes. The succession of radiation, turnover and extinction of the Ediacara biota strongly reflects glacial-deglacial dynamics.

Tonian carbonaceous compressions indicate that Horodyskia is one of the oldest multicellular and coenocytic macro-organisms.

Macrofossils with unambiguous biogenic origin and predating the one-billion-year-old multicellular fossils Bangiomorpha and Proterocladus interpreted as crown-group eukaryotes are quite rare. Horodyskia is one of these few macrofossils, and it extends from the early Mesoproterozoic Era to the terminal Ediacaran Period. The biological interpretation of this enigmatic fossil, however, has been a matter of controversy since its discovery in 1982, largely because there was no evidence for the preservation of organic walls. Here we report new carbonaceous compressions of Horodyskia from the Tonian successions (~950-720 Ma) in North China. The macrofossils herein with bona fide organic walls reinforce the biogenicity of Horodyskia. Aided by the new material, we reconstruct Horodyskia as a colonial organism composed of a chain of organic-walled vesicles that likely represent multinucleated (coenocytic) cells of early eukaryotes. Two species of Horodyskia are differentiated on the basis of vesicle sizes, and their co-existence in the Tonian assemblage provides a link between the Mesoproterozoic (H. moniliformis) and the Ediacaran (H. minor) species. Our study thus provides evidence that eukaryotes have acquired macroscopic size through the combination of coenocytism and colonial multicellularity at least ~1.48 Ga, and highlights an exceptionally long range and morphological stasis of this Proterozoic macrofossils.

Cracking the superheavy pyrite enigma: possible roles of volatile organosulfur compound emission.

The global deposition of superheavy pyrite (pyrite isotopically heavier than coeval seawater sulfate in the Neoproterozoic Era and particularly in the Cryogenian Period) defies explanation using the canonical marine sulfur cycle system. Here we report petrographic and sulfur isotopic data (δ34Spy) of superheavy pyrite from the Cryogenian Datangpo Formation (660-650 Ma) in South China. Our data indicate a syndepositional/early diagenetic origin of the Datangpo superheavy pyrite, with 34S-enriched H2S supplied from sulfidic (H2S rich) seawater. Instructed by a novel sulfur-cycling model, we propose that the emission of 34S-depleted volatile organosulfur compounds (VOSC) that were generated via sulfide methylation may have contributed to the formation of 34S-enriched sulfidic seawater and superheavy pyrite. The global emission of VOSC may be attributed to enhanced organic matter production after the Sturtian glaciation in the context of widespread sulfidic conditions. These findings demonstrate that VOSC cycling is an important component of the sulfur cycle in Proterozoic oceans.

Cryptic terrestrial fungus-like fossils of the early Ediacaran Period.

The colonization of land by fungi had a significant impact on the terrestrial ecosystem and biogeochemical cycles on Earth surface systems. Although fungi may have diverged ~1500-900 million years ago (Ma) or even as early as 2400 Ma, it is uncertain when fungi first colonized the land. Here we report pyritized fungus-like microfossils preserved in the basal Ediacaran Doushantuo Formation (~635 Ma) in South China. These micro-organisms colonized and were preserved in cryptic karstic cavities formed via meteoric water dissolution related to deglacial isostatic rebound after the terminal Cryogenian snowball Earth event. They are interpreted as eukaryotes and probable fungi, thus providing direct fossil evidence for the colonization of land by fungi and offering a key constraint on fungal terrestrialization.

Facile synthesis of zirconia-coated mesoporous silica particles by hydrothermal strategy under low potential of hydrogen conditions and functionalization with dodecylphosphonic acid for high-performance liquid chromatography.

In this work, multilayer zirconia-coated silica (ZrO2/SiO2-n) microspheres were successfully produced by a straightforward hydrothermal procedure with a low concentration of Zr4+ (5 mM) under low potential of hydrogen (pH) conditions (pH = =2). The obtained ZrO2/SiO2-n materials exhibited favorable characteristics for high-performance liquid chromatography (HPLC) separation, including high surface area and pore volume, good pore structure, narrow particle size, and pore size distribution. In addition, the zirconia coverage in the mesopores was confirmed by soaking the material in 1 M NaOH solution, with the particles showing strong resistance to the basic solution. The obtained ZrO2/SiO2-n stationary phases were packed into a fused-silica capillary tubing for the separation of alkaloids in hydrophilic interaction chromatography (HILIC) mode, and a column efficiency of 47,800 plates/m was obtained for berberine on a ZrO2/SiO2-6 micro column. The ZrO2/SiO2-6 microspheres were further modified by dodecylphosphonic acid (C12P-2-ZrO2/SiO2-6); the C12P-2-ZrO2/SiO2-6 material showed great potential for application in reversed-phase liquid chromatography (RPLC) mode. The C12P-2-ZrO2/SiO2-6 micro column showed a column efficiency of 55,000 plates/m for naphthalene and 51,300 plates/m for benzene.

A problematic animal fossil from the early Cambrian Hetang Formation, South China.

The lower-middle Hetang Formation (Cambrian Stage 2-3) deposited in slope-basinal facies in South China is well-known for its preservation of the earliest articulated sponge fossils, providing an important taphonomic window into the Cambrian explosion. However, the Hetang Formation also hosts a number of problematic animal fossils that have not been systematically described. This omission results in an incomplete picture of the Hetang biota and limits its contribution to the understanding of the early evolution of animals. Here we describe a new animal taxon, Cambrowania ovata Tang and Xiao, new genus new species, from the middle Hetang Formation in the Lantian area of southern Anhui Province, South China. Specimens are preserved as carbonaceous compressions, although some are secondarily mineralized. A comprehensive analysis using reflected light microscopy, scanning electron microscopy, energy dispersive X-ray spectroscopy, and micro-CT reveals that the new species is characterized by a spheroidal to fusoidal truss-like structure consisting of rafter-like crossbars, some of which are secondarily baritized and may have been internally hollow. Some specimens have aperture-like structures that are broadly similar to oscula of sponges, whereas others show evidence of a medial split reminiscent of gaping carapaces. While the phylogenetic affinity of Cambrowania ovata Tang and Xiao, new genus new species remains problematic, we propose that it may represent carapaces of bivalved arthropods or more likely sponges in early life stages. Along with other problematic metazoan fossils such as hyolithids and sphenothallids, Cambrowania ovata Tang and Xiao, new genus new species adds to the diversity of the sponge-dominated Hetang biota in an early Cambrian deep-water slope-basinal environment.

Early animal evolution and highly oxygenated seafloor niches hosted by microbial mats.

The earliest unambiguous evidence for animals is represented by various trace fossils in the latest Ediacaran Period (550-541 Ma), suggesting that the earliest animals lived on or even penetrated into the seafloor. Yet, the O2 fugacity at the sediment-water interface (SWI) for the earliest animal proliferation is poorly defined. The preferential colonization of seafloor as a first step in animal evolution is also unusual. In order to understand the environmental background, we employed a new proxy, carbonate associated ferrous iron (Fecarb), to quantify the seafloor oxygenation. Fecarb of the latest Ediacaran Shibantan limestone in South China, which yields abundant animal traces, ranges from 2.27 to 85.43 ppm, corresponding to the seafloor O2 fugacity of 162 µmol/L to 297 µmol/L. These values are significantly higher than the oxygen saturation in seawater at the contemporary atmospheric pO2 levels. The highly oxygenated seafloor might be attributed to O2 production of the microbial mats. Despite the moderate atmospheric pO2 level, microbial mats possibly provided highly oxygenated niches for the evolution of benthic metazoans. Our model suggests that the O2 barrier could be locally overcome in the mat ground, questioning the long-held belief that atmospheric oxygenation was the key control of animal evolution.

Death march of a segmented and trilobate bilaterian elucidates early animal evolution.

The origin of motility in bilaterian animals represents an evolutionary innovation that transformed the Earth system. This innovation probably occurred in the late Ediacaran period-as evidenced by an abundance of trace fossils (ichnofossils) dating to this time, which include trails, trackways and burrows1-3. However, with few exceptions4-8, the producers of most of the late Ediacaran ichnofossils are unknown, which has resulted in a disconnection between the body- and trace-fossil records. Here we describe the fossil of a bilaterian of the terminal Ediacaran period (dating to 551-539 million years ago), which we name Yilingia spiciformis (gen. et sp. nov). This body fossil is preserved along with the trail that the animal produced during a death march. Yilingia is an elongate and segmented bilaterian with repetitive and trilobate body units, each of which consists of a central lobe and two posteriorly pointing lateral lobes, indicating body and segment polarity. Yilingia is possibly related to panarthropods or annelids, and sheds light on the origin of segmentation in bilaterians. As one of the few Ediacaran animals demonstrated to have produced long and continuous trails, Yilingia provides insights into the identity of the animals that were responsible for Ediacaran trace fossils.

Transient marine euxinia at the end of the terminal Cryogenian glaciation.

Termination of the terminal Cryogenian Marinoan snowball Earth glaciation (~650-635 Ma) is associated with the worldwide deposition of a cap carbonate. Modeling studies suggest that, during and immediately following deglaciation, the ocean may have experienced a rapid rise in pH and physical stratification followed by oceanic overturn. Testing these predictions requires the establishment of a high-resolution sequence of events within sedimentary records. Here we report the conspicuous occurrence of pyrite concretions in the topmost Nantuo Formation (South China) that was deposited in the Marinoan glacial deposits. Sedimentary facies and sulfur isotope data indicate pyrite precipitation in the sediments with H2S diffusing from the overlying sulfidic/euxinic seawater and Fe (II) from diamictite sediments. These observations suggest a transient but widespread presence of marine euxinia in an ocean characterized by redox stratification, high bioproductivity, and high-fluxes of sulfate from chemical weathering before the deposition of the cap carbonate.

Late Ediacaran trackways produced by bilaterian animals with paired appendages.

Ediacaran trace fossils provide key paleontological evidence for the evolution of early animals and their behaviors. Thus far, however, this fossil record has been limited to simple surface trails and relatively shallow burrows. We report possible trackways, preserved in association with burrows, from the terminal Ediacaran Shibantan Member (ca. 551 to ca. 541 million years ago) in the Yangtze Gorges area of South China. These trace fossils represent the earliest known trackways. They consist of two rows of imprints arranged in poorly organized series or repeated groups. These trackways may have been produced by bilaterian animals with paired appendages, although the phylum-level phylogenetic affinity of the trace makers remains unknown. It is possible that the trackways and associated burrows were produced by the same trace maker, indicating a complex behavior involving both walking and burrowing. Together, these trackways and burrows mark the arrival of a new era characterized by an increasing geobiological footprint of bilaterian animals.

Molar tooth carbonates and benthic methane fluxes in Proterozoic oceans.

Molar tooth structures are ptygmatically folded and microspar-filled structures common in early- and mid-Proterozoic (∼2,500-750 million years ago, Ma) subtidal successions, but extremely rare in rocks <750 Ma. Here, on the basis of Mg and S isotopes, we show that molar tooth structures may have formed within sediments where microbial sulphate reduction and methanogenesis converged. The convergence was driven by the abundant production of methyl sulphides (dimethyl sulphide and methanethiol) in euxinic or H2S-rich seawaters that were widespread in Proterozoic continental margins. In this convergence zone, methyl sulphides served as a non-competitive substrate supporting methane generation and methanethiol inhibited anaerobic oxidation of methane, resulting in the buildup of CH4, formation of degassing cracks in sediments and an increase in the benthic methane flux from sediments. Precipitation of crack-filling microspar was driven by methanogenesis-related alkalinity accumulation. Deep ocean ventilation and oxygenation around 750 Ma brought molar tooth structures to an end.

Ediacaran Marine Redox Heterogeneity and Early Animal Ecosystems.

Oxygenation has widely been viewed as a major factor driving the emergence and diversification of animals. However, links between early animal evolution and shifts in surface oxygen levels have largely been limited to extrapolation of paleoredox conditions reconstructed from unfossiliferous strata to settings in which contemporaneous fossils were preserved. Herein, we present a multi-proxy paleoredox study of late Ediacaran (ca. 560-551 Ma) shales hosting the Miaohe Konservat-Lagerstätte of South China and, for comparison, equivalent non-fossil-bearing shales at adjacent sections. For the fossiliferous strata at Miaohe there is geochemical evidence for anoxic conditions, but paleontological evidence for at least episodically oxic conditions. An oxygen-stressed environment is consistent with the low diversity and simple morphology of Miaohe Biota macrofossils. However, there is no evidence for euxinic (anoxic and sulphidic) conditions for the fossiliferous strata at Miaohe, in contrast to adjacent unfossiliferous sections. Our results indicate that Ediacaran marine redox chemistry was highly heterogeneous, even at the kilometre-scale. Therefore, our study provides direct-rather than inferred-evidence that anoxia played a role in shaping a landmark Ediacaran ecosystem. If the anoxic conditions characteristic of the studied sections were widespread in the late Neoproterozoic, environmental stress would have hindered the development of complex ecosystems.

Cell differentiation and germ-soma separation in Ediacaran animal embryo-like fossils.

Phosphorites of the Ediacaran Doushantuo Formation (∼600 million years old) yield spheroidal microfossils with a palintomic cell cleavage pattern. These fossils have been variously interpreted as sulphur-oxidizing bacteria, unicellular protists, mesomycetozoean-like holozoans, green algae akin to Volvox, and blastula embryos of early metazoans or bilaterian animals. However, their complete life cycle is unknown and it is uncertain whether they had a cellularly differentiated ontogenetic stage, making it difficult to test their various phylogenetic interpretations. Here we describe new spheroidal fossils from black phosphorites of the Doushantuo Formation that have been overlooked in previous studies. These fossils represent later developmental stages of previously published blastula-like fossils, and they show evidence for cell differentiation, germ-soma separation, and programmed cell death. Their complex multicellularity is inconsistent with a phylogenetic affinity with bacteria, unicellular protists, or mesomycetozoean-like holozoans. Available evidence also indicates that the Doushantuo fossils are unlikely crown-group animals or volvocine green algae. We conclude that an affinity with cellularly differentiated multicellular eukaryotes, including stem-group animals or algae, is likely but more data are needed to constrain further the exact phylogenetic affinity of the Doushantuo fossils.

New Ediacara fossils preserved in marine limestone and their ecological implications.

Ediacara fossils are central to our understanding of animal evolution on the eve of the Cambrian explosion, because some of them likely represent stem-group marine animals. However, some of the iconic Ediacara fossils have also been interpreted as terrestrial lichens or microbial colonies. Our ability to test these hypotheses is limited by a taphonomic bias that most Ediacara fossils are preserved in sandstones and siltstones. Here we report several iconic Ediacara fossils and an annulated tubular fossil (reconstructed as an erect epibenthic organism with uniserial arranged modular units), from marine limestone of the 551-541 Ma Dengying Formation in South China. These fossils significantly expand the ecological ranges of several key Ediacara taxa and support that they are marine organisms rather than terrestrial lichens or microbial colonies. Their close association with abundant bilaterian burrows also indicates that they could tolerate and may have survived moderate levels of bioturbation.

Sedimentary constraints on the duration of the Marinoan Oxygen-17 Depletion (MOSD) event.

The ~635 Ma Marinoan glaciation is marked by dramatic Earth system perturbations. Deposition of nonmass-dependently (17)O-depleted sulfate (SO4(2-)) in worldwide postglacial sediments is, thus far, unique to this glaciation. It is proposed that an extremely high-pCO2 atmosphere can result in highly (17)O-depleted atmospheric O2, or the Marinoan Oxygen-17 Depletion (MOSD) event. This anomalous (17)O signal was imparted to sulfate of oxidative weathering origin. However, (17)O-depleted sulfate occurs in limited sedimentary intervals, suggesting that Earth surface conditions conducive to the MOSD had a finite duration. An MOSD duration can, therefore, provide much needed constraint on modeling Earth system responses at that time. Unfortunately, the sulfate (17)O record is often sparse or lacks radiometric dates. Here, we report 11 barite layers from a post-Marinoan dolostone sequence at Wushanhu in the South China Block. The (17)O depletion fluctuates in magnitude in lower layers but is persistently absent up section, providing the most confident first and last sedimentary appearance of the anomaly. δ(13)C chemostratigraphy is used to correlate the Wushanhu section to two proximal sections on the same shallow platform that lack barite layers but have published U-Pb dates that occur in dolostone and shale. Assuming a similar pattern and rate for carbonate and shale deposition among the different sections, we estimate the MOSD duration at 0-0.99 My. This number can be further constrained by new radiometric dates from equivalent sequences worldwide, thus underpinning models on the nonsteady-state Earth system response in the immediate aftermath of the Marinoan meltdown.

Comment on "Fossilized nuclei and germination structures identify Ediacaran 'animal embryos' as encysting protists".

On the basis of putative nuclei and endospores, Huldtgren et al. (Reports, 23 December 2011, p. 1696) propose that embryo-like Doushantuo microfossils are nonmetazoan holozoans akin to mesomycetozoeans. However, both size and preservation preclude interpretation of internal structures as nuclei. Moreover, the authors may have conflated two different populations; some specimens display a pseudoparenchymatous organization incompatible with a mesomycetozoean comparison.

An early Ediacaran assemblage of macroscopic and morphologically differentiated eukaryotes.

The deep-water Avalon biota (about 579 to 565 million years old) is often regarded as the earliest-known fossil assemblage with macroscopic and morphologically complex life forms. It has been proposed that the rise of the Avalon biota was triggered by the oxygenation of mid-Ediacaran deep oceans. Here we report a diverse assemblage of morphologically differentiated benthic macrofossils that were preserved largely in situ as carbonaceous compressions in black shales of the Ediacaran Lantian Formation (southern Anhui Province, South China). The Lantian biota, probably older than and taxonomically distinct from the Avalon biota, suggests that morphological diversification of macroscopic eukaryotes may have occurred in the early Ediacaran Period, perhaps shortly after the Marinoan glaciation, and that the redox history of Ediacaran oceans was more complex than previously thought.