Susannah M. Porter

Testate amoebae in the Neoproterozoic Era: evidence from vase-shaped microfossils in the Chuar Group, Grand Canyon

Abstract Vase-shaped microfossils (VSMs) occur globally in Neoproterozoic rocks, but until now their biological relationships have remained problematic. Exceptionally preserved new populations from the uppermost Chuar Group, Grand Canyon, Arizona, display details of morphology and taphonomy that collectively point to affinities with the testate amoebae. The fossils are tear-shaped tests, ∼20–300 μm long and ∼10–200 μm wide, that are circular in transverse section, expand aborally toward a rounded or slightly pointed pole, and taper orally toward a “neck” that ends in a single aperture. Apertures may be circular, hexagonal, triangular, or crenulate, and may be rimmed by a distinct collar. Approximately 25% of the Chuar VSMs are curved, such that the oral and aboral poles do not lie opposite each other. Tests are preserved as mineralized casts and molds, commonly coated with organic debris or iron minerals, but they were originally composed of nonresistant organic matter. Approximately 1% have a “honeycomb-patterned” wall attributable to the original presence of mineralized scales whose bases were arranged regularly in the test wall. Scale-bearing testate amoebae, such as members of the Euglyphidae, are essentially identical to the honeycomb VSMs, and a close relationship between other Grand Canyon VSMs and additional testate amoebae, both lobose and filose, is likely. The VSM population therefore most likely represents a multispecies assemblage whose spatial association reflects a common habitat and/or taphonomic circumstances that favor test preservation. The assignment of these fossils to the testate amoebae strengthens the case for a major diversification of eukaryotic organisms by mid-Neoproterozoic times and, more significantly, provides the earliest morphological evidence for heterotrophic eukaryotes in marine ecosystems.

VASE-SHAPED MICROFOSSILS FROM THE NEOPROTEROZOIC CHUAR GROUP, GRAND CANYON: A CLASSIFICATION GUIDED BY MODERN TESTATE AMOEBAE

Abstract Vase-shaped microfossil (VSM) assemblages from early diagenetic carbonate nodules in >742 ± 6 Ma black shales of the Chuar Group, Grand Canyon, provide evidence for affinities with testate amoebae. Not only are VSMs exceptionally preserved in Chuar rocks, they exhibit a much higher degree of morphological diversity than was previously known. Using the taxonomy of modern testate amoebae as a guide, nine new species and eight new genera of VSMs are described, augmenting the eight species and two genera already recognized. Taxa described here are Melanocyrillium hexodiadema Bloeser, 1985, Trigonocyrillium horodyskii (Bloeser, 1985) n. comb., T. fimbriatum (Bloeser, 1985) n. comb., Cycliocyrillium simplex n. sp., C. torquata n. sp., Bonniea dacruchares n. sp., B. pytinaia n. sp., Trachycyrillium pudens n. sp., Palaeoarcella athanata n. sp., Hemisphaeriella ornata n. sp., Bombycion micron n. sp., and Melicerion poikilon n. sp. All of the test characters observed in VSM taxa (e.g., collars; indentations; hexagonal symmetry; lobed, triangular or invaginated apertures; curved necks) occur in modern testate amoeban taxa, though not always in the same combinations. Some VSM species have characters found today in diverse extant taxa, making it difficult to assess their relationships. A few species, however, have character combinations that closely approximate those found in specific genera of both lobose and filose testate amoebae, suggesting that at least stem group, and possibly crown group, representatives of these taxa were present ∼742 Ma. These fossils indicate that ecosystems were diverse and complex, that eukaryotic biomineralization had already evolved, and that the last common ancestor of animals+fungi had already appeared by ∼750 Ma.

The earliest Cambrian record of animals and ocean geochemical change

The Cambrian diversification of animals was long thought to have begun with an explosive phase at the start of the Tommotian Age. Recent stratigraphic discoveries, however, suggest that many taxa appeared in the older Nemakit-Daldynian Age, and that the diversification was more gradual. We map lowest Cambrian (Nemakit-Daldynian through Tommotian) records of δ 13 C CaCO 3 variability from Siberia, Mongolia, and China onto a Moroccan U/Pb–δ 13 C CaCO 3 age model constrained by five U/Pb ages from interbedded volcanic ashes. The δ 13 C CaCO 3 correlations ignore fossil tie points, so we assume synchroneity in δ 13 C trends rather than synchroneity in first appearances of animal taxa. We present new δ 13 C org , 87 Sr/ 86 Sr, uranium, and vanadium data from the same carbonate samples that define the Moroccan δ 13 C CaCO 3 curve. The result is a new absolute time line for first appearances of skeletal animals and for changes in the carbon, strontium, and redox chemistry of the ocean during the Nemakit-Daldynian and Tommotian ages at the beginning of the Cambrian. The time line suggests that the diversification of skeletal animals began early in the Nemakit-Daldynian, with much of the diversity appearing by the middle of the age. Fossil first appearances occurred in three pulses, with a small pulse in the earliest Nemakit-Daldynian (ca. 540–538 Ma), a larger pulse in the mid- to late Nemakit-Daldynian (ca. 534–530 Ma), and a moderate pulse in the Tommotian (ca. 524–522 Ma). These pulses are associated with rapid reorganizations of the carbon cycle, and are superimposed on long-term increases in sea level and the hydrothermal flux of Sr.

Chuar Group of the Grand Canyon: record of breakup of Rodinia, associated change in the global carbon cycle, and ecosystem expansion by 740 Ma

The Chuar Group (approximately 1600 m thick) preserves a record of extensional tectonism, ocean-chemistry fluctuations, and biological diversification during the late Neoproterozoic Era. An ash layer from the top of the section has a U-Pb zircon age of 742 +/- 6 Ma. The Chuar Group was deposited at low latitudes during extension on the north-trending Butte fault system and is inferred to record rifting during the breakup of Rodinia. Shallow-marine deposition is documented by tide- and wave-generated sedimentary structures, facies associations, and fossils. C isotopes in organic carbon show large stratigraphic variations, apparently recording incipient stages of the marked C isotopic fluctuations that characterize later Neoproterozoic time. Upper Chuar rocks preserve a rich biota that includes not only cyanobacteria and algae, but also heterotrophic protists that document increased food web complexity in Neoproterozoic ecosystems. The Chuar Group thus provides a well-dated, high-resolution record of early events in the sequence of linked tectonic, biogeochemical, environmental, and biological changes that collectively ushered in the Phanerozoic Eon.

Calcite and aragonite seas and the de novo acquisition of carbonate skeletons

A longstanding question in paleontology has been the influence of calcite and aragonite seas on the evolution of carbonate skeletons. An earlier study based on 21 taxa that evolved skeletons during the Ediacaran through Ordovician suggested that carbonate skeletal mineralogy is determined by seawater chemistry at the time skeletons first evolve in a clade. Here I test this hypothesis using an expanded dataset comprising 40 well-defined animal taxa that evolved skeletons de novo in the last 600 Myr. Of the 37 taxa whose mineralogy is known with some confidence, 25 acquired mineralogies that matched seawater chemistry of the time, whereas only two taxa acquired non-matching mineralogies. (Ten appeared during times when seawater chemistry is not well constrained.) The results suggest that calcite and aragonite seas do have a strong influence on carbonate skeletal mineralogy, however, this appears to be true only at the time mineralized skeletons first evolve. Few taxa switch mineralogies (from calcite to aragonite or vice versa) despite subsequent changes in seawater chemistry, and those that do switch do not appear to do so in response to changing aragonite-calcite seas. This suggests that there may be evolutionary constraints on skeletal mineralogy, and that although there may be increased costs associated with producing a mineralogy not favored by seawater, the costs of switching mineralogies are even greater.

Constraints on early Cambrian carbon cycling from the duration of the Nemakit-Daldynian–Tommotian boundary δ13C shift, Morocco

The Nemakit-Daldynian–Tommotian (ND-T) boundary marks the first appearance of metazoan reefs and calcite biomineralizers and is associated with the largest δ 13 C shift during the Phanerozoic Eon. Biological transitions in Earth history are often accompanied by excursions in the carbon isotopic composition (δ 13 C) of the ocean, where δ 13 C variability is interpreted to reflect changes in the global carbon cycle. The duration and thus rate of these δ 13 C anomalies are rarely known, making it difficult to constrain their possible causes and their relationship, if any, to biologic transitions. We report sedimentological and δ 13 C data from a new 2.5-km-thick section that spans the early Cambrian evolutionary “explosion” in the Moroccan Anti-Atlas Mountains. Three new zircon 206 Pb- 238 U ages from tuffs within the stratigraphy constrain the timing of the ND-T boundary to 524.84 ± 0.09 Ma. Two of the tuffs exactly bracket the ND-T transition and constrain the duration of the −8‰ δ 13 C shift to 506 ± 126 k.y. With a simple box model, we explore a range of geochemical processes that could account for such a rapid ND-T δ 13 C shift, and conclude that metamorphic and/or volcanic fluxes of carbon may have been sustained at levels 4–16 times higher than today for millions of years.

Chapter 10 Neoproterozoic-Cambrian Biogeochemical Evolution ☆

Abstract The half a billion of years claimed by the Neoproterozoic Era and Cambrian Period marks a great turning point in the history of Earth, beginning with a low diversity and low- P O 2 ocean and atmosphere and ending with a more familiar, oxygen-rich atmosphere–ocean system, populated by diverse animal life. This time period encapsulates many other extraordinary events that helped shape the Earths surface environment, including the break-up and amalgamation of supercontinents, snowball glaciations, true polar wander, and enormous perturbations to the global carbon cycle. The wealth of data emerging from abundant Neoproterozoic-Cambrian sedimentary successions increasingly points to an intimate connection between tectonic, geochemical, climatic, and biospheric change during this pivotal time, highlighting the complexity of the Earth system. Here we briefly review the tectonic, geochemical, and palaeontological records spanning the Neoproterozoic-Cambrian transition as a template for reconstructing the biogeochemical evolution of the surface environment as a habitable Earth emerged.

HALKIERIIDS IN MIDDLE CAMBRIAN PHOSPHATIC LIMESTONES FROM AUSTRALIA

Abstract Halkieriids are part of a distinctive Early Cambrian fauna, the “Tommotian fauna” sensu Sepkoski (1992), that is preserved mostly as phosphatic and secondarily phosphatized skeletal elements. The distinctiveness of the Tommotian fauna is ascribed, in part, to its preferential elimination during the end-Early Cambrian mass extinction event (the “Botomian extinction”). Newly discovered halkieriids in phosphatic limestones of the Middle Cambrian (Ptychagnostus gibbus Zone) Monastery Creek Formation, Georgina Basin, Australia, now indicate that this group not only survived the end-Early Cambrian extinction, but was at least locally abundant thereafter. Most of the Georgina halkieriid sclerites can be accommodated within a single species, Australohalkieria superstes new genus and species, described and partly reconstructed here. Remaining sclerites probably represent two additional but rare halkieriid species. Additional newly discovered sclerites may have affinities with the sachitids, another problematic “Tommotian” taxon related to the halkieriids. Rare wiwaxiid sclerites extend the taphonomic and geographic distribution of this clade. The Monastery Creek Formation provides a valuable window on Middle Cambrian life, both because it provides information that is distinct from but complementary to other, similarly aged windows (e.g., the Burgess Shale) and because it represents a taphonomic window similar to those that preserve Early Cambrian small shelly problematica. A decline during the Cambrian in conditions necessary for the early diagenetic phosphatization of shallow-shelf and platform limestones may have effectively closed this taphonomic window, potentially biasing apparent patterns of diversity change through the period.

Organic-walled microfossil assemblages from glacial and interglacial Neoproterozoic units of Australia and Svalbard

Before the onset of the Neoproterozoic Snowball Earth glaciations, eukaryotes had begun diversifying, and in their aftermath, macroscopic life, including both animals and macroalgae, became abundant and widespread. Although glacially driven mass extinctions have been hypothesized, little is known about the biosphere during and between these glaciations. Here we present new data from organic-walled microfossil assemblages from five successions in Australia and Svalbard that collectively span the first (Sturtian) glaciation and interglacial interval and integrate them with data derived from a critical evaluation of the literature to produce a new estimate of eukaryotic diversity from 850 to 650 Ma. These new glacial and interglacial assemblages consist of only smooth-walled spheroids (leiosphaerids), aggregates of cells, and filaments, in contrast to the much more diverse organic-walled microfossil assemblages found in early Neoproterozoic rocks. This contrast is not attributed to biases in deposition or preservation, but is instead interpreted as reflecting an interval of lowered eukaryotic diversity that spanned the glaciations and that may have begun millions of years prior to their onset.

Tiny vampires in ancient seas: evidence for predation via perforation in fossils from the 780–740 million-year-old Chuar Group, Grand Canyon, USA

One explanation for the Early Neoproterozoic expansion of eukaryotes is the appearance of eukaryovorous predators—i.e. protists that preyed on other protists. Evidence for eukaryovory at this time, however, is indirect, based on inferences from character state reconstructions and molecular clocks, and on the presence of possible defensive structures in some protistan fossils. Here I describe 0.1–3.4 µm circular holes in seven species of organic-walled microfossils from the 780–740 million-year-old Chuar Group, Grand Canyon, Arizona, USA, that are similar to those formed today by predatory protists that perforate the walls of their prey to consume the contents inside. Although best known in the vampyrellid amoebae, this ‘vampire-like’ behaviour is widespread among eukaryotes, making it difficult to infer confidently the identity of the predator. Nonetheless, the identity of the prey is clear: some—and perhaps all—of the fossils are eukaryotes. These holes thus provide the oldest direct evidence for predation on eukaryotes. Larger circular and half-moon-shaped holes in vase-shaped microfossils from the upper part of the unit may also be the work of ‘tiny vampires’, suggesting a diversity of eukaryovorous predators lived in the ancient Chuar sea.