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Micropaleontology of the lower Mesoproterozoic Roper Group, Australia, and implications for early eukaryotic evolution

Published online by Cambridge University Press:  22 December 2016

Emmanuelle J. Javaux
Affiliation:
Department of Geology, UR Geology, University of Liège, 14 allée du 6 Août B18, Quartier Agora, Liège 4000, Belgium 〈ej.javaux@ulg.ac.be〉
Andrew H. Knoll
Affiliation:
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA 〈aknoll@oeb.harvard.edu〉

Abstract

Well-preserved microfossils occur in abundance through more than 1000 m of lower Mesoproterozoic siliciclastic rocks composing the Roper Group, Northern Territory, Australia. The Roper assemblage includes 34 taxa, five interpreted unambiguously as eukaryotes, nine as possible eukaryotes (including Blastanosphaira kokkoda new genus and new species, a budding spheromorph with thin chagrinate walls), eight as possible or probable cyanobacteria, and 12 incertae sedis. Taxonomic richness is highest in inshore facies, and populations interpreted as unambiguous or probable eukaryotes occur most abundantly in coastal and proximal shelf shales. Phylogenetic placement within the Eukarya is difficult, and molecular clock estimates suggest that preserved microfossils may belong, in part or in toto, to stem group eukaryotes (forms that diverged before the last common ancestor of extant eukaryotes, or LECA) or stem lineages within major clades of the eukaryotic crown group (after LECA). Despite this, Roper fossils provide direct or inferential evidence for many basic features of eukaryotic biology, including a dynamic cytoskeleton and membrane system that enabled cells to change shape, life cycles that include resting cysts coated by decay-resistant biopolymers, reproduction by budding and binary division, osmotrophy, and simple multicellularity. The diversity, environmental range, and ecological importance of eukaryotes, however, were lower than in later Neoproterozoic and Phanerozoic ecosystems.

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Copyright © 2016, The Paleontological Society

Introduction

In classifying the past 541 million years as the Phanerozoic Eon, stratigraphers give formal recognition to the animal fossils commonly found in rocks of this age. In terms of evolution, the age of animals must form the latter part of a phylogenetically broader and historically deeper age of eukaryotes, but when protists emerged as major participants in marine ecosystems remains uncertain. Molecular clocks, calibrated largely by Phanerozoic fossils, nearly all suggest that crown group eukaryotes emerged during the Proterozoic Eon. The error bars are large, but even so, the oldest (ca. 2000 Ma) and youngest (800 Ma or a bit earlier) molecular estimates for the divergence of crown group eukaryotes do not overlap (e.g., Douzery et al., Reference Douzery, Snell, Bapteste, Delsuc and Philippe2004; Hedges et al., Reference Hedges, Blair, Venturi and Shoe2004; Yoon et al., Reference Yoon, Hackett, Ciniglia, Pinto and Bhattacharya2004; Berney and Pawlowski, Reference Berney and Pawlowski2006; Chernikova et al., Reference Chernikova, Motamedi, Csueroes, Koonin and Rogozin2011; Parfrey et al., Reference Parfrey, Lahr, Knoll and Katz2011; Eme et al., Reference Eme, Sharpe, Brown and Roger2014). Neither early nor late crown group emergence precludes the possibility of a substantial earlier record of stem group eukaryotes (Javaux et al., Reference Javaux, Marshall and Bekker2010; Javaux, Reference Javaux2011; Knoll, Reference Knoll2014; Sugitani et al., Reference Sugitani, Mimura, Takeuchi, Lepot, Ito and Javaux2015; Butterfield, Reference Butterfield2015).

Diverse eukaryotic microfossils occur in rocks 800 Ma and younger (Porter et al., Reference Porter, Meisterfeld and Knoll2003; Butterfield, 2004; Butterfield, Reference Butterfield2005a, Reference Butterfield2005b; Knoll et al., Reference Knoll, Javaux, Hewitt and Cohen2006; Cohen and Knoll, Reference Cohen and Knoll2012), and these include at least a few populations assigned with confidence to extant eukaryotic clades (e.g., Butterfield et al., Reference Butterfield, Knoll and Swett1994; Porter et al., Reference Porter, Meisterfeld and Knoll2003). Accepting the ~1100-Ma fossil Bangiomorpha pubescens as a red alga (Butterfield, Reference Butterfield2000), possibly a stem group rhodophyte (Yang et al., Reference Yang, Boo, Battacharya, Saunders, Knoll, Fredericq, Graf and Yoon2016), further requires that crown group eukaryotes evolved earlier than this. Older microfossils potentially push the eukaryotic crown group still deeper into the past (Moczydłowska et al., Reference Moczydłowska, Landing, Zang and Palacios2011; Butterfield, Reference Butterfield2015), but only if these fossils can be confidently interpreted not only as eukaryotes but also as crown versus stem group taxa—a potentially challenging distinction in ancient rocks (Knoll, Reference Knoll2014).

Improved understanding of the timing and context of early eukaryotic divergence begins with careful systematic analysis of well-preserved fossil populations drawn from basins characterized by good age and environmental control. One such basin is recorded by the Mesoproterozoic Roper Group, Northern Territory, Australia. Abundant microfossils were discovered in coastal marine mudstones of the McMinn Formation, near the top of the group (Peat et al., Reference Peat, Muir, Plumb, McKirdy and Norwick1978). Our investigations reveal that fossils are abundant and exceptionally well preserved throughout the Roper succession, enabling us to document the paleoenvironmental as well as stratigraphic distribution of microfossil assemblages (Javaux et al., Reference Javaux, Knoll and Walter2001).

Geologic setting

The Roper Group is a ramp-like sedimentary succession developed in association with regional rifting following an episode of late Paleoproterozoic tectonism known locally as the Isan Orogeny (Betts and Gilles, Reference Betts and Gilles2006; de Vries et al., Reference de Vries, Pryer and Fry2008). Although limited Roper outcrop is dominated by erosionally resistant sandstone units, an extensive and lithologically heterogeneous record of Roper deposition is available in drill core obtained during the 1970s and 1980s. The >1800 m Roper succession consists almost entirely of siliciclastic rocks divided by Abbott and Sweet (Reference Abbott and Sweet2000) into half a dozen third-order sedimentary sequences. Environments recorded in each sequence range from basinal black shales deposited below storm wave base during maximum flooding to paralic and even fluviatile sandstones, as well as oolitic ironstones found as a marginal-marine facies in highstand systems tracts. Depositional age is constrained by a U-Pb zircon age of 1492±4 Ma for a tuff in the Mainoru Formation, low in the Roper succession (Jackson et al., Reference Jackson, Sweet, Page and Bradshaw1999), Re-Os shale dates of 1417±29 Ma and 1361±21 Ma for the Velkerri Formation in the upper part of the succession (Kendall et al., Reference Kendall, Creaser, Gordon and Anbar2009), and a less reliable, but broadly consistent Rb-Sr illite date of 1429±31 Ma for shale within the McMinn Formation, near the top of the group (Kralick, Reference Kralik1982). Thus, Roper deposition took place about 1500–1400 Ma (Figure 1).

Figure 1 The Roper Group, showing location, facies distribution and stratigraphic column (modified from Javaux et al., Reference Javaux, Knoll and Walter2001).

Surface waters in the Roper seaway were oxic, as determined by iron-speciation chemistry (Shen et al., Reference Shen, Knoll and Walter2003), but several lines of evidence indicate that within the Roper basin the oxygen minimum zone was commonly anoxic and ferruginous, and at times euxinic (Shen et al., Reference Shen, Knoll and Walter2003; Planavsky et al., Reference Planavsky, McGoldrick, Scott, Li, Reinhard, Kelly, Chu, Bekker, Love and Lyons2011). Consistent with this, S isotopic data document an active microbial sulfur cycle (Shen et al., Reference Shen, Knoll and Walter2003; Johnston et al., Reference Johnston, Farquhar, Summons, Shen, Kaufman, Masterson and Canfield2008), with facies-specific differences in expressed fractionation suggesting that bacterial sulfate reduction occurred in the water column in basinal environments, but was confined to sediments in coastal settings (Shen et al., Reference Shen, Knoll and Walter2003). Mo abundance and isotope values for Roper samples point more broadly to early Mesoproterozoic oceans with widespread subsurface anoxia, including sulfidic water masses more extensive than today (Arnold et al., Reference Arnold, Anbar, Barling and Lyons2004; Kendall et al., Reference Kendall, Creaser, Gordon and Anbar2009), with some exceptions locally (Sperling et al., Reference Sperling, Rooney, Hays, Sergeev, Vorob’eva, Sergeeva, Selby, Johnston and Knoll2014).

Materials and methods

Carbonaceous shales occur throughout the Roper succession in environmental settings that range from basinal to lagoonal (Abbott and Sweet, Reference Abbott and Sweet2000; Javaux et al., Reference Javaux, Knoll and Walter2001). A majority of these shales contain microfossils preserved as organic compressions, and in a subset of these, distributed throughout the succession, preservation is excellent. The fossils described here come from the following cores: Amoco (A) 82-3 and Golden Grove (GG) 1, reposited at the Northern Territory Geological Survey in Darwin, and Urapunga (U) cores 4, 5, and 6, reposited at the Australian Geological Survey Organization, Canberra. Collectively, these cores represent most of the Roper Group, save for the upper McMinn and Chambers River formations at the top of the succession.

All microfossils come from residues of static acid maceration and have been examined with transmitted light microscopy. For some taxa, detailed morphological observations with SEM, wall ultrastructure with TEM, and wall microchemistry are described elsewhere (Javaux et al., Reference Javaux, Knoll and Walter2003, Reference Javaux, Knoll and Walter2004; Marshall et al., Reference Marshall, Javaux, Knoll and Walter2005). Systematic description is focused on the genus and species levels, with taxa ordered alphabetically, and the International Code of Nomenclature for Algae, Fungi, and Plants is followed. Sample number includes core number and depth (e.g., U6 230.8 m is sample from core Urapunga 6 at 230.8 m depth).

Repositories and institutional abbreviations

All illustrated specimens are reposited in the Paleobotanical Collections of Harvard University (HU numbers).

Systematic paleontology

Classification of Roper microfossils presents challenges at either end of the Linnean hierarchy, in both cases reflecting the limited availability of systematically useful characters and character states. At the fine scale, the challenge is to recognize discrete populations and classify them in light of previously diagnosed taxa. Populations can be demarcated in terms of general form (e.g., spheroidal versus cylindrical), size frequency distribution, surface ornamentation when present, and wall thickness and textures (when obvious ornamentation is absent).

Preliminary research shows that morphologically simple Mesoproterozoic microfossils can also preserve distinct wall ultrastructures (Javaux et al., Reference Javaux, Knoll and Walter2004), but extensive TEM imaging would be prohibitive, and existing diagnoses do not take ultrastructural characters into account. Because of character limitations and the ways that observed traits have been used in classification, it can be easier to recognize populations as distinct than it is to assign them to formal taxa, especially for the abundant but simple spheroidal vesicles known as leiosphaerids. We recognize 34 distinct entities within the Roper assemblage.

The other systematic challenge is to relate Roper populations to higher taxa, which can be problematic even at the level of domain. For this reason, we find it useful to provide qualitative confidence estimates for phylogenetic interpretation—with what degree of certainty we recognize a given population as eukaryotic or bacterial. We show that five morphospecies can be classified with confidence as eukaryotes, including three distinct populations of ornamented spheromorphic acritarchs (Dictyosphaera delicata, Satka favosa, and Valeria lophostriata), one acanthomorphic acritarch (Tappania plana), and one population of large striated tubes (Lineaforma elongata). Nine additional taxa are considered possible eukaryotes (six smooth-walled spheromorphs: Leiosphaeridia crassa, L. jacutica, L. minutissima, L. tenuissima, Leiosphaeridia sp., and L. ternata; one spheromorph population with a granular wall texture (L. atava), and two populations of budding spheromorphs (cf., Gemuloides doncookii and Blastanosphaira kokkoda). Eight taxa of filaments (Palaeolyngbya catenata, five species of Siphonophycus, Trachytrichoides sp.) and vesicles with rounded bulges inferred to be imprints of internal cells (Squamosphaera colonialica), are interpreted as probable cyanobacteria, whereas 12 distinctive populations can be classified only as incertae sedis; this group includes five types of spheromorphs (Unnamed forms B to E), six colonial forms (Chlorogloeaopsis contexta, cf. Coneosphaera arctica, Eomicrocystis magilca, Synsphaeridium spp., Symplassosphaeridium spp., and a large compartmentalized multicellular form—unnamed form A), and two filamentous taxa (Tortunema sp. and unnamed form F). Some of the Roper colonial and filamentous microfossils are interpreted as probable cyanobacteria because of both their occurrence in shallow-water photic zone and their morphology.

Genus Blastanosphaira new genus

Type species

Blastanosphaira kokkoda, by monotypy

Diagnosis

As for type species.

Etymology

From the greek βλασταυω, to bud or to germinate, σφαιρα, sphere, and κοκκωδη, granular.

Blastanosphaira kokkoda new species

Figure 2.1–2.11

Figure 2 Photographs of Roper organic-walled microfossils: (1–11) Blastanosphaira kokkoda n. gen. n. sp.; (2) specimen starting budding; (3) specimen showing an elongate expansion; (4) specimen showing circular opening; (6) the bottom specimen’s wall is peeling off the vesicle; (8) thick folds between attached specimens; (5–8) specimens showing multiple budding; (11) SEM picture showing details of granular wall. (12–13) Chlorogloeaopsis contexta. (14) Coneosphaera artica. (15) Dictyosphaera delicata. (16–18) Eomicrocystis magilca: (17) detail of (16) showing oval cells and absence of external envelope. Scale bar in (1) is: (1, 2, 8, 9, 10) 13 µm; (3, 14, 16, 18) 20 µm; (4, 13, 17) 10 µm; (5) 80 µm; (6, 7) 15 µm; (11) 500 nm; (12) 50 µm. Slides and England coordinates are (1) U5 569.1 m .2 Q42, (2, 3) U5 569.1 m .2 Q40/2, (4) U5 569.1 m .2 R43, (5) U5 569.1 m .2 R/S42, (6) U5 569.1 m .2 R43, (7–10) U5 536.6 m .2 P33, (12, 13) U6 240.2 m .2 S16, (14) A82/3 311.3 m O5/2, (15) GG1 48.75 m .2 J43/4, (16) U5 125.1 m .2 N33/2, (18) U6 230.8 m H16.

Holotype

Specimen Figure 2.1, palynological slide U5 569.1 m, England finder coordinates R/S42, from the Wood Duck Member of the Mainoru Formation, Roper Group.

Diagnosis

Spheromorph, a few up to ~100 µm in diameter, with very thin chagrinate wall, small sinuous folds, and one lanceolate fold predominantly near the margins of compressed vesicles. Division by budding, with one or several large spherical scars left by detaching buds; serial budding without cells detaching common, leading to a colonial habit. Commonly, taphonomic alteration results in the thin wall peeling off the vesicle from an equally tenuous internal layer.

Occurrence

Mesoproterozoic, Wood Duck Member of the Mainoru Formation, Roper Group, Australia.

Description

Spheromorph with very thin chagrinate wall and small sinuous folds, and one lanceolate fold predominantly near the margins of compressed vesicles. Size 3–93 µm in minimum diameter (mean: 28.7 µm, σ=16.8 µm, N=149). Two specimens oval shaped (52–104 µm long and 32–64 µm wide), and one specimen (27 µm in diameter) bears an elongate expansion (40 µm long x 8 µm wide) (Fig. 2.3). Division by budding, with cells staying attached and forming irregular colonies, cells rarely isolated, often attached to one to four other cells, commonly with large spherical scars left by detaching buds or adjacent cells. Range of diameter and morphology may vary greatly, from spherical to oval to filamentous. Commonly, taphonomic alteration results in the thin wall peeling off the vesicle from an equally tenuous internal layer.

Materials

149 specimens measured, as clustered populations in basinal facies (samples U5 581.9 m and 569.1 m in the Wood Duck Member of the Mainoru Formation).

Remarks

The Roper population forms an essentially monospecific assemblage in euxinic basinal shales, and is rare in other facies. It differs from Gemmuloides by the thin chagrinated wall, circular scars, and multiple attached buds forming colonies. It also differs from Eosaccharomyces ramosus Hermann, another budding spheromorph forming colonies, by the chagrinate ornamentation of the vesicle wall, and taphonomic features such as circular scars (Fig. 2.4) and one large lanceolate fold at periphery and very thin folds more centrally distributed (Fig. 2.1, 2.10). The attachment to a biofilm reported and illustrated by Hermann (Reference Hermann1990, pl. 14) and Hermann and Podkovyrov (Reference Hermann and Podkovyrov2012) is not observed for the Roper population, although it is not mentioned as a diagnostic character (Jankauskas et al., Reference Jankauskas, Mikhailova and Hermann1989). Growth of oval cells oriented in the direction of the “branches” of the colony do occur in the Lakhanda material, as underscored by Knoll et al. (Reference Knoll, Javaux, Hewitt and Cohen2006), but this is not always the case (see Hermann Reference Hermann1990, pl. 14, figs. 5, 7), and is not reported as a diagnostic criterion in Jankauskas et al. (Reference Jankauskas, Mikhailova and Hermann1989). The chagrinate spheromorphs commonly show evidence of budding (Fig. 2.2–2.8), forming spheres (Fig. 2.6–2.8) or elongate extensions (Fig. 2.3), with up to seven specimens attached. Some specimens bear a distinct circular hole rimmed by a fold in the wall (with a diameter up to more than 60% of the vesicle diameter) (Fig. 2.4). Because budding specimens may bear this hole (Fig. 2.7), it cannot be interpreted as a pylome (excystment structure), but rather as a scar left when connected individuals detached. Commonly, the thin wall has partially peeled off, exposing the lighter inner side of the vesicle wall (Fig. 2.6). Cells can be isolated, or more commonly attached to 1 to 4 other cells (Fig 2.7). Blastanosphaira kokkoda differs also from other spheromorphs with chagrinate walls, such as L. obsuleta and L. atava, by its prominent budding habit and consequent colonial association, very thin wall, and circular scars.

The chagrinate appearance seems to be an ornamentation rather than taphonomic alteration, suggesting eukaryotic affinity. SEM shows a granular wall and occasional taphonomic holes (Fig. 2.11). Budding is also consistent with eukaryotic affinities, resembling yeast behavior, but detailed ultrastructural and microchemical analyses will be required to confirm the affinity of this population. Due to its budding without cells detaching and forming colonies, E. ramosus has been interpreted as a possible fungus (yeast-like) by Hermann and Podkovyrov (Reference Hermann and Podkovyrov2012) or as social amoebae, although these are difficult to preserve as compressions (Porter, Reference Porter2006), except in stages of their life cycle when they can produce cellulose walls. Interestingly, cells of the modern yeast Saccharomyces may bear several circular scars, and when budding rapidly, form pseudomycelia. However, budding as a form of asexual reproduction also occurs in some bacteria (cyanobacteria, prosthecate proteobacteria; Angert, Reference Angert2005), in addition to some protists, fungi (yeast), and animals. The chagrinate ornamentation of the wall combined with large size suggest the Roper fossils are probable eukaryotes, and their common budding and pseudocolonial habit shows they represent metabolically active, reproducing vegetative cells. Their restricted distribution in deeper anoxic facies may suggest an anaerobic metabolism (see Muller et al., 2012 for a review of modern anaerobic eukaryotes) or facultatively aerobic metabolism at low oxygen tensions. Alternatively, they could have been planktonic, but in this case, their limitation to deeper anoxic facies is difficult to explain.

Genus Chlorogloeaopsis Maithy, Reference Maithy1975, emend. Hofmann and Jackson, Reference Hofmann and Jackson1994

Type species

Chlorogloeaopsis zairensis Maithy, Reference Maithy1975, from the Bushimay (now Mbuyi-Mayi) Supergroup, RDC, Meso-Neoproterozoic.

Other species

Chlorogloeaopsis kanshiensis (Maithy, Reference Maithy1975), n. comb. Hofmann and Jackson, Reference Hofmann and Jackson1994; Chlorogloeaopsis contexta (Hermann, 1976) n. comb. Hofmann and Jackson, Reference Hofmann and Jackson1994.

Chlorogloeaopsis contexta (Hermann in Timofeev, Hermann, and Mikhailova, Reference Timofeev, Hermann and Mikhailova1976), emend. Hofmann and Jackson, Reference Hofmann and Jackson1994

Figure 2.12–2.13

1976 Polysphaeroides contextus Hermann in Reference Timofeev, Hermann and MikhailovaTimofeev, Hermann, and Mikhailova, p. 42, pl. 14, fig. 3

1989 Polysphaeroides contextus; Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 119, pl. 27, figs. 10a, b

1990 Polysphaeroides contextus; Reference HermannHermann, p. 26, pl. 8, fig. 8

1994 Chlorogloeaopsis contexta; (Hermann in Timofeev et al., Reference Timofeev, Hermann and Mikhailova1976), emend. Reference Hofmann and JacksonHofmann and Jackson, p. 19, figs. 12.13–12.15

Holotype

Polysphaeroides contextus Hermann, 1976 in Timofeev, Hermann, and Mikhailova, p. 42–43, pl. 14, fig. 3; from the late Riphean (Tonian) Miroedikha Formation of the Turukhan Uplift, Siberia.

Occurrence

Mesoproterozoic and Neoproterozoic successions worldwide, such as the Mbuyi-Mayi Supergroup, RDC; the Miroedikha Formation of the Turukhan Uplift, Siberia; the Roper Group, Australia; the Bylot Supergroup, Canada.

Description

One cylindrical colony without envelope, composed of several indistinctly defined rows of cells 3–5 µm wide; colony 400 µm long and 25 µm wide.

Materials

One specimen from sample U6 240.2 m, Mainoru Formation.

Remarks

The spelling of the genus was corrected by Hofmann and Jackson (Reference Hofmann and Jackson1994, p. 18–19) and simultaneously (both in July 1994) by Butterfield et al. (Reference Butterfield, Knoll and Swett1994, p. 72). Hofmann and Jackson (Reference Hofmann and Jackson1994) recognized three species of Chlorogloeaopsis: C. contexta (Hermann, 1976) n. comb. Hofmann and Jackson, Reference Hofmann and Jackson1994, has indistinct rows of cells and cell diameter ranging from 1 to 5 µm; C. zairensis Maithy, Reference Maithy1975 with cells 8 to 10 µm in diameter, two to four in a row, while C. kanshiensis has cells 10–15 µm in diameter, two or three distinct rows of cells. The Roper population differs from C. kanshiensis, defined by two or three rows of cells, and from Polysphaeroides spp., which are loose aggregates of spheroidal dispersed cells or pairs, tetrads, octads, and spheroidal colonies of up to 10–20 cells in a sheath.

Genus Coneosphaera Luo, Reference Luo1991

Type species

Coneosphaera inaequalalis Luo, Reference Luo1991, from the Changlongshan Formation, Neoproterozoic, China.

Other species

Coneosphaera artica Hofmann and Jackson, Reference Hofmann and Jackson1994; Coneosphaera sp. Hofmann and Jackson, Reference Hofmann and Jackson1994.

Coneosphaera sp.

Figure 2.14

Description

50–51 µm thin-walled light brown spheromorphs loosely associated with many smaller 2–4 µm vesicles on the wall surface and close to their periphery. Three specimens observed.

Materials

Three specimens from sample U6 226.95 m, Mainoru Formation.

Remarks

Our specimens differ from C. artica, which shows larger diameters of both large and small vesicles (79–130 µm and 8–11 µm, respectively) and a higher number of the loosely attached or closely associated small vesicles. It also differs from C. sp. in the Bylot Group (Hofmann and Jackson, Reference Hofmann and Jackson1994), which has a few vesicles firmly attached to a larger central one and resembles a specimen illustrated by Hermann (Reference Hermann1990, p. 20, pl. 5.11) in the Miroedikha Formation, Siberia. It differs from C. inaequalalis, which is characterized by a large cell three or four times bigger than the attached smaller cells, and one cell much smaller than the others (Luo, Reference Luo1991, p. 193).

Genus Dictyosphaera Xing and Liu, Reference Xing and Liu1973

Type species

Dictyosphaera macroreticulata Xing and Liu, Reference Xing and Liu1973, from the Chuanlingguo Formation, Yenliao region; Chih County of Hopei, northern China, Mesoproterozoic.

Dictyosphaera macroreticulata Xing and Liu, Reference Xing and Liu1973

Figure 2.15

1973 Dictyosphaera macroreticulata Reference Xing and LiuXing and Liu, p. 22, 58, pl. 1, 16–17.

1982 Dictyosphaera delicata; Reference Hu and FuHu and Fu, p. 108, pl. 2, figs. 3–6.

2001 Dictyosphaera sp.; Reference Javaux, Knoll and WalterJavaux et al., fig 1e.

2003 Dictyosphaera delicata; Reference Kaufman and XiaoKaufman and Xiao, fig. 1.

2005 Dictyosphaera delicata; Reference Yin, Yuan, Meng and HuYin et al., p. 52, fig. 2.1, 2.2, 2.4, 2.5, 2.7, 2.9, 2.10.

2007 Dictyosphaera delicata; Reference Yin and YuanYin and Yuan, p. 351, fig. 1.1.

2009 Dictyosphaera delicata; Reference Schiffbauer and XiaoSchiffbauer and Xiao, fig. 3f.

?2011 “ellipsoidal vesicle with a micro-reticulate wall” Reference Strother, Battison, Brasier and WellmanStrother et al., fig. 1i, j.

2015 Dictyosphaera macroreticulata; Reference Agic, Moczydłowska and YinAgic et al., p. 32, figs. 2–4.

Lectotype

Specimen originally described as Dictyosphaera sinica Xing and Liu, Reference Xing and Liu1973, from the Chuanlingguo Formation, Yenliao region, Chih County of Hopei, northern China, Mesoproterozoic, and junior synonym of D. macroreticulata Xing and Liu (Reference Xing and Liu1973, pl. I:18) (Agic et al., Reference Agic, Moczydłowska and Yin2015).

Occurrence

Paleoproterozoic and Mesoproterozoic of China (Ruyang and Gaoshanhe Groups) (Xing and Liu, Reference Xing and Liu1973), Australia (Roper Group) (Javaux et al., Reference Javaux, Knoll and Walter2001), Belt Supergroup (Adam, Reference Adam2014).

Description

Only three specimens observed in the Roper population, one specimen measured: 50 µm in diameter with polygonal plates less than 2 µm wide. No excystment structure observed.

Materials

Three specimens in basinal mudstones of the Velkerri Formation (sample GG1 48.75 m).

Remarks

Agic et al. (Reference Agic, Moczydłowska and Yin2015) revised the taxonomy of the genus Dictyosphaera and synonymized all the species previously described (D. delicata, D. sinica, D. gyrorugosa, D. incrassata) to the senior species D. macroreticulata, described as 10 to 300 µm vesicles ornamented by a reticulate polygonal pattern consisting of interlocking 1–6 µm polygonal plates. Excystment by pylome or medial split. Because the holotype was not available for re-examination, they selected a lectotype from the same material as the holotype. In their original diagnosis, Hu and Fu (Reference Hu and Fu1982) described a reticulate surface ornamentation, but did not comment on its fine structure. TEM analysis by Yin et al. (Reference Yin, Yuan, Meng and Hu2005) subsequently demonstrated that the wall is made of interlocked polygonal plates 1–3 µm wide, perforated by nanopores observed with SEM on both the exterior and interior vesicle surfaces (Kaufman and Xiao, Reference Kaufman and Xiao2003). The wall ultrastructure is multilayered (FIB-EM analyses; Schiffbauer and Xiao, Reference Schiffbauer and Xiao2009), and excystment by partial rupture or a circular opening (pylome) has also been observed (Yin et al., Reference Yin, Yuan, Meng and Hu2005).

Dictyosphaera macroreticulata is reported from the ~1580–1460 Ma Lower Belt Group, USA (Adam, Reference Adam2014), as well as the 1400–1700 Ma Ruyang and broadly correlative Gaoshanhe groups of China, where it co-occurs with abundant Shuiyousphaeridium macroreticulatum, an acanthomorph with similar wall ornamentation but bearing many processes (Xiao et al., Reference Xiao, Knoll, Kaufman, Yin and Zhang1997; Schiffbauer and Xiao, Reference Schiffbauer and Xiao2009). In the Chinese assemblages, Dictyosphaera specimens may include life cycle or taphonomic variants of Shuiyousphaeridium (Xiao et al., Reference Xiao, Knoll, Kaufman, Yin and Zhang1997) that either lost or never formed the outer wall layer from which processes arise (Javaux et al., Reference Javaux, Knoll and Walter2004). The Chinese population includes vesicles ranging from 28 to 240 µm in diameter, with 1–4 µm platelets (Agic et al., Reference Agic, Moczydłowska and Yin2015). In the Roper Group, however, D. macroreticulata (=D. delicata) is rare and Shuiyousphaeridium absent. Dictyosphaera possibly occurs, as well, in the ~1000 Ma Stoer and lower Torridon groups, Scotland (Javaux, personal observation, 2008), although it is unnamed in Strother et al. (Reference Strother, Battison, Brasier and Wellman2011), who described a population as ellipsoidal fossils with walls made of highly ordered circular pits, creating a reticulate pattern and, therefore, differing from the plate-like wall structure of the Mesoproterozoic Dictyosphaera.

Kaufman and Xiao (Reference Kaufman and Xiao2003) suggested that D. macroreticulata (=D. delicata) was a photosynthetic eukaryote based on its complex morphology and C-isotopic composition. Neither morphology nor isotopic composition, however, is diagnostic with respect to energy metabolism, although the eukaryotic nature of this ornamented acritarch is convincing. Functionally, D. macroreticulata is most likely a cyst or resting stage common to the life cycles of metabolically diverse eukaryotes (see below).

Recently, Tang et al. (Reference Tang, Pang, Yuan, Wan and Xiao2015) described a new species, D. tacita, based on two specimens that differ from the other species by their smooth external surface and the presence of hexagonal platelets only on the interior vesicle surface. The hexagons are smaller (0.5–0.9 µm) and the vesicle diameter larger (100–120 µm) than those of D. macroreticulata (2–6 µm platelets, 10–20 µm vesicle diameter), D. sinica (0.5–1.5 µm platelets, 15–45 µm vesicle diameter), and D. delicata (1–3 µm platelets, 50–300 µm vesicle diameter). However, Agic et al. (Reference Agic, Moczydłowska and Yin2015) proposed a synonymy among D. delicata, D. macroreticulata, and other species of the genus based on the overlapping size range of the vesicles and wall platelets, and similar morphologies. Tang et al. (Reference Tang, Pang, Yuan, Wan and Xiao2015) argued that this needs reevaluation.

Genus Eomicrocystis Golovenok and Belova, Reference Golovenok and Belova1986

Type species

Eomicrocystis magilca Golovenok and Belova, Reference Golovenok and Belova1986

Other species

Eomicrocystis elegans Golovenok and Belova, Reference Golovenok and Belova1986

Eomicrocystis magilca Golovenok and Belova, Reference Golovenok and Belova1986

Figure 2.16–2.18

1986 Eomicrocystis magilca Reference Golovenok and BelovaGolovenok and Belova, p. 95 [English version p. 89], pl. 7., figs. 5–7.

1989 Eomicrocystis magilca; Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 91, pl. 19, fig. 7.

1994 Eomicrocystis magilca; Reference Hofmann and JacksonHofmann and Jackson, p. 25, pl. 18, figs. 2–4.

1997 Eomicrocystis magilca; Reference CotterCotter, p. 258, fig. 7A, B.

2016 Eomicrocystis magilca; Baludikay et al., Reference Baludikay, Storme, François, Baudet and Javaux2016, p. 179, fig. 12f.

Holotype

Eomicrocystis malgica Golovenok and Belova, Reference Golovenok and Belova1986, pl. 7, fig. 5, from the Malgina Formation in the Uchur-Maya region, eastern Siberia.

Description

Small ovoid or spheroidal colonies of light brown, loosely packed, small spheroidal to ovoid vesicles of uniform size, sometimes dividing by binary fission, without enclosing envelope. Three colonies observed, with cells 3 µm wide and 6–7 µm long.

Occurrence

Mesoproterozoic and early Neoproterozoic, Roper Group, Australia; Malgina Formation in the Uchur-Maya region, eastern Siberia (Golovenok and Belova, Reference Golovenok and Belova1986); Bylot Supergroup, Canada (Hofmann and Jackson, Reference Hofmann and Jackson1994); Belt Supergroup, USA (Adam et al., 2016); Mbuyi-Mayi Supergroup, RDC (Baludikay et al., Reference Baludikay, Storme, François, Baudet and Javaux2016).

Materials

Three colonies in samples U5 125.1 m from the Jalboi Formation and U6 230.8 m from the Mainoru Formation.

Remarks

Eomicrocystis differs from the genus Coleogleba (Strother et al., Reference Strother, Knoll and Barghoorn.1983) in lacking an organic matrix or distinct envelope enclosing the cell clusters, and from the genus Coniunctiophycus by the absence of a single dense mass less than a micron in diameter within cells, the smaller cell size (10 µm in C. sp), and the shape of the colony described in the Belt Supergroup as “spheroidal colony of tens of individuals, from which a wide, linear extension of more cells emerges and folds back onto itself to form a single reticulate fold” (Adam et al., Reference Adam, Skidmore and Mogk2016, p. 16). It also differs from described species of Myxococcoides (Schopf, Reference Schopf1968) in the size and organization of constituent cells. Eomicrocystis malgica differs from E. elegans by the smaller size of the cells’ minimum diameter (3–5 µm versus 6–9 µm) and more regular shape of the aggregate. The Roper colonies have cell diameters intermediate between the two species, but also have an irregular aggregate shape, and therefore are identified as E. malgica.

Genus Gemmuloides Samuelsson and Butterfield, Reference Samuelsson and Butterfield2001

Type species

Gemmuloides doncooki Samuelsson and Butterfield Reference Samuelsson and Butterfield2001

cf. Gemmuloides doncooki Samuelsson and Butterfield, Reference Samuelsson and Butterfield2001

Figure 4.1

2001 Gemmuloides doncooki Reference Samuelsson and ButterfieldSamuelsson and Butterfield, p. 248, fig 7, D–F.

2014 Gemmuloides doncooki; Reference AdamAdam, p. 35, fig. 13.

Holotype

Gemmuloides doncooki Samuelsson and Butterfield, Reference Samuelsson and Butterfield2001, p. 248, 249, GSC 117042 (Fig. 7D), Lone Land Formation, NW flank of Cap Mountain (63°24'11''N, 123°14'12''W), Canada, approximately 2 m above carbonate ledge. Sample 94-LL-8. GSC loc. C-404520.

Description

Two spheromorphs, 260 and 85 µm diameter, with chagrinate wall were observed, each with a dark central sphere; only one shows evidence of budding. The presence of a dark central body is not included in the original description, but this may reflect taphonomic rather than systematic differences. The presence of a bud allies the Roper fossils with Gemmuloides doncooki.

Occurrence

Roper Group, Australia; Lone Land Formation, Canada (Samuelsson and Butterfield, Reference Samuelsson and Butterfield2001); Belt Supergroup, USA (Adam, Reference Adam2014).

Materials

Two adjacent specimens in samples A82/3 328.35 m from the Jalboi Member and U6 240.2 m from the Mainoru Formation.

Remarks

The Roper assemblage includes another budding spheromorph, Blastanosphaira kokkoda, which differs from cf. G. doncooki by its colonial habit, smaller diameter, thinner chagrinate wall with thin folds, and multiple buds of larger size relative to the mother cell, as well as by the presence of circular scars left by detached buds. Coneosphaera sp. in the Bylot Group (Hofmann and Jackson, Reference Hofmann and Jackson1994) has several smaller vesicles attached to a central one, resembling a specimen illustrated by Hermann (Reference Hermann1990, p. 20, pl. 5.11) from the Miroedikha Formation, Siberia, which also differs from cf. G. doncooki. Gemmuloides doncooki is also reported in the Belt Supergroup, Montana, USA (Adam, Reference Adam2014).

Genus Leiosphaeridia Eisenack, Reference Eisenack1958, emend. Downie and Sarjeant, Reference Downie and Sarjeant1963, emend. Turner, Reference Turner1984

Type species

Leiosphaeridia baltica Eisenack, Reference Eisenack1958.

Remarks

Jankauskas (1989) revised the taxonomy of the genus Leiosphaeridia (see for detailed synonymy) and proposed an operational approach to species recognition within the genus Leiosphaeridia, essentially diagnosing species based on a combination of two characters: size and wall texture. Subsequent workers have tended to follow this scheme, with some modifications (e.g., Butterfield et al., Reference Butterfield, Knoll and Swett1994; Hofmann and Jackson, Reference Hofmann and Jackson1994). Jankauskas (1989) discriminated four smooth-walled Leiosphaeridia species: L. crassa and L. jacutica are thick-walled leiospheres, smaller or larger than 70 µm in diameter, respectively; L. minutissima and L. tenuissima are thin-walled vesicles, again smaller or larger than 70 µm in diameter, respectively. A fifth species, L. ternata differs from other species in having a distinctively rigid, opaque wall that fractures radially. Chuaria circularis is also a smooth-walled spheromorph, but can be discriminated from the leiospheres by its much thicker wall (at least 2 µm thick), concentric folds and wrinkles, and large diameter (0.43–3.5 mm), leaving textured imprints on bedding surfaces (Butterfield et al., Reference Butterfield, Knoll and Swett1994).

The difficulty of applying the modified Jankauskas classification lies in the potential challenge of estimating wall thickness (underscored by Butterfield et al., Reference Butterfield, Knoll and Swett1994) and in classifying populations that do not fit neatly within the proposed size classes, as also noticed by Porter and Riedman (in press) in populations from the Neoproterozoic Chuar Group. Thus, while Butterfield et al. (2004) and Hofmann and Jackson (Reference Hofmann and Jackson1994) reported a taxonomic break at 70 µm, there is little in the size frequency diagrams they present to justify this. Wall thickness has commonly been estimated on the basis of color or fold morphology, but wall color can vary as a function of taphonomy, thermal maturity, or original composition. Butterfield (in Butterfield et al., Reference Butterfield, Knoll and Swett1994, p. 11–12) has discussed the distinction between the thickness of folds and the thickness of the wall, which are not necessarily correlated. Previous study of wall ultrastructure in different Leiosphaeridia species from the Roper Group (Javaux et al., Reference Javaux, Knoll and Walter2003, Reference Javaux, Knoll and Walter2004) showed that L. crassa with thick lanceolate folds had a thinner wall than L. tenuissima with thin sinuous folds. We suggest that fold morphology, which reflects the taphonomy of walls with biological differences in flexibility, provides a more objective criterion than wall thickness or color. In this view, L. crassa and L. jacutica have thick lanceolate folds, whereas L. minutissima and L. tenuissima have thin sinuous folds.

Size frequency distribution presents a second complication, because many leiosphaerid populations transgress the 70 µm boundary taken to separate species. For example, we measured the minimum diameter of specimens of different color (dark brown, medium brown, light brown) and fold morphology (broad lanceolate or thin sinuous folds) within the Roper assemblage and observed no size break around 70 µm in these different morphotypes (Figs. 3.1–3.7, 4.4–4.8). This difficulty has also been underlined by Porter and Riedman (2016) for Chuar Group populations. We suggest that species should be distinguished on the basis of modal rather than maximum diameter, so that Leiosphaeridia with lanceolate folds and a modal size <70 µm would be assigned to L. crassa, whereas populations with lanceolate folds and a modal size >70 µm would be placed in L. jacutica. This has the advantage of removing ambiguity in size frequency distributions while retaining the species distinctions used in many previous publications.

Figure 3 Size frequency distribution of leiospheres: (1) Size frequency distribution of all Leiosphaeridia crassa/jacutica (dark-, medium-, and light-brown walls); (2) Size frequency distribution of dark-brown Leiosphaeridia crassa/jacutica; (3) Size frequency distribution of medium-brown Leiosphaeridia crassa/jacutica; (4) Size frequency distribution of light-brown Leiosphaeridia crassa/jacutica; (5) Size frequency distribution of all Leiosphaeridia minutissima/tenuissima (medium- and light-brown walls); (6) Size frequency distribution of light-brown Leiosphaeridia minutissima/tenuissima; (7) Size frequency distribution of medium-brown Leiosphaeridia minutissima/tenuissima.

Figure 4 Photographs of Roper organic-walled microfossils (color figures are available in the online version of this paper): (1) cf. Gemmuloides doncooki. (2, 3) Leiosphaeridia atava. (4) Light-brown Leiosphaeridia crassa/jacutica. (5) Medium-brown Leiosphaeridia crassa/jacutica. (6) Dark-brown Leiosphaeridia crassa/jacutica. (7) Light-brown Leiosphaeridia minutissima/tenuissima. (8) Medium-brown Leiosphaeridia minutissima/tenuissima. (9) Leiosphaeridia ternata. (10–12) Leiosphaeridia sp., (11) showing details of wall texture of specimen in (10). Scale bar in (1) is: (1) 85 µm; (2) 12 µm; (3) 15 µm; (4) 14 µm; (5) 17 µm; (6) 10 µm; (7–8) 6 µm; (9) 90 µm; (10) 30 µm; (11) 60 µm; (12) 10 µm. Slides and England coordinates are (1) U6 230.8 m .2 L2Y/1; (2) U6 305.1 m.2A O26 ¾; (3) U6 305.1 m.2A U37/1; (4, 7) U6 230.8 m .2 H46/G46 (area); (5) U6 240.2 m .2 O34/3; (6) U6 305.1 m .2A T26/1; (8) U6 305.1 m .2A U20; (9) U5 125.1 m; (10, 11) U6 305.1 m 2A N20; (12) U6 230.8 m.2 S24/2.

Based on the presence of a multilayered recalcitrant wall, Roper leiospheres have been interpreted as eukaryotic (Javaux et al., Reference Javaux, Knoll and Walter2004). In the absence of supporting TEM analyses of wall ultrastructure, this attribution cannot be extended to all Proterozoic leiospheres; very likely the genus Leiosphaeridia is polyphyletic and their simple morphologies may record both prokaryotes and eukaryotes. Occasionally, medial split excystment structures have been observed in Roper specimens, suggesting that at least some of these fossils were resting cysts; however, even here, caution is advisable, because baeocyte-producing cyanobacterial cells can split in ways that resemble medial split excystment (Waterbury and Stanier, Reference Waterbury and Stanier1978, p. 13, fig. 4).

Leiospheres may occur as isolated specimens assigned to Leiosphaeridia, compact colonies called Synsphaeridium spp., or loose colonies named Symplassosphaeridium spp., possibly reflecting cyst and vegetative stages of the same population or life stages of different organisms. Single leiospheres might also be detached specimens from a colony (Hofmann and Jackson, Reference Hofmann and Jackson1994). The simple morphologies of leiospheres make it difficult to choose among these hypotheses, but more detailed analyses of wall ultrastructure and chemistry may provide the requisite tests (Javaux et al., Reference Javaux, Knoll and Walter2004; Javaux and Marshall, Reference Javaux and Marshall2006).

Leiosphaeridia atava (Naumova, Reference Naumova1960) Jankauskas, Mikhailova, and Hermann, Reference Jankauskas, Mikhailova and Hermann1989

Figure 4.2–4.3

1960 Megasacculina atava Reference NaumovaNaumova, pl. 3, fig. 15.

1989 Leiosphaeridia atava (Naumova, Reference Naumova1960); Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 74, pl. 10, figs. 4–7.

2016 Leiosphaeridia atava; Reference Sergeev, Knoll, Vorob’eva and SergeevaSergeev et al., fig. 4.5.

Holotype

Preparation 452/1, paleontological collection at the Institute of Precambrian Geology and Geochronology, St. Petersburg, Russia, upper Riphean (Tonian), Lakhanda Group, Neryuen Formation, Uchur-Maya region, Siberia. (The holotype was lost, as mentioned by Sergeev and Lee, Reference Sergeev and Lee2006).

Occurrence

The Mainoru Formation, Roper Group, Australia; the Lakhanda Group, Neryuen Formation, Uchur-Maya region, Siberia (Jankauskas, 1989); the Koltasy Formation, Russia (Sergeev et al., Reference Sergeev, Knoll, Vorob’eva and Sergeeva2016); the El Mreiti Group, Taoudeni Basin, Mauritania (Beghin et al., in Reference Beghin, Storme, Blanpied, Gueneli, Brocks, Poulton and Javauxreview).

Description

Spheroidal to oval vesicle with a fine granular, flexible wall, with numerous folds, 46 to 56 µm in diameter (N=4); two specimens with a dark, internal bleb of organic matter. No excystment structures observed.

Materials

Four specimens observed in sample U6 230.8 m from the Mainoru Formation.

Remarks

Leiosphaeridia atava differs from L. obsuleta by its diameter larger than 70 µm (Jankauskas, 1989).

Leiosphaeridia crassa (Naumauva, Reference Naumova1949), emend. Jankauskas in Jankauskas, Mikhailova, and Hermann, Reference Jankauskas, Mikhailova and Hermann1989

Figure 4.4–4.6

1949 Leiotriletes crassus Reference NaumovaNaumova, p. 54, pl. 1, figs. 5, 6; pl. 2, figs 5, 6.

1989 Leiosphaeridia crassa; Jankauskas in Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 75, pl. 9, figs. 5–10.

1989 Leiosphaeridia minutissima; Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 75, pl. 9, figs. 2, 3.

Holotype

No holotype was designated by Naumova (Reference Naumova1949), from the Lontova Formation, lower Cambrian, Estonia. A lectotype was designated by Jankauskas (in Jankauskas et al., Reference Jankauskas, Mikhailova and Hermann1989, p. 75) from Naumova (Reference Naumova1949, pl. 1, fig. 3), but this specimen was part of Leiotriletes simplicissimus, which is a species that Jankauskas et al. (Reference Jankauskas, Mikhailova and Hermann1989) synonymized with a different species of L. minutissima (Porter and Riedman, 2016).

Emended diagnosis

A species of Leiosphaeridia with smooth, pliant walls with lanceolate folds and a modal diameter of less than 70 µm.

Occurrence

Proterozoic and lower Paleozoic, worldwide.

Description

Smooth-walled leiospheres with large lanceolate folds (Fig. 3.1–3.4). Minimum diameter ranges from 5 to 390 µm (mean: 58.1±40.2 µm, N=669). No statistical differences among dark brown, medium, and light brown subpopulations, with mean diameters and standard deviations of, 54.5±21.6 µm (N=61), 55.3±30.7 µm (N=191 µm), and 56.0±27.7 µm (N=116). Excystment by partial rupture and medial split.

Materials

These are the most common microfossils in the Roper assemblage, especially in samples U6 305.1 m from the Mainoru Formation and U5 125.1 m from the Jalboi Member.

Remarks

As noted above, the rationale for emending the diagnosis of this species stems from the desire to focus on observed rather than inferred wall characters and to articulate size distinctions in a way that will minimize ambiguity in observed populations. The emended diagnosis considers the presence of lanceolate folds on a smooth wall as a diagnostic character as opposed to the wall color, which is not considered as a valid character.

Leiosphaeridia jacutica (Timofeev, Reference Timofeev1966), emend. Mikhailova and Jankauskas in Jankauskas, Mikhailova, and Hermann, Reference Jankauskas, Mikhailova and Hermann1989

Figure 4.4–4.6

1966 Kildinella jacutica Reference TimofeevTimofeev, p. 30, pl. 7, fig. 2.

1989 Leiosphaeridia jacutica (Timofeev, Reference Timofeev1966); Mikhailova and Jankauskas in Jankauskas et al., Reference Jankauskas, Mikhailova and Hermann1989, p. 77, pl. 9, fig. 12; pl. 12, figs. 3, 6, 7, 9.

Holotype

Preparation number 452/1, Biostratigraphy Laboratory, Maya River Collection, late Mesoproterozoic/early Neoproterozoic Lakhanda Group, Russia (Timofeev, Reference Timofeev1966, pl. 7, fig. 2).

Emended diagnosis

A species of Leiosphaeridia characterized by smooth, pliant walls with lanceolate folds and a modal diameter greater than 70 µm.

Occurrence

Proterozoic worldwide.

Description

A species of Leiosphaeridia characterized by smooth, pliant walls with lanceolate folds and a modal diameter greater than 70 µm. Excystment by partial rupture and medial split. While we cannot exclude the possibility that these represent a long right-hand tail of the L. crassa population, we suspect that, by comparison to other mid-Proterozoic assemblages, distinct populations of large leiosphaerids were present in the Roper seaway.

Materials

The Roper assemblage contains a relatively small proportion of very large, smooth walled leiosphaerids, in samples U6 305.1 m and 240.2 m from the Mainoru Formation and sample GG1 326.2 m from the Corcoran Formation.

Remarks

As noted above, the rationale for emending the diagnosis of this species stems from the desire to focus on observed rather than inferred wall characters and to articulate size distinctions in a way that will minimize ambiguity in observed populations. The emended diagnosis considers the presence of lanceolate folds on a smooth wall as a diagnostic character, as opposed to wall color, which is not considered as a valid character.

Leiosphaeridia minutissima (Naumova, Reference Naumova1949), emend. Jankauskas in Jankauskas, Mikhailova, and Hermann, Reference Jankauskas, Mikhailova and Hermann1989

Figure 4.7–4.8

1949 Leiotreletes minutissimus Reference NaumovaNaumova, p. 52, pl. 1, figs. 1, 2; pl. 2, figs. 1, 2.

1989 Leiosphaeridia minutissima (Naumova); Jankauskas in Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 79, pl. 9, figs. 1, 4, 11.

Lectotype

No holotype was designated by Naumova (Reference Naumova1949). Jankauskas (in Jankauskas et al., Reference Jankauskas, Mikhailova and Hermann1989, p. 80) designated a specimen of Leiotriletes minutissimus (pl. 1, fig. 1) from Naumova (Reference Naumova1949) as lectotype.

Emended diagnosis

A species of Leiosphaeridia characterized by smooth walls with sinuous folds and a modal diameter less than 70 µm.

Description

Smooth-wall spheromorphs with sinuous folds and a modal diameter less than 70 µm. Minimum diameter 21–117 µm (mean: 50.6±18.2 µm, N=216) (Figure 3.5–3.7). Light brown specimens 21–117 µm in minimum diameter (N=116, mean: 50.8±17.9 µm) and medium brown specimens 27–111 µm (N=47, mean: 49.6±19.1 µm). No dark brown specimens observed.

Occurrence

Proterozoic worldwide.

Materials

Common in inshore facies of the Roper Group, especially in samples U6 305.1 m, and U6 273.7 m from the Mainoru Formation.

Remarks

As noted above, the rationale for emending the diagnosis of this species stems from the desire to focus on observed rather than inferred wall characters and to articulate size distinctions in a way that will minimize ambiguity in observed populations. The emended diagnosis considers the presence of sinuous folds on a smooth, thin wall as a diagnostic character, as opposed to wall color, which is not considered as a valid character.

Leiosphaeridia tenuissima Eisenack, Reference Eisenack1958 emend.

Figure 4.7–4.8

1958 Leiosphaeridia tenuissima Reference EisenackEisenack, p. 391, pl. 1, figs. 2, 3.

1989 Leiosphaeridia tenuissima; Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 81, pl. 9, fig. 13.

Holotype

Preparation A3, 3 number 4 from the Dictyonema-shales of the lower Ordovician, St Petersburg area, Russia (Eisenack, Reference Eisenack1958, pl. 1, fig. 2).

Emended diagnosis

A species of Leiosphaeridia characterized by smooth walls with sinuous folds and a modal diameter (rather than maximum diameter) greater than 70 µm; the wall color is not a diagnostic criteria.

Description

Smooth wall spheromorphs with sinuous folds and a modal diameter greater than 70 µm. These may reflect a larger, uncommon population of Leiosphaeridia in Roper shales.

Occurrence

Proterozoic worldwide.

Materials

Uncommon specimens in samples U6 305.1 m and U6 230.8 m from the Mainoru Formation.

Remarks

As noted above, the rationale for emending the diagnosis of this species stems from the desire to focus on observed rather than inferred wall characters and to articulate size distinctions in a way that will minimize ambiguity in observed populations. The emended diagnosis considers the presence of sinuous folds on a smooth, thin wall as a diagnostic character as opposed to wall color, which is not considered as a valid character.

Leiosphaeridia ternata (Timofeev, Reference Timofeev1966), emend. Mikhailova and Jankauskas in Jankauskas et al., Reference Jankauskas, Mikhailova and Hermann1989

Figure 4.11

1966 Turuchanica ternata Reference TimofeevTimofeev, p. 45, pl. 9, fig. 8.

1989 Leiosphaeridia ternata (Timofeev); Mikhailova and Jankauskas in Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 81, pl. 11, figs. 2–4; pl. 12, figs. 4, 5, 8.

2016 Leiosphaeridia ternata; Reference Sergeev, Knoll, Vorob’eva and SergeevaSergeev et al., fig. 4.3, 4.4.

Holotype

Preparation 169/1, Biostratigraphical laboratory LAGED AN SSSR, Turukhansk collection, lower Tungunska, Turukhansk district; Miroedikhinsk series, Riphean (Mesoproterozoic and early Neoproterozoic boundary), rarely Ordovician (Timofeev, Reference Timofeev1966).

Occurrence

Found globally in worldwide Proterozoic successions.

Description

Compressed opaque spheromorph with thick, rigid walls commonly showing characteristic radial fractures. Diameter 15 to 110 µm.

Materials

A few specimens were observed in samples A82/3 157.5 m in the Jalboi Member, GG1 326.2 m in the Corcoran Formation, and U6 305.1 m in the Mainoru Formation.

Leiosphaeridia sp.

Figure 4.10–4.12

Description

Large medium to dark brown spheroidal to oval vesicles with a characteristic cork-like wall texture made of 5–11 µm, irregular patchy areas of different colors and fabric; this texture may well be taphonomic, but if so, it reflects original differences in wall composition, compared to other leiosphaerids. Concentric folds at the periphery. The minimum diameter of 19 spheroidal specimens is 56–455 µm (mean: 159.8±96.3 µm). Three oval specimens measured 75–210 µm wide and 160–330 µm long.

Materials

22 specimens in the Gibb Member, samples U6 305.1 m, U6 230.8 m of the Mainoru Formation, and in sample GG1 171.5 m of the Corcoran Formation.

Remarks

This species differs from another large leiosphere L. jacutica by its particular cork-like wall texture and a morphology that ranges from spheroidal to ovoidal. It also differs from Chuaria circularis, which has a thicker opaque, smooth wall. These specimens are left in open nomenclature until further characterization by SEM and TEM.

Genus Lineamorpha Vorob’eva, Sergeev, and Yu, Reference Vorob’eva, Sergeev and Yu2015

Type species

Lineamorpha elongata Vorob’eva, Sergeev, and Yu, Reference Vorob’eva, Sergeev and Yu2015, by monotypy.

Lineamorpha elongata Vorob’eva et al., Reference Vorob’eva, Sergeev and Yu2015

Figure 5.1–5.4

Figure 5 Photographs of Roper organic-walled microfossils: (1–4) Lineaforma lineata: (2) showing hollow extremity of specimen in (1), (3) specimen in situ in thin section. (5) Paleolyngbya catenata. (6–9) Satka favosa: (6) showing medial split and hollow interior, (8) showing hollow interior. (10) Siphonophycus kestron (bottom specimen) and S. typicum (top specimen). (11) Siphonophycus robustum. (12) Siphonophycus septatum. (13) Siphonophycus thulenema. (14) Squamosphaera colonialica. (15) Symplassophaeridium sp, (16–18) Synsphaeridium spp. Scale bar in (1) is: (1) 60 µm; (2) 100 µm; (3) 50 µm; (4) 110 µm; (5, 7) 15 µm; (6, 8) 20 µm; (9) 40 µm; (10, 13) 20 µm; (11, 12) 10 µm; (14) 50 µm; (15, 16) 33 µm; (17, 18) 15 µm. Slides and England coordinates are (1, 2) U5 125.1 m C13/3; (3) thin section 3785a R47/1; (4) A82/3 328.35 m.3 N41/4; (5) U5 130.5 ker E21; (6) U6 240.8 m .2 K23/3; (7) U6 305.1 m . E29; (8) U6 230.8 m.2 F14; (9) U6 230.8 m .2 J26/4; (10) U6 240.2 m .2 Z27/2; (11) U5 125.1 m .2 X48/4; (12) GG1 340.2 m.3 M13; (13) U6 240.2 m .2 Q18/3; (14) A82/3 328.35 m .3 K/L35; (15) A82/3 311.3 m .2 O5/2; (16) U5 125.1 m .2 R34/3; (17) A82/3 311.3 m .2 H40/4; (18) U5 151.3 m .2 Q/R29.

2004 “large striated tubes” Reference Javaux, Knoll and WalterJavaux et al., p. 126, fig 3 g–k.

2015 Lineamorpha elongata; Reference Vorob’eva, Sergeev and YuVorob’eva et al., p. 216, figs. 7 1–7.5.

2016 Lineamorpha elongata; Adam et al., fig. 9 A–D.

Holotype

Figure 7.4, Vorob’eva et al., Reference Vorob’eva, Sergeev and Yu2015, GINPC 14711-804, locality AK-14, Kotuikan River valley, Kotuikan Formation, Anabar Uplift, northern Siberia.

Occurrence

Early Mesoproterozoic, Jalboi, Crawford, and upper Mainoru formations, Roper Group, Australia; Belt Supergroup, Montana, US (Adam, Reference Adam2014); and Kotuikan Formation, northern Siberia (Vorob’eva et al., Reference Vorob’eva, Sergeev and Yu2015).

Description

Longitudinally striated hollow tubes (not a sheath around bundled filamentous sheaths) that often break into fragments, so maximum length is unknown but millimetric, 34 to 150 µm in diameter, fragment length: 131 to 473 µm (N=25).

Materials

562 specimens observed in maceration, in lower-shoreface to inner shelf facies of the Jalboi, Crawford, and upper Mainoru formations, Roper Group; one observed in thin section, 25 measured specimens. Abundant specimens observed in samples U5 125.1 m and U5 151.3 m of the Jalboi Member; in samples U5 334.3 m and U5 412.1 m of the Arnold sandstone Member; in samples A82/3 311 m of the Crawford Formation; and in samples U6 305.1 m, U6 230.8 m, and U6 240.2 m from the basal Mainoru Formation, but rare elsewhere.

Remarks

In the Roper population, there seems to be no relation between diameter and fragment length, nor dominant fragment length, suggesting random fragmentation of longer, probably millimetric, tubes. Light microscopy shows longitudinal, micron-scale striations along the tubes while SEM reveals a thick multilayered wall of densely packed granules, but no longitudinal striations. At the ultrastructural level (TEM), however, transverse sections of the wall show a clear alternation of electron-dense and electron-tenuous bands that correspond in size and distribution to the striations observed by light microscopy (Javaux et al., Reference Javaux, Knoll and Walter2004). The wall is ~1 μm thick, occasionally with an outer, electron-dense layer. The striations, thus, are not wall sculpture, but reflect original compositional heterogeneities in the tube wall, indicating complex physiological controls on wall formation.

The Roper material appears to be indistinguishable from the type of Lineaforma elongata from the lower Mesoproterozoic Kotuikan Formation, northern Siberia (Vorob’eva et al., Reference Vorob’eva, Sergeev and Yu2015). In the Roper Group, these filaments occur as transported fragments, contributing less than 3% to the entire assemblage, but up of 40% in lower-shoreface to inner-shelf shales. The rounded, closed tube ends observed in the Russian population were not observed in fragmental Roper specimens. The large size and complex wall ultrastructure of these microfossils suggest a eukaryotic affinity (Javaux et al., Reference Javaux, Knoll and Walter2004).

Genus Palaeolyngbya Schopf, Reference Schopf1968

Type species

Palaeolyngbya barghoorniana Schopf, Reference Schopf1968

Palaeolyngbya catenata Hermann, Reference Hermann1974

Figure 5.5

1974 Palaeolyngbya catenata Reference HermannHermann, p. 8, pl. 6, fig. 5.

1980 Oscillariopsis robusta; Reference Horodyski and DonaldsonHorodyski and Donaldson, p. 149, fig. 13H.

1994 Palaeolyngbya catenata; Butterfield et al., Reference Butterfield, Knoll and Swett1994, p. 61, fig. 25F–G.

Holotype

No holotype designated by Hermann, Reference Hermann1974, p. 8, 9, pl. 6, fig. 5, Tonian, Miroedikha Formation, Russia.

Description

Cellular trichome within a single encompassing sheath, cells 26 µm wide and 6 µm long.

Materials

One fragmented specimen with ripped sheath in sample U5 130.5 m from the Jalboi Member.

Genus Satka Jankauskas, Reference Jankauskas1979a

Type species

Satka favosa Jankauskas, Reference Jankauskas1979a

Satka favosa Jankauskas, Reference Jankauskas1979a

Figure 5.6–5.9

1979a Satka favosa Reference JankauskasJankauskas, pl. 4, fig. 2.

1980 “polygonally segmented sphaeromorphs” Reference HorodyskiHorodyski, p. 658, pl. 2, figs. 8–12.

1989 Satka favosa; Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 51, pl. 4, figs. 1, 2?

1989 Satka elongata; Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 51, pl. 4, figs. 3, 5.

1989 Satka granulosa; Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 51, pl. 4, fig. 8.

1994 Satka spp. Reference Hofmann and JacksonHofmann and Jackson, pl. 18, figs. 26–31.

2001 Satka favosa; Reference Javaux, Knoll and WalterJavaux et al., pl. 1e, f.

2003 Satka favosa; Reference Javaux, Knoll and WalterJavaux et al., figs. 1–10, 11.

2004 Satka favosa; Javaux et al., Reference Javaux, Knoll and Walter2004, p. 125, fig. 3a–f.

Holotype

Specimen pl. 4, fig. 2, preparation 16-1815-635, lower and middle Riphean (Mesoproterozoic) successions of the southern Urals, Russia (Jankauskas, 1989).

Description

Hollow oval spheromorph, 24 to 100 µm wide and 29 to 100 µm long (N=122), with walls made of tessellated 6 to 16 µm (minimum diameter) polygonal plates and with no external envelope. Excystment by medial split (Fig. 5.6).

Occurrence

Satka favosa, as described here, seems to be restricted to Mesoproterozoic rocks, including lower Mesoproterozoic shales of the Belt Supergoup (“polygonally segmented sphaeromorphs” of Horodyski, Reference Horodyski1980; Adam, Reference Adam2014), the Bylot Supergroup of the Canadadian Arctic (Hofmann and Jackson, Reference Hofmann and Jackson1994, as Satka spp., pl. 18, figs. 26–31), and lower and middle Riphean (Mesoproterozoic) successions of the southern Urals (Jankauskas et al., Reference Jankauskas, Mikhailova and Hermann1989).

Materials

Many specimens observed in shoreface facies of the Gibb Member, basal Mainoru Formation (samples U6 240.2 m, U6 273.7 m, U6 305.1 m), but rare elsewhere.

Remarks

The wall construction of S. favosa identifies it as a eukaryote, most likely the resting stage of some protist. Great confusion exists in the literature concerning Satka and its species. Jankauskas (1989) differentiated S. favosa from S. elongata (40–70 µm) by its smaller size and the characteristic shape of its inward-curving plates; S. colonialica (up to 150 µm) was segregated because of its simpler regular shape and better-defined plates; and S. granulosa (40–50 µm wide to 75–125 µm long) was differentiated by its smaller size and granular appearance (linked to the presence of internal bodies). The specimens illustrated by Jankauskas (1989) as Satka elongata (pl. 4, figs. 3, 5) and Satka granulosa (pl. 4, fig. 8) also resemble Satka favosa as described here. Satka squamifera is described as having rounded plates and an external envelope. From our observations, however, the “plates” of S. squamifera represent the imprints of spheroidal cells on an encompassing envelope; therefore, we interpret this population as a colonial microorganism, perhaps cyanobacterial, which is unlikely to be linked to S. favosa at the domain level, and recently placed within the new genus Squamosphaera (Tang et al., Reference Tang, Pang, Yuan, Wan and Xiao2015).

Genus Siphonophycus Schopf, Reference Schopf1968, emend. Knoll, Swett, and Mark, Reference Knoll, Swett and Mark1991

Type species

Siphonophycus kestron Schopf (Reference Schopf1968).

Occurrence

Widespread in Proterozoic assemblages, common throughout the Roper Group.

Description

Fragments of smooth, non-septate tubes, commonly interpreted as the sheaths of oscillatorialean cyanobacteria.

Remarks

Different species are distinguished on the basis of cross-sectional diameter (revision in Butterfield et al., Reference Butterfield, Knoll and Swett1994): S. thulenema: 0.5 µm; S. septatum: 1–2 µm; S. robustum: 2–4 µm; S. typicum: 4–8 µm; S. kestron: 8–16 µm; and S. solidum: 16–32 µm. Five species occur in Roper shales: S. kestron, S. robustum, S. septatum and S. typicum occur as transported fragments; and S. thulenema forms small balls of thin filamentous sheaths. Siphonophycus spp. are commonly interpreted as the sheaths of oscillatorialean cyanobacteria.

Siphonophycus kestron Schopf, Reference Schopf1968

Figure 5.10

1968 Siphonophycus kestron Reference SchopfSchopf, p. 671, pl. 80, figs. 1–3.

1971 Siphonophycus kestron; Reference Schopf and BlacicSchopf and Blacic, pl. 109, figs. 3, 4.

1992 Siphonophycus kestron; Reference SergeevSergeev, p. 95, pl. 16, figs. 8, 9.

1992 Siphonophycus kestron; Reference SchopfSchopf, pl. 31, fig. J.

1994 Siphonophycus kestron; Reference Butterfield, Knoll and SwettButterfield et al., fig. 21D.

2001 Siphonophycus kestron; Reference Sergeev and LeeSergeev and Lee, p. 8, pl. 1, fig. 1.

2006 Siphonophycus kestron; Reference Sergeev and LeeSergeev and Lee, pl. 1, fig. 10.

2006 Siphonophycus kestron; Reference SergeevSergeev, p. 214, pl. 22, figs. 1, 2; pl. 28, fig. 3; pl. 36, fig. 3; pl. 44, fig. 11; pl. 45, figs. 3, 6.

Holotype

Specimen pl. 80, fig. 1 (Schopf, Reference Schopf1968), thin section Bit. Spr. 6-3, Paleobotanical Collections, Harvard University number 58469, from Neoproterozoic Bitter Springs Formation, Amadeus Basin, Australia.

Description

Fragments of smooth, non-septate tubes, 8–16 µm in diameter, most specimens 8–9 µm, a few up to 16 µm.

Materials

Dozens of filamentous sheaths, abundant in samples GG1 340.2 m of the Corcoran Formation, a few in sample GG1 48.75 m from the Velkerri Formation.

Siphonophycus robustum (Schopf, Reference Schopf1968) Knoll, Swett, and Mark, Reference Knoll, Swett and Mark1991

Figure 5.11

1968 Eomycetopsis robusta Reference SchopfSchopf, p. 685, pl. 82, figs. 2–3; pl. 83, figs. 1–4.

1991 Siphonophycus robustum; Knoll et al., p. 565, fig. 10.3, 10.5.

1994 Siphonophycus robustum; Reference Butterfield, Knoll and SwettButterfield et al., p. 64, figs. 26A, G.

Holotype

Specimen pl. 83, fig. 1 (Schopf, Reference Schopf1968), thin section Bit. Spr. 10-1, Paleobotanical Collections, Harvard University number 58491 from Neoproterozoic Bitter Springs Formation, Amadeus Basin, Australia.

Description

Smooth filamentous sheaths 2–4 μm in diameter, most specimens 2–3 µm in diameter.

Materials

Dozens of specimens, most abundant in sample GG1 340.2 m of the Corcoran Formation and sample U6 240.6 m of the Mainoru Formation.

Siphonophycus septatum (Schopf, Reference Schopf1968) Knoll, Swett, and Mark, Reference Knoll, Swett and Mark1991

Figure 5.12

1968 Tenuofilum septatum Reference SchopfSchopf, p. 679, pl. 86, figs. 10–12.

1991 Siphonophycus septatum; Knoll et al., p. 565, fig. 10.2.

Holotype

Specimen pl. 86, fig. 11 (Schopf, Reference Schopf1968), thin section Bit/Spr 6–3, Paleobotanical collections, Harvard University, number 58527 from the Neoproterozoic Bitter Springs Formation, Amadeus Basin, Australia.

Description

Fragments of smooth, non-septate tubes, 1–2 µm in diameter. Common, as transported fragments.

Materials

Common in the Roper Group, abundant in sample U5 508.6 m of the Mainoru Formation.

Siphonophycus thulenema Butterfield, Knoll, and Swett, Reference Butterfield, Knoll and Swett1994

Figure 5.13

1994 Siphonophycus thulenema Butterfield et al., fig. 22I.

Siphonophycus thulenema Butterfield, Knoll, and Swett, Reference Butterfield, Knoll and Swett1994, fig. 22I

Holotype

HUPC 62718, fig. 22I, slide 86-G-62-46, R-28-3, Algal Dolomite Member, Svanbergfjellet Foramtion, Geerabukta (79°35'30''N, 17°44''E), 55 m above base of member.

Description

Fragments of thin, smooth, non-septate tubes, 0.5 µm in diameter, forming small balls of enrolled filamentous sheaths.

Materials

Rare, in sample U5 125.1 m of the Jalboi Member.

Siphonophycus typicum (Hermann, Reference Hermann1974), Butterfield, Knoll, and Swett, Reference Butterfield, Knoll and Swett1994

Fig. 5.10

1974 Leiothrichoides tipicus Reference HermannHermann, p. 7, pl. 6, figs. 1–2.

1994 Siphonophycus typicum; Reference Butterfield, Knoll and SwettButterfield et al., p. 66, figs. 23B–D, 26B, H, I.

Holotype

Specimen pl. 6, figs. 1, 2 (Hermann, Reference Hermann1974), preparation number 49/2T, Neoproterozoic Miroyedikha Formation, Krasnoyarsk Krai in Turukhansk region, near Maya River, Siberia.

Description

Fragments of thin smooth, non-septate tubes, 4–8 µm in diameter.

Materials

Common; most abundant in samples U5 508.6 m of the Mainoru Formation, GG1 46.75 m of the Velkerri Formation and GG1 340.2 m of the Corcoran Formation.

Genus Squamosphaera Tang et al., Reference Tang, Pang, Yuan, Wan and Xiao2015

Type species

Squamosphaera colonialica (Jankauskas, Reference Jankauskas1979b) Tang et al., Reference Tang, Pang, Yuan, Wan and Xiao2015 by monotypy

Squamosphaera colonialica (Jankauskas, Reference Jankauskas1979b) Tang et al., Reference Tang, Pang, Yuan, Wan and Xiao2015

Figure 5.14

1979b Satka colonialica Reference JankauskasJankauskas, p. 192, pl. 1, figs. 4, 6.

1985 Satka colonialica; Reference Knoll and SwettKnoll and Swett, p. 468, pl. 53, figs. 4–6, 8.

1989 Satka colonialica; Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 51, pl. 4, figs. 4, 7.

1989 Satka squamifera; Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 52, pl. 4, fig. 10; pl. 5, fig.1–8

1997 Satka colonialica; Reference SamuelssonSamuelsson, p. 175, fig. 9A, B.

1999 Satka colonialica; Reference CotterCotter, p. 77, fig. 7C.

1999 Satka colonialica; Reference Samuelsson, Dawes and VidalSamuelsson et al., fig. 4G.

2015 Squamosphaera colonialica; Tang et al., Reference Tang, Pang, Yuan, Wan and Xiao2015, p. 312, fig. 12 A–C2, fig. 13 A–F2

in press Squamosphaera colonialica; Reference Porter and RiedmannPorter and Riedman, fig. 17, 1–7. [See for complete synonymy]

Holotype

Number 16-62-4762/22, slide 1. Well Kabakovo-62, 4762-4765 m. Neoproterozoic Zigazino-Komarovo Formation, Ufa, Bashkirian Urals (Jankauskas, 1979, fig. 4).

Description

Single-walled, spheroidal, tomaculate, or irregularly shaped vesicles with irregular outline characterized by numerous broadly domical bulges. Vesicles 29–166 µm wide and 66–184 µm long (N=37); individual bulges 11 to 14 µm in diameter.

Materials

Many specimens were observed in all facies except the most basinal and are particularly abundant in the lower-shoreface to storm-dominated shelf facies of the Jalboi Member and Crawford Formation (samples A82/3 311 m, A82/3 166 m, U5 125.1 m, U5 151.3 m, U5 334.3 m, U5 412.1 m).

Remarks

The Roper population closely matches the emended diagnosis provided by Porter and Riedman (in Reference Porter and Riedmannpress). Populations assigned here to the genus Squamosphaera were originally classified as a species of the genus Satka (Jankauskas, Reference Jankauskas1979b). As discussed above, the type species of Satka, S. favosa, is characterized by a wall of tessellated plates, which is far different from the vesicles observed in S. colonialica. The two species should not be placed in the same genus and doubtfully belong to the same domain. Tang et al. (Reference Tang, Pang, Yuan, Wan and Xiao2015) gave formal recognition to this by segregating populations of Satka colonialica into the new genus. Tang et al.’s (Reference Tang, Pang, Yuan, Wan and Xiao2015) diagnosis and description suggest that Squamosphaera was a cyst wall ornamented by broadly domical processes, but this conflicts with the irregular morphology of individual vesicles, both within Tang et al.’s (Reference Tang, Pang, Yuan, Wan and Xiao2015) illustrated materials and populations observed elsewhere. For this reason, Porter and Riedman (in Reference Porter and Riedmannpress) emended the diagnosis of Squamosphaera, identifying the domical surface features simply as bulges. Roper populations closely resemble those from the Chuar Group, and we interpret them as enveloped marked by imprints of internal cells no longer present.

Hofmann and Jackson (Reference Hofmann and Jackson1994, p. 28) described Satka colonialica from the Bylot Supergroup, the Canadadian Arctic, as a colony of packaged cells in “distinct belt-like rows transverse to the long axis of the colony,” with a smooth surface and distinct curvilinear folds. They further suggested that S. squamifera, S. granulosa, and S. elongata might be taphonomic variants of the same taxon, and mentioned S. elongata Jankauskas, 1989 as the senior synonym to which other species should be referred. Satka favosa, however, is actually the senior species of the genus Satka (Jankauskas, Reference Jankauskas1979b). Hofmann and Jackson (Reference Hofmann and Jackson1994) also include in their suggestion of synonymy a Bylot population referred to Satka spp. that we interpret as S. favosa (see above). Several types of coccoidal cyanobacteria (Chroococcales and Pleurocapsales) and green algae (such as Pandorina) can produce colonies of packed spheroidal cells embedded in an envelope of amorphous mucilage matrix. Less commonly, the individual cells have a single wall rather than a multilamellate envelope, are closely packed, and the colony is surrounded in a structurally defined envelope, such as in modern cyanobacteria that produce baeocytes (endospores) within a parental wall (Chroococcidiopsis and Staniera/Dermocarpa). Squamosphaera colonialica resembles these pleurocapsalean cyanobacteria, with the internal cells not preserved, only their imprints on the wall. Squamosphaera differs from Synsphaeridium spp., which are colonies without an envelope.

Genus Symplassosphaeridium Timofeev, Reference Timofeev1959

Symplassosphaeridium sp.

Figure 5.15

Description

Aggregates of loosely packed, smooth-walled vesicles of variable size, but with similar morphology and size within a colony. Differs from Synsphaeridum by the loose packing of vesicles.

Materials

Dozens of colonies observed.

Genus Synsphaeridium Eisenack, Reference Eisenack1965

Type species

Synsphaeridium gotlandicum Eisenack, Reference Eisenack1965.

Synsphaeridium sp.

Figure 5.16–5.18

Occurrence

Widespread in Proterozoic and Phanerozoic rocks.

Description

Aggregates of contiguous smooth-walled vesicles, sometimes with internal inclusions, without envelope. Vesicles are similar in morphology and size within a colony. Colonies have variable size, from broadly spherical to elongated and irregular. Cell diameter ranges from 4 to 40 µm, and colonies can be up to 180 µm or more in diameter.

Materials

Dozens of colonies observed, especially in samples GG1 326.2 m, in the Corcoran Formation and in samples U5 125.1 m and U5 151.3 m of the Jalboi Member.

Genus Tappania Yin, Reference Yin1997

Type species

Tappania plana Yin, Reference Yin1997.

Other species

Tappania tubata Yin, Reference Yin1997; Tappania gangaei Prasad and Asher, Reference Prasad and Asher2001.

Tappania plana Yin, Reference Yin1997

Figure 6.1–6.15

Figure 6 Photographs of Roper organic-walled microfossils: (1–15) Tappania plana: arrow in (1) showing furcating process, arrows in (2–4) showing septae in processes, (3) showing details from specimen in (2), arrow in (11) showing the area of locally grouped small processes shown in (12), arrow in (15) shows open neck-like expansion, suggesting excystment structure. (16) Tortunema sp. (17, 18) Trachytrichoides sp.: (18) showing details of cells morphology in filaments in (17). Scale bar in (1) is: (1, 2) 40 µm; (3, 11) 10 µm; (4, 8, 14) 20 µm; (5, 9, 16, 17) 30 µm; (6, 10, 12, 15, 18) 15 µm; (7) 27 µm; (13) 25 µm. Slide and England finder coordinates: (1) GG1 340.2 m .3 B X36/2, (2, 3) GG1 340.2 m .2 A J47/2, (4) GG1 340.2 m .3B T40/2, (5) GG1 340.2 m .2A E28/4, (6) U5 151.3 m .2 Q28/3, (7) GG1 326.2 m .2 V33/1, (8) U5 151.3 m .2 Y14/2, (9) GG1 340.2 m .3 H26/2, (10) GG1 326.2 m .3 F39/1, (11, 12) GG1 340.2 m .2 E17/1, (13) GG1 326.2 m .2 Y28/4, (14) GG1 340.2 m .3 O19/1, (15) U5 130.5 m .2 U9, (16) A82/3 379.1M G57/0, and (17) U6 240.2 m .2B J34/1.

1997 Tappania plana Reference YinYin, p. 23, pl. 1, figs. 4, 6, 7.

1997 Tappania tubata Reference YinYin, p. 23, 24, pl. 2, figs. 1, 3, 4, 6.

1997 Tappania plana; Reference Xiao, Knoll, Kaufman, Yin and ZhangXiao et al., p. 205, fig. 3c.

2001 Tappania plana; Reference Prasad and AsherPrasad and Asher, p. 73, pl. 2, figs. 1–3, 9; pl. 3, figs. 1–6.

2001 Tappania tubata; Reference Prasad and AsherPrasad and Asher, p. 74, pl. 2, figs. 4–7.

2001 Tappania gangaei; Reference Prasad and AsherPrasad and Asher, p. 74, pl. 2, figs. 8, 10.

2001 Tappania plana; Reference Javaux, Knoll and WalterJavaux et al., pl. 1a–c.

2004 Tappania plana; Reference Javaux, Knoll and WalterJavaux et al., p. 124, fig. 2a–e.

2009 Tappania plana; Reference NagovitsinNagovitsin, fig. 2 a–e.

Holotype

Sample and slide M 9208-1, L4/37, Shuiyou section, southern Shanxi, North China; lower shales of Beidajian Formation of the Ruyang Group (Meso-Neoproterozoic) (Yin, Reference Yin1997, pl. 1, fig. 7).

Description

Size 15 to 158 µm (N=48), irregularly spheroidal vesicle bearing zero to 21 tubular, heteromorphic, sometimes branching, sometimes septate processes with closed relatively dark, rounded ends; zero to four neck-like expansions; zero to three bulbous protrusions. Process length up to 8 µm; bulbous expansions 2 µm wide; neck up to 2 µm high and 2 µm wide; two specimens show septate processes (Fig. 6.2–6.4), two others with branching processes. One specimen with a neck-like expansion shows a concentration of small (~8 µm long) processes with dark ends in one area of the vesicle surface, and another has small (3–5 µm long), hair-like spines, which are probably developing processes (not shown). The vesicle occasionally includes a dark cytoplasmic remnant. Specimens may bear only broad neck-like extensions (Fig. 6.6, 6.7, 6.10), or only processes (zero to 21) (Fig. 6.2, 6.5, 6.9, 6.13), or both. Neck-like extensions usually have a dark rim. In one specimen without processes, this trapezoidal extension is open, possibly indicating excystment (Fig. 6.15). Some specimens also show bulbous expansions suggestive of division by budding (Fig. 6.1); buds have semi-circular to oval convex morphology, whereas neck-like expansions have a trapezoidal shape, with side walls flaring outward and a convex end.

Occurrence

Tappania plana seems to be restricted to uppermost Paleoproterozoic and Mesoproterozoic rocks, including, in addition to the Roper Group, Australia (Javaux et al., Reference Javaux, Knoll and Walter2001); the Ruyang Group, China (Xiao et al., Reference Xiao, Knoll, Kaufman, Yin and Zhang1997; Yin, Reference Yin1997); the Bahraich and Kheinjua groups, India (Prasad and Asher, Reference Prasad and Asher2001; Prasad et al., Reference Prasad, Uniyal and Asher2005); the Kamo Group of Siberia (Nagovitsin Reference Nagovitsin2009; Nagovitsin et al., Reference Nagovitsin, Stanevich and Kornilova2010); and the Lower Belt Group, USA (Adam, Reference Adam2014).

Materials

48 specimens measured in samples, U5 151.3 m and U5 130.5 m from the Jalboi Formation (proximal shelf facies), and from GG1 340.2 m and GG1 326.2 m from the Corcoran Formation (TST, distal shelf facies).

Remarks

We observed a wide range of morphologies within Tappania, ranging from specimens with only broad, neck-like extensions, or only processes, to individuals with both broad, neck-like extensions and processes. On one fragmented specimen bearing a neck-like expansion, very small processes with dark, rounded closed ends are locally grouped on the vesicle wall. This is the first time this morphology has been reported in Tappania plana, however a single fragmented specimen and the large variability of the species precludes the creation of a new species at this time. Rare specimens show processes with septa, suggesting Tappania was multicellular. Ultrastructural analyses show a unilayered homogenous wall (Javaux et al., Reference Javaux, Knoll and Walter2004). The Roper population shows division by budding, and possible excystment through the opening of a neck-like extension. Specimens from the Kotuikan Formation illustrated by Nagovitsin (Reference Nagovitsin2009) suggest that Tappania could also reproduce by a simple binary division of the vesicle.

Yin (Reference Yin1997) described a second species of Tappania, T. tubata, that co-occurs with T. plana and has a broad tube-like extension but not trapezoidal neck-like extension, with a fimbriate distal margin and a few small processes on its extension surface. The Roper Tappania population displays the range of morphological characters originally ascribed to T. plana and T. tubata, occasionally on a single specimen. Therefore, we consider T. tubata to be a synonym of the senior species, Tappania plana. Prasad and Asher (Reference Prasad and Asher2001) described a third species, Tappania gangaei, based on the rounded bulbous extension, rather than trapezoidal or tube-like. However, in the Roper population, specimens may bear both neck-like and rounded extension (interpreted as budding structures), therefore here too, we consider T. plana as the senior synonym.

Vesicles bearing neck-like expansions but no processes are reported as cf. Tappania? in the late Mesoproterozoic–early Neoproterozoic Mbuyi-Mayi Supergroup, RDC (Baludikay et al., Reference Baludikay, Storme, François, Baudet and Javaux2016). However, the absence of processes on any of the six specimens observed so far and the younger age of these fossils leaves this occurrence ambiguous, even though Tappania populations elsewhere also include similar morphologies without processes. Indeed, so far, Tappania plana seems to be restricted to uppermost Paleoproterozoic to Mesoproterozoic rocks. Butterfield (Reference Butterfield2005a) described specimens from the mid-Neoproterozoic Wynniatt Formation, the Canadian arctic as Tappania, but these show a complex pattern of septation, peripheral branching and anastomosis not found in Mesoproterozoic populations and lack the neck-like expansions or the closed and rounded process terminations characteristic of older fossils. Therefore, the Neoproterozoic population might usefully be placed into a separate genus.

Genus Tortunema Hermann, 1976

Type species

Tortunema wernadskii (Schepeleva, Reference Schepeleva1960) Butterfield et al., Reference Butterfield, Knoll and Swett1994.

Tortunema sp.

Figure 6.16

Description

Fragmental remains of compressed cylindrical sheaths, 250–300 µm long and 30 µm wide (N=2), marked by thin, regularly spaced, transverse annulations that record cell boundaries of originally ensheathed trichomes. Spacing of prominent annulations 6 µm, commonly with less-pronounced annulations between them.

Materials

Two specimens.

Discussion

Pseudoseptate filaments, widely distributed in Proterozoic platform and inner-shelf shales, are generally interpreted as the empty sheaths of cyanobacteria (e.g., Jankauskas, 1989; Butterfield et al., Reference Butterfield, Knoll and Swett1994). These sheaths are larger than the type species of the genus, T. wernadskii (Schepeleva) Butterfield. Because they are rare, we have little sense of their size frequency distribution, so only identify them as Tortunema sp.

Genus Trachytrichoides Hermann in Timofeev, Hermann, and Mikhailova, Reference Timofeev, Hermann and Mikhailova1976

Type species

Trachytrichoides ovalis Hermann in Timofeev et al., Reference Timofeev, Hermann and Mikhailova1976.

Trachytrichoides sp.

Figure 6.17–6.18

Description

Multicellular filaments with ovoid cells and thick intercellular septa, no external sheath, 157 µm long and 5 µm wide (N=3), with individual ellipsoidal cells 5 µm wide x 6 µm long.

Materials

Three filaments observed in sample U6 240.2 m of the Mainoru Formation.

Remarks

A rare component of the Roper Group, differs from other filamentous taxa by the oval shape of the cells and absence of ellipsoidal fold between the cells (as in Arctacellularia), and from the type species T. ovalis by the smaller cell size than those of the holotype (25–35 µm wide and 30–60 µm long).

Genus Valeria Jankauskas, Reference Jankauskas1982, emend. Nagovitsin, Reference Nagovitsin2009

Type species

Valeria lophostriata (Jankauskas, Reference Jankauskas1979b) Jankauskas, Reference Jankauskas1982.

Valeria lophostriata (Jankauskas, Reference Jankauskas1979b) Jakauskas, Reference Jankauskas1982

Figure 7.1–7.4

Figure 7 Photographs of Roper organic-walled microfossils: (1–4) Valeria lophostriata: (1) showing half enrolled vesicle following medial split, (2) showing start of medial split, (3, 4) showing wall ornamentation by characteristic concentric striations. (5, 6) Unnamed form A, large compartmentalized colonial forms. (7, 8) Unnamed form B, opaque spheromorph, (8) showing details of folds at periphery. (9) Unnamed form C, spheromorphs connected by a filamentous expansion. (10) Unnamed form D, spheromorph with a filamentous expansion. (11) Unnamed form E, large smooth thick brittle spheromorph. (12) Unnamed form F, large filament in indented sheath. Scale bar in (1) is: (1) 100 µm, (2, 4, 8) 25 µm, (3) 10 µm, (5) 70 µm, (6) 120 µm, (7) 45 µm, (9) 18 µm, (10, 15) 30 µm, (11) 80 µm, and (12) 55 µm. Slide and England finder coordinates: (1) U6 305.1 m .2A S41, (2) U6 230.8 m .2 N27/2, (4) U6 233.6 B45/0, (5) U6 305.1 m .2A O/N39, (6) U6 305.1 m B45/1, (7) GG1 340.2 m .3B U30, (9) U5 125.1 m .2 M41/3, (10) GG1 326.2 m .2 E20/1, (11) U6 240.2 m .2U27/2, (12) U5 436.7 m .2 S51.

1979b Kildinella lophostriata Reference JankauskasJankauskas, p. 153, fig. 1.13–1.15.

1982 Valeria lophostriata; Reference JankauskasJankauskas, p. 109, pl. 39, fig. 2.

1983 Kildinosphaera lophostriata; Reference Vidal and SiedleckaVidal and Siedlecka, p. 59, fig. 6A–G.

1985 Kildinosphaera lophostriata; Reference Vidal and FordVidal and Ford, p. 361, fig. 4C, E–F.

1989 Valeria lophostriata; Reference Jankauskas, Mikhailova and HermannJankauskas et al., p. 86, pl. 16, figs. 1–5. [See for additional synonymy]

1994 Valeria lophostriata; Hofmann and Jackson, Reference Hofmann and Jackson1994, p. 24, pl. 17, figs. 14–15; pl. 19, fig. 4.

1997 Valeria lophostriata: Reference Xiao, Knoll, Kaufman, Yin and ZhangXiao et al., p. 201, fig. 3e.

1999 Valeria lophostriata; Reference Samuelsson, Dawes and VidalSamuelsson et al., p. 15, fig. 8E.

2001 Valeria lophostriata; Reference Javaux, Knoll and WalterJavaux et al., fig. 1D.

2004 Valeria lophostriata; Reference Javaux, Knoll and WalterJavaux et al., fig. 2F–I.

2009 Valeria lophostriata; Reference Nagy, Porter, Dehler and ShenNagy et al., fig. 1A, B.

2009 Valeria lophostriata; Reference NagovitsinNagovitsin, p. 144, fig. 4E.

2009 ovoidal acritarch with striated ornamentation Reference Peng, Bao and YuanPeng et al., fig. 4.

2009 ovoidal acriatrch with striated ornamentation Reference Lamb, Awramik, Chapman and ZhuLamb et al., fig. 4 A.

?2012 “dark walled megasphaeric coccoid with a subradial striation” Reference Battison and BrasierBattison and Brasier, fig. 8B.

2015 Valeria lophostriata; Reference Tang, Pang, Yuan, Wan and XiaoTang et al., p. 315, fig. 11.

in press Valeria lophostriata; Reference Riedman and PorterRiedman and Porter, p. 10, fig. 4.1.

in press Valeria lophostriata; Reference Porter and RiedmannPorter and Riedman, fig. 19.1–19.3.

(For additional synonymy see Jankauskas et al., Reference Jankauskas, Mikhailova and Hermann1989, and Hofmann and Jackson, Reference Hofmann and Jackson1994)

Holotype

Number 16-62-4762/16, sp. 1, DH Kabakovo 62 drill core, depth 4762 to 4765 meters, Neoproterozoic Zigazino-Komarovo Formation, southern Urals (Jankauskas, Reference Jankauskas1979b, fig. 1.14).

Description

Large vesicle, 104–160 µm in minimum diameter, with lanceolate folds and a distinctive ornamentation of concentric ridges, giving the appearance of a “target” (Fig. 7.3, 7.4).

Occurrence

This taxon is found worldwide (Hofmann, Reference Hofmann1999) from the late Paleoproterozoic Era (Javaux et al., 2004; Lamb et al., Reference Lamb, Awramik, Chapman and Zhu2009; Peng et al., Reference Peng, Bao and Yuan2009) to the Cryogenian (Nagy et al., Reference Nagy, Porter, Dehler and Shen2009).

Materials

Several specimens observed, mostly in samples U6 305.1 m, U6 273.7 m, and U6 240.2 m from the Mainoru Formation.

Remarks

SEM analyses show that the striations are 1-µm ridges located on the inside of the vesicle wall (Javaux et al., Reference Javaux, Knoll and Walter2004). Excystment by medial split gives rise to two half vesicles that commonly enroll onto themselves (Fig. 7.1, 7.2).

Unnamed form A

Figure 7.5–7.6

Description

A large ovoidal or irregular and globular envelope including several contiguous compartments, each surrounded by an envelope and containing closely packed spheroidal cells. Two fragmented specimens are 350 µm wide and 600–700 µm long, internal compartments surrounded by an inner envelope 39–85 µm in diameter, containing poorly defined, closely packed cells. The external envelope is 8–13 µm thick.

Materials

Two specimens in sample U6 305.1 m from the Mainoru Formation.

Unnamed form B

Figure 7.7–7.8

Description

Black opaque vesicles, 141 and 215 µm in diameter (N=2), with medial split and folds at periphery.

Materials

Two specimens in sample GG1 340.2 m from the Corcoran Formation.

Remarks

These vesicles differ from Chuaria circularis by the translucent margin showing folds.

Unnamed form C

Figure 7.9

Description

Vesicles with smooth to chagrinate walls, 30 and 35 m in diameter (N=2), connected by a 14-µm-long filamentous expansion.

Materials

Two vesicles in sample U5 125.1 m from the Jalboi Member.

Unnamed form D

Figure 7.10

Description

Vesicle 40 µm in diameter, attached to a large 80 µm filamentous expansion, but not communicating with the cell interior (thus distinct from Germinosphaera).

Materials

One specimen in sample GG1 326.2 m from the Corcoran Formation.

Unnamed form E

Figure 7.11

Description

Large, smooth-walled, thick, brittle, brown-orange wall fragment of a spheromorph, 310 µm in diameter.

Materials

One specimen in sample U6 240.2 m from the Mainoru Formation.

Unnamed form F

Figure 7.12

Description

Large, 16 to 29 µm wide filament in a 72 µm x 171 µm smooth indented sheath.

Materials

A single specimen in sample U5 437 m from the Mainoru Formation (Showell Creek Member).

Remarks

This large filamentous fossil differs from other sheathed filamentous taxa by the indentation of the sheath and absence of septae in the filament, although these characters could be taphonomic. Other taxa, such as Rugosoopsis, can reach large diameters, but have a distinct transverse fabric not observed here. Palaeolyngbya may also have a wide sheath, but is characterized by regular uniseriate array of well-preserved cells (Butterfield et al., 1994).

Discussion

Paleoecology: the distribution of Roper fossils in space.—Abbott and Sweet (Reference Abbott and Sweet2000) interpreted Roper sequence stratigraphy in terms of four facies groups: (1) paralic to fluviatile redbeds characterized by heterolithic, iron-rich sandstones along with finer siliciclastics and oolitic ironstone, dessication cracks and paleosols; (2) tide-dominated shoreline sandstones dominated by trough cross-bedded quartz arenite; (3) shore-face to storm-dominated shelf deposits with alternating rippled and cross-bedded quartz arenites and laminated siltites and shales; and (4) basinal facies consisting of thinly laminated shales deposited below storm wave base. In a preliminary study, Javaux et al. (Reference Javaux, Knoll and Walter2001) suggested that Roper diversity peaked in coastal facies, and analysis of the entire sample suite confirms this view. Microfossils do not occur in tidal sandstones and ironstones, but are abundant in shaley intervals of shoreface and proximal shelf successions. Indeed, diversity is highest in shallow shelf environments characterized by interbedded shales and cross-bedded sandstones, with individual taxa peaking in abundance at different points along the shelf gradient (Fig. 8).

Figure 8 Paleoecological distribution of selected microfossils in the Roper Group.

Eukaryotes and probable eukaryotes are least abundant and diverse in basinal shales throughout the Roper succession, the exception being Blastanosphaira kokkoda, which locally forms a monospecific assemblage in basinal shales, and rare Dictyosphaera. It has long been apparent empirically that quality of microfossil preservation varies inversely with total organic content (Butterfield et al., Reference Butterfield, Knoll and Swett1994). Therefore the limited presence of eukaryotes in basinal shales could reflect, in part, the high organic content of many basinal samples. That noted, even where basinal shales contain reasonably preserved microfossils, diversity is low. Bitumens occur throughout the Roper Group, in part the result of migration from source beds in the Velkerri Formation (Jackson and Raiswell, Reference Jackson and Raiswell1991; Dutkiewicz et al., Reference Dutkiewicz, Volk, Ridley and George2003). Biomarker analysis of carbonaceous shales in the underlying McArthur Group suggests strong dominance of open water primary production by bacteria, including anoxygenic photosynthetic bacteria that inhabited anoxic waters within the photic zone (Brocks et al., Reference Brocks, Love, Summons, Knoll, Logan and Bowden2005).

Biostratigraphy: the distribution of Roper fossils in time

Early work in Russia established a broad biostratigraphic framework for organic-walled microfossils in Proterozoic shales, with Satka favosa characterizing early Mesoproterozoic samples and Valeria lophostriata more common in Neoproterozoic successions (summaries in Jankauskas et al., Reference Jankauskas, Mikhailova and Hermann1989; Sergeev et al., Reference Sergeev, Semikhatov, Fedonkin and Vorob’eva2010). More recent research shows that both of these morphospecies co-occur with Tappania plana and other Roper taxa in the Kamo Group, Siberia, and in correlative shales of the Debengda Formation (Nagovitsin, Reference Nagovitsin2009; Stanevich et al., Reference Stanevich, Maksimova, Kornilova, Gladkochub, Mazukabzov and Donskaya2009; Nagovitsin et al., Reference Nagovitsin, Stanevich and Kornilova2010). The fossiliferous shales are interspersed with stromatolitic carbonates and so represent shallow platform environments. Depositional age is constrained only broadly by shale dating techniques to be ca. 1000–1500 Myr. Another possible Mesoproterozoic index fossil includes Lineaforma from the Roper Group, the Kotuikan Formation of Siberia (Vorob’va et al., Reference Vorob’eva, Sergeev and Yu2015), and Belt Supergroup of Montana, USA (Adam, Reference Adam2014).

Tappania plana occurs as well in the Ruyang Group, China (Xiao et al., Reference Xiao, Knoll, Kaufman, Yin and Zhang1997; Yin, Reference Yin1997; Yin et al., Reference Yin, Yuan, Meng and Hu2005); the Sarda Formation of the Bahraich Group, Ganga Basin (Prasad and Asher, Reference Prasad and Asher2001) and possibly correlative beds of the Kheinjua Group,Vindhyan Basin (Prasad et al., Reference Prasad, Uniyal and Asher2005) in northern India; and in the Lower Belt Group, Montana (Adam, Reference Adam2014; Adam et al., Reference Adam, Skidmore and Mogk2016). Detrital zircons indicate that Ruyang deposition began no earlier than 1700 Ma (Hu et al., Reference Hu, Zhao and Zhou2014), and xenotime Pb-Pb ages of about 1400 Ma for the overlying Luoyu Group constrain deposition from above (Lan et al., Reference Lan, Li, Chen, Li, Hofmann, Zhang, Liu, Tang, Ling and Li.2014). A U-Pb zircon date from an ash bed within the Luoyu Group potentially constrains Ruyang deposition to be older than 1611±8 Ma, but the abundance of detrital grains in the dated bed and the wide range of ages for individual zircons (Su et al., Reference Su, Li, Xu, Jia, Geng, Zhou, Wang and Pu2012) suggest that the published date may provide only a maximum age constraint on Luoyu deposition (Lan et al., Reference Lan, Li, Chen, Li, Hofmann, Zhang, Liu, Tang, Ling and Li.2014). Belt microfossils, which share many taxa in common with the Roper Group (Horodyski, Reference Horodyski1980, Reference Horodyski1993; Adam, Reference Adam2014; Adam et al., 2016), are similarly constrained by a 1576±13 Ma basement, 1460–1470 Ma sills that intrude into the fossiliferous stratigraphy and a U-Pb zircon date of 1454±9 Ma for bentonite in the overlying Helena Formation (Lydon, Reference Lydon2007). U-Pb zircon dating of ash beds just below the Vindhyan succession containing unambiguous Tappania indicates that these fossils are ≤1631±1 Ma (Ray et al., Reference Ray, Martin, Veizer and Bowring2002). Thus, all known occurrences of T. plana fall within the latest Paleoproterozoic or Mesoproterozoic Era, with the Roper and Belt populations being the most tightly constrained by radiometric ages. The absence in Roper assemblages of distinctive taxa (e.g., the distinctive acanthomorphic taxon Shuiyousphaeridium macroreticulatum or the ornamented forms Miroedichia sp. and Lophosphaeridium sp.) that co-occur with Tappania elsewhere could reflect differences in either age or environment (e.g., Nagovitsin et al., Reference Nagovitsin, Stanevich and Kornilova2010).

More broadly, the moderately diverse protist compressions of the Roper Group are intermediate in nature between the simple leiosphere-dominated assemblages found in most late Paleoproterozoic shales (e.g., Lamb et al., Reference Lamb, Awramik, Chapman and Zhu2009; Peng et al., 2009) and the slightly more diverse (and taxonomically distinctive) assemblages reported from late Mesoproterozoic shales (e.g., Hermann, Reference Hermann1990; Samuelsson et al., Reference Samuelsson, Dawes and Vidal1999). Recently, Vorob’eva et al. (Reference Vorob’eva, Sergeev and Yu2015) reported a relatively diverse assemblage of microfossils in the ~1.5 Ga Kotuikan Formation of Siberia. The assemblage includes 12–14 spheroidal and filamentous forms plausibly interpreted as eukaryotes, but no acanthomorphs. Notably, the Kotuikan assemblage contains the distinctively striated filament Lineaforma elongata, which is also found in the Roper Group. Sergeev et al. (Reference Sergeev, Knoll, Vorob’eva and Sergeeva2016) also reported well-preserved microfossils in shales of the 1.4–1.45 Ga Kaltasy Formation, East European Platform, Russia. This assemblage includes a number of probable eukaryotic taxa, but also lacks conspicuously ornamented spheromorphic populations, which in this case possibly reflects the unusual (for Mesoproterozoic successions) combination of basinal deposition and oxic bottom waters. In general, then, the summed occurrences suggest that while many of the organic-walled microfossils in the Roper and other assemblages have long stratigraphic ranges, some can be used to identify uppermost Paleoproterozoic and Mesoproterozoic sedimentary successions and may, in time, permit the broad subdivision of Mesoproterozoic time.

The phylogenetic and functional interpretation of Roper fossils

Because Roper fossils are both unusually well preserved and differentially well constrained by age and environment, they prompt questions of phylogenetic affiliation. In particular, can individual populations be identified with confidence as eukaryotes and, if so, can they further be assigned to extant eukaryotic clades?

In principle, Roper populations could include the polysaccharide sheaths and envelopes of cyanobacteria or other bacteria, the walls of metabolically active eukaryotic cells, and eukaryotic resting or reproductive cysts. Cyst walls are commonly reinforced with compounds that improve preservation potential, for example, sporopollenin in plant spores, dinosporin in some dinoflagellates, and algaenan in a few green algae and eustigmatophytes (de Leeuw et al., Reference De Leeuw, Vesteegh and van Bergen2006; Kodner et al., Reference Kodner, Knoll and Summons2009; Scholz et al., Reference Scholz, Weiss, Jinkerson, Jing, Roth, Goodenough, Posewitz and Gerkene2014). Known and assumed protistan cysts predominate in Phanerozoic marine shales, and this has understandably influenced the interpretation of older microfossils. We must recognize, however, that prospects for the preservation of vegetative walls would have been enhanced in the low-oxygen, bioturbation-free muds found widely in earlier seaways, as illustrated by the preservation of simple multicellular and coenocytic remains in Neoproterozoic shales (Butterfield et al., Reference Butterfield, Knoll and Swett1994; Butterfield, Reference Butterfield2009) and carbonaceous seaweeds in Ediacaran and Paleozoic successions (e.g., Xiao et al., Reference Xiao, Yuan, Steiner and Knoll2002; LoDuca et al., Reference LoDuca, Kluessendorf and Mikulic2003; Kenrick and Vinther, Reference Kenrick and Vinther2006; Yuan et al., Reference Yuan, Chen, Xiao, Zhou and Hua2011).

Bacterial microfossils do occur in the Roper assemblage, especially Siphonophycus spp., which is found as minor components of Roper assemblages. Sheath-forming filaments occur in a number of bacterial clades, but given their relatively large size and occurrence in oxic waters within the shallow reaches of the photic zone, Siphonophycus populations are most readily interpreted as cyanobacteria comparable to modern Lyngbya, Plectonema, and Phormidium (Rippka et al., Reference Rippka, Deruelles, Waterbury, Herdman and Stanier1979). The Roper assemblage also includes rare trichomes and pseudoseptate filaments that may record cyanobacteria or other bacteria. Such an interpretation is fully in accord both with microfossil assemblages preserved in Proterozoic cherts and molecular clocks that indicate major cyanobacterial diversification before the time of Roper deposition (Tomitani et al., Reference Tomitani, Knoll, Cavanaugh and Ohno2006, and references cited therein).

Cyanobacteria may also occur among spheromorphic forms. Horodyski (Reference Horodyski1993), for example, interpreted Satka squamifera as possible envelopes of colonial entophysalid cyanobacteria, a view formalized by the reassignment of this and other probable synonyms of Satka colonialica to Squamosphaera (Tang et al., Reference Tang, Pang, Yuan, Wan and Xiao2015; Porter and Riedman, in Reference Porter and Riedmannpress). Simple leiosphaerid compressions could also include the envelopes of colonial coccoidal cyanobacteria, some of which can have both a large diameter and medial splits similar to those commonly interpreted as excystment structures in microfossils (Waterbury and Stanier, Reference Waterbury and Stanier1978). TEM may be necessary to ascertain the affinities of leiospherids, especially those with very thin walls. In the limited number of Roper specimens examined to date, preserved complex multilayered wall ultrastructure suggests eukaryotic rather than cyanobacterial affinities (Javaux et al., Reference Javaux, Knoll and Walter2004; see systematic paleontology section).

While comparisons to cyanobacteria are based principally on morphological similarities, constrained by paleoenvironmental setting (e.g., Knoll and Golubic, Reference Knoll and Golubic1992), taphonomic experiments underscore the preservation potential of cyanobacterial sheaths and envelopes (e.g., Bartley, Reference Bartley1996). Recent microanalyses of modern and subfossil mats in Antarctic lakes provide strong evidence for the preservation of cyanobacterial morphologies and chemistries, including sheaths and the sheath pigment scytonemin (Lepot et al., Reference Lepot, Compère, Gérard, Namsaraev, Verleyen, Tavernier, Hodgson, Vyverman, Gilbert, Wilmotte and Javaux2014).

If eukaryotic, Roper microfossils must be viewed as the remains of cell walls, which places both functional and phylogenetic constraints on interpretation. Cell walls are best known from algae, especially the cellulosic cell walls of green, red, brown, dinoflagellate, and some golden-brown algae (Graham and Wilcox, Reference Graham and Wilcox2000). Walls occur, as well, in osmotrophic eukaryotes, including the chitinous walls of fungi and the cellulosic walls of oomycetes (Melida et al., Reference Melida, Sandoval-Sierra, Dieguez-Uribeondo and Bulone2013). Moreover, a wall can form during a specific life cycle stage, even in organisms not otherwise characterized by cell wall synthesis (e.g., the cellulosic macrocyst walls of dictyostelid amoebozoans) (Saga and Yanagisawa, Reference Saga and Yanagisawa1982; Blanton et al., Reference Blanton, Fuller, Iranfar, Grimson and Loomis2000) and chemically uncharacterized walls synthesized by coccoidal cells in chlorarachniophyte rhizarians (Ishida and Hara, Reference Ishida and Hara1994).

Walled resting or reproductive cysts occur widely within the Eukarya, not only in algae, but also in heterotrophic clades. Ciliates, for example, make cyst walls that can be smooth or conspicuously ornamented (Beers, Reference Beers1948, Reference Beers1966; Foissner et al., Reference Foissner, Mueller and Agatha2007; Verni and Rosati, Reference Verni and Rosati2011), and so do many animals (e.g., Blades-Eckelbarger and Marcus, Reference Blades-Eckelbarger and Marcus1992). In many eukaryotes, cyst formation (commonly but not always associated with sexual fusion) is induced by conditions that inhibit growth, including desiccation, nutrient deprivation, and anoxia, and so one might expect a resting stage to occur in the life cycles of eukaryotes in oceans with anoxic water masses beneath a thin oxic mixed layer (Johnston et al., Reference Johnston, Goldberg, Poulton, Sergeev, Podkovyrov, Vorob’eva, Bekker and Knoll2012). The broad phylogenetic distribution of cellulose and other wall compounds suggests that the ability to synthesize a protective wall evolved early in the Eukarya, perhaps before the earliest divergences of crown group taxa.

Tappania plana has been interpreted as a metabolically active microorganism on the basis of its irregularly placed, occasionally branching processes that extend outward from the main vesicle (Xiao et al., Reference Xiao, Knoll, Kaufman, Yin and Zhang1997; Javaux et al., Reference Javaux, Knoll and Walter2003, Reference Javaux, Knoll and Walter2004). Bulbous extensions on the same individuals may record vegetative reproduction. Cell walls that completely encompass individuals are common in photosynthetic and osmotrophic eukaryotes, but the cylindrical extensions provide a functional argument in favor of osmotrophy. These structures would increase the surface area for absorption and enable cells to probe nutrient-rich habitat patches, but would do little to enhance primary production. Butterfield (Reference Butterfield2005a), in fact, interpreted Tappania as a possible fungus, based on a population from Neoproterozoic shales of the Shaler Group, the Canadian Arctic (but see Butterfield, Reference Butterfield2015). As noted in the systematic paleontology section, Shaler fossils differ in many ways from Roper and other Mesoproterozoic Tappania, but the functional argument holds. In eukaryote evolution, phagotrophy is the ancestral state (evolved at least at the time of LECA, Knoll and Lahr, Reference Knoll and Lahr2016), while phototrophy required the evolution of chloroplast by endosymbiosis of a cyanobacteria, and thus is derived and evolved not later than 1.1 Ga—the age of Bangiomorpha. Today, many marine protists are mixotrophs (able to use both phagotrophy and phototrophy; Mitra et al., Reference Mitra2016).

The ability to absorb dissolved organic molecules (osmotrophy) is ubiquitous among protists (Mitra et al., Reference Mitra2016), but only a few clades, chiefly fungi and oomycetes, employ osmotrophy as the primary or sole means of obtaining food, having lost phagotrophy (Richards and Talbot, Reference Richards and Talbot2013). Recently, Knoll and Lahr (Reference Knoll and Lahr2016) investigated the phylogenetic distribution of major feeding modes within the Eukarya. While bacterivory is basal within the domain, other feeding modes evolved early, helping to explain the later Mesoproterozoic diversification of crown groups. Molecular clock estimates for the initial divergence of crown group fungi generally postdate Roper time (e.g., 800 Ma, Berney and Pawlowski, Reference Berney and Pawlowski2006; 730–820 Ma, Lücking et al., Reference Lücking, Huhndorf, Pfister, Plata and Lumbsch2009; 1050 Ma, Parfey et al., Reference Parfrey, Lahr, Knoll and Katz2011; 812 Ma, Floudas et al., Reference Floudas2012). Crown group Stramenopiles may also have late Mesoproterozoic or Neoproterozoic origins (e.g., Parfrey et al., Reference Parfrey, Lahr, Knoll and Katz2011). For this reason, it is possible that early Mesoproterozoic Tappania fossils record stem group protists functionally, but not necessarily phylogenetically comparable to extant osmotrophic heterotrophs. In any event, the complex morphology of Tappania provides direct evidence for cell organization by a dynamic cytoskeleton and membrane system, which is a fundamental feature of eukaryotic biology (Javaux et al., Reference Javaux, Knoll and Walter2001; Knoll et al., Reference Knoll, Javaux, Hewitt and Cohen2006).

Other Roper fossils find reasonable interpretation as cyst walls, for example, Valeria lophostriata, with its distinctive ornamentation of parallel ridges and opening by medial split (Javaux et al., Reference Javaux, Knoll and Walter2003, Reference Javaux, Knoll and Walter2004). Accepting V. lophostriata as a resting or reproductive cyst relaxes any constraint on its metabolism or placement within a specific subgroup of the eukaryotic domain (as noted above, cysts occur in many eukaryotic taxa that lack walls on metabolically active cells). Similarly, the ornamented spheromorphs Dictyosphaera delicata, with its reticulated wall, and Satka favosa, with its wall made of polygonal plates and (rare) opening by medial split, are best interpreted as eukaryotic cysts. Blastanosphaira kokkoda has a finely chagrinate wall, and intensive budding, both of which are evidence for vegetative reproduction.

Spheromorphic microfossils in Paleo- and Mesoproterozoic rocks have sometimes been interpreted as green algae, requiring an early origin of photosynthesis in the domain (Moczydłowska et al., Reference Moczydłowska, Landing, Zang and Palacios2011). Chlorophyte algae are sometimes recognized on the basis of a distinctive trilaminar structure (TLS) observed in TEM images of cell walls (Allard and Templier, Reference Allard and Templier2000), and TLS has been documented in microfossils as old as Cambrian (Talyzina and Moczydłowska, Reference Talyzina and Moczydłowska2000). TLS covaries phylogenetically with the biosynthetic capacity to make long-chain aliphatic molecules called algaenans (Allard and Templier, 2000), and a phylogenetic survey of this capacity suggests that it may be limited to two (now) non-marine clades within the Trebouxiophyceae and Chlorophyceae (Kodner et al., Reference Kodner, Knoll and Summons2009), neither of which is likely to have diverged much earlier than the Ediacaran or Cambrian periods. In the Roper Group’s taxa studied with TEM, the occurrence of TLS has not been observed to date and we have no indication for photosynthetic eukaryotic crown group taxa (Javaux et al., Reference Javaux, Knoll and Walter2004).

Alternatively, prasinophyte algae, a paraphyletic group at the base of the green algal tree, can form thick-walled phycomata, which are found widely in Paleozoic shales (Colbath and Grenfell, Reference Colbath and Grenfell1995). Some phycomata have a diagnostic ultrastructure (Talyzina and Moczydłowska, Reference Talyzina and Moczydłowska2000), but this has not been observed in Roper or other microfossils of comparable age. Thus, the argument that Roper and other early microfossil assemblages contain green algae must rely on broad comparisons of simple morphologies and the debatable assumption that preserved eukaryotic microfossils are likely to be algal.

Molecular estimates for the origin of crown group green algae vary widely (Fig. 10), but generally suggest late Mesoproterozoic or younger diversification (e.g., 1100 Ma, Heckman et al., Reference Heckman, Geiser, Eidell, Stauffer, Kardos and Hedges2001; 1200 Ma, Yoon et al., Reference Yoon, Hackett, Ciniglia, Pinto and Bhattacharya2004; 1000–900 Ma, Parfrey et al., Reference Parfrey, Lahr, Knoll and Katz2011; 936 Ma, Becker, Reference Becker2013; and even ~700 Ma, Berney and Pawlowski, Reference Berney and Pawlowski2006). The ~800 Ma Cladophora-like fossil Proterocladus casts doubt on the youngest molecular clock estimates, and the early diverging red alga Bangiomorpha from 1100–1200 Ma cherts in the Canadian Arctic (Butterfield, Reference Butterfield2000) further constrains the age of total (but not crown) group green algae. Nonetheless, if even the oldest of current molecular clock estimates is broadly correct, it is unlikely that Roper microfossils can be interpreted in terms of specific extant clades within the green algae.

If Roper leiosphaerids cannot be assigned to crown group green algal clades, what are the possibilities for phylogenetic placement? Not surprisingly, age estimates for the last eukaryotic common ancestor (LECA) of all extant eukaryotes vary among treatments, but those not rejected on the basis of Bangiomorpha’s age and interpretation suggest a late Paleoproterozoic or early Mesoproterozoic time of origin for the eukaryotic crown group (Fig. 9). Accepting this, Roper fossils could include the vegetative walls or resting cysts of stem-group green algae, stem-group taxa of the more inclusive Archaeplastida (green algae/embryophytes, red algae and glaucocystophytes, united by the presence of a chloroplast derived via primary endosymbiosis with a cyanobacterium), stem-group or morphologically unrecognizable crown-group members of other non-photosynthetic eukaryotic clades, or stem-group eukaryotes (before LECA). In the absence of additional data, we find it impossible to choose among these possibilities. Note, however, that it would not be unusual to have a biota dominated by stem-group members of a clade. For example, most arthropod diversity in early and mid-Cambrian oceans belonged to stem group members of the phylum, and the same is true of Cambrian echinoderms, Carboniferous seed plants, and many other clades. Stem-group taxa are common in the deep fossil record.

Figure 9 Comparison of Roper age with molecular clock estimates for the divergences of crown group green algae, photosynthetic eukaryotes, and crown group eukaryotes. Circle, diamond and triangles are the mean ages for the origin of crown group algae, plastid, crown group eukaryotes, respectively, and the dark gray, medium gray and white rectangles represent the errors on estimates, respectively.

Finally, there are the large, striated tubes of Lineaforma elongata, which commonly are fragmental but locally abundant in Roper samples. The size and complexity of these tubes favor a eukaryotic interpretation, but more specific attribution is impossible.

In general, then, eukaryotic remains are prominent, even dominant components of the Roper assemblage, but all are simple and, at lower taxonomic levels, problematic. Consistent with molecular clock inferences, Roper eukaryotes may include stem-group taxa; early, morphologically unattributable crown-group species; or both. Missing from the Roper biota are highly ornamented cysts of the type found commonly in later Neoproterozoic and, especially, Phanerozoic shales. Cyst ornamentation can serve a number of purposes (see, for example, Cohen et al., Reference Cohen, Kodner and Knoll2009), one of which is defense against predation (e.g., Peterson and Butterfield, Reference Peterson and Butterfield2005). The last common ancestor of extant eukaryotes was probably a heterotroph capable of phagocytosing bacteria and other small particles; eukaryotes that eat other eukaryotic cells, however, are derived (Knoll and Lahr, Reference Knoll and Lahr2016). The limited ornamentation of Roper microfossils is consistent with the hypothesis that predation on protists was low prior to the Neoproterozoic Era, because of the relatively late radiation of eukaryovorous protists (Knoll, Reference Knoll2014) and animals (Butterfield, Reference Butterfield2015).

Taxonomy aside, the Roper assemblage documents biological innovations in early eukaryotes (Fig. 10; see also Javaux, Reference Javaux2006, Reference Javaux2011; Knoll et al., Reference Knoll, Javaux, Hewitt and Cohen2006). Reproductive modes in Roper populations include simple binary division and budding (e.g., Tappania, Blastanosphaira). We have no direct evidence for sex in Roper populations, but this reflects absence of evidence and not necessarily evidence of absence. Sex was present in the last common ancestor of extant eukaryotes, so any paleontological inference must rest on currently uncertain systematic interpretations of Roper fossils as stem- or crown-group eukaryotes. Whether associated with sexual fusion or not, Roper protists formed resting cysts, with excystment by medial split (Valeria, Satka favosa) and possibly by the opening of neck-like expansions (Tappania). Simple multicellularity is observed both in eukaryotes (septa in Tappania processes) and in prokaryotes (colonies of diverse types and filaments). The wall ornamentation of several taxa, especially Tappania’s heteromorphic processes and the plates of Satka favosa and Dictyosphaera delicata, implies the presence of a eukaryotic cytoskeleton. The tessellation of organic plates to make up the wall of these acritarchs further suggests the presence of an internal membrane system (including endoplasmic reticulum, or ER) and Golgi apparatus. The Golgi apparatus (or remnants of, in parasites) and the ER are essential for intracellular transport, occur in all extant eukaryotes, and are associated with the nuclear envelope (Jékely, Reference Jékely2006), although the relative timing of their appearance is unknown and the origin of the nucleus itself is far from constrained (see review in Lopez-Garcia and Moreira, Reference Lopez-Garcia and Moreira2015).

Figure 10 Biological innovations in early eukaryotes inferred from preserved microfossils (modified from Javaux, Reference Javaux2011).

Conclusions

Roper microfossils contribute to an increasingly refined picture of life in Mesoproterozoic oceans, complementing the window opened by microfossils preserved in silicified carbonates. Chert assemblages largely illuminate peritidal environments dominated by diverse cyanobacteria and contain few recognizable eukaryotes (Muir, Reference Muir1976, Reference Muir1979; Oehler, Reference Oehler1978; Horodyski and Donaldson, Reference Horodyski and Donaldson1980, Reference Horodyski and Donaldson1983; Zhang, Reference Zhang1981; Golubic et al., Reference Golubic, Sergeev and Knoll1995; Sergeev et al., Reference Sergeev, Knoll and Grotzinger1995).

Stromatolites further indicate that microbial mat communities covered extensive portions of the Mesoproterozoic seafloor, extending from supratidal environments to the base of the photic zone (Bertrand-Sarfati and Walter, Reference Bertrand-Sarfati and Walter1981; Walter et al., Reference Walter, Krylov and Muir1988). Cyanobacteria are generally accepted as the principal architects of Mesoproterozoic stromatolites, but whether eukaryotes participated in mat communities is difficult to know, given that few stromatolites contain well-preserved microfossils. Variation in macrostructure may well tell us mostly about the range of physical and chemical environments in which stromatolites accreted (e.g., Grotzinger and Knoll, Reference Grotzinger and Knoll1999; Bosak et al., Reference Bosak, Knoll and Petroff2013), but microstructure, or petrofabric, can preserve clues to microbial community diversity (Knoll et al., Reference Knoll, Wörndle and Kah2013). Eukaryotes could be recorded by macroscopic chain-of-beads impressions called Horodyskia (Grey and Williams, Reference Grey and Williams1990; Fedonkin and Yochelson, Reference Fedonkin and Yochelson2002; review in Dong et al., Reference Dong, Xiao, Shen and Zhou2008) and the Mesoproterozoic specimens of coiled centimeter-scale septate compressions named Grypania (Walter et al., Reference Walter, Du and Horodyski1990), both exposed on siliciclastic bedding planes. The phylogenetic and functional nature of these organisms remains obscure.

Microfossils suggest that eukaryotic organisms were most common in the water column and non-mat benthos of well-oxygenated, shallow-shelf environments. Because the last common ancestor of extant eukaryotes was a phagocytosing heterotroph that consumed bacteria and other small particles, Roper eukaryotes certainly would have played a role in completing the marine carbon cycle. This may have been true in anoxic as well as oxic environments, because many eukaryotes retain the capacity for anaerobic metabolism (Müller et al., Reference Müller, Mentel, van Hellemond, Henze, Woehle, Gould, Yu, van der Giezen, Tielens and Martin2012). Osmotrophic uptake of organic molecules must also have occurred, and appears to have the primary form of carbon acquisition in Tappania plana. As discussed above, phagotrophic protists were present in Mesoproterozoic oceans, but these may not have included protists able to eat other large eukaryotic cells.

Whether eukaryotes played an important role as primary producers is less clear. As noted above, microfossil morphologies are agnostic with respect to this metabolism, and limited organic geochemical data suggest that bacteria were the principal primary producers in Mesoproterozoic oceans (Brocks et al., Reference Brocks, Love, Summons, Knoll, Logan and Bowden2005). Primary production by eukaryotes might well have been limited by fixed nitrogen availability (Anbar and Knoll, Reference Anbar and Knoll2002; Reinhard et al., Reference Reinhard, Planavsky, Robbins, Partin, Gill, Lalonde, Bekker, Konhauser and Lyons2013), especially in oxic waters above sulfidic water masses (Boyle et al., Reference Boyle, Clark, Poulton, Shields-Zhou, Canfield and Lenton2013). The spatial distribution of presumed eukaryotes in the Roper Basin is consistent with isotopic inferences about Mesoproterozoic nitrogen cycling (Stüeken, Reference Stüeken2013). Upward mixing of anoxic and sometimes sulfidic waters would also have constituted a persistent challenge for eukaryotes in the photic zone (Johnston et al., Reference Johnston, Wolfe-Simon, Pearson and Knoll2009, Reference Johnston, Poulton, Dehler, Porter, Husson and Canfield2010; Guilbaud et al., Reference Guilbaud, Poulton, Butterfield, Zhu and Shields-Zhou2015).

In short, Mesoproterozoic oceans supported diverse microbial communities that included early eukaryotes, some of them preserved in Roper shales. The diversity and ecological importance of these early protists, however, were much lower than in later Neoproterozoic and Phanerozoic ecosystems, which is a function, at least in part, of ecological constraints involving food web complexity and physical constraints imposed by marine redox profiles.

Acknowledgments

We thank M. Walter and the core facility staffs at the Northern Territory Geological Survey in Darwin and the Australian Geological Survey Organization in Canberra for making it possible to sample Roper cores. We also thank Z. Adam, V.N. Sergeev, L.A. Riedman, and S. Porter for discussion and access to unpublished materials, and reviewers for helpful criticisms of an earlier draft. E.J acknowledges support from European Research Council Stg ELITE FP7/308074, Belspo IAP Planet Topers, and the Francqui Foundation research professorship. AHK acknowledges support from NASA Exobiology Grant NAG5-3645 and the NASA Astrobiology Institute.

References

Abbott, S.T., and Sweet, I.P., 2000, Tectonic control on third-order sequences in a siliciclastic ramp-style basin: an example from the Roper Superbasin (Mesoproterozoic), northern Australia: Australian Journal of Earth Sciences, v. 47, p. 637657.CrossRefGoogle Scholar
Adam, Z.R., 2014, Microfossil Paleontology and Biostratigraphy of the Early Mesoproterozoic Belt Supergroup, Montana [Ph.D. dissertation]: Bozeman, Montana State University, 192 p.Google Scholar
Adam, Z.R, Skidmore, M.L., and Mogk, D.W., 2016, Paleoenvironmental implications of an expanded microfossil assemblage from the Chamberlain Formation, Belt Supergroup, Montana: The Geological Society of America Special Paper, v. 522, 20 p.Google Scholar
Agic, H., Moczydłowska, M., and Yin, L.-M., 2015, Affinity, life cycle, and intracellular complexity of organic-walled microfossils from the Mesoproterozoic of Shanxi, China: Journal of Paleontology, v. 89, p. 2850.Google Scholar
Allard, B., and Templier, J., 2000, Comparison of neutral lipid profile of various trilaminar outer cell wall (TLS)-containing microalgae with emphasis on algaenan occurrence: Phytochemistry, v. 54, p. 369380.Google Scholar
Anbar, A.D., and Knoll, A.H., 2002, Proterozoic ocean chemistry and evolution: a bioinorganic bridge?: Science, v. 297, p. 11371142.Google Scholar
Angert, E.R., 2005, Alternative to division in Bacteria: Nature Reviews Microbiology, v. 3, p. 214224.CrossRefGoogle ScholarPubMed
Arnold, G.L., Anbar, A.D., Barling, J., and Lyons, T.W., 2004, Molybdenum isotope evidence for widespread anoxia in mid-Proterozoic oceans: Science, v. 304, p. 8790.CrossRefGoogle ScholarPubMed
Baludikay, B.K., Storme, J.-Y., François, C., Baudet, D., and Javaux, E.J., 2016, A diverse and exquisitely preserved organic-walled microfossil assemblage from the Meso–Neoproterozoic Mbuji-Mayi Supergroup (Democratic Republic of Congo) and implications for Proterozoic biostratigraphy: Precambrian Research, v. 281, p. 166184.Google Scholar
Bartley, J., 1996, Actualistic taphonomy of cyanobacteria: implications for the Precambrian fossil record: Palaios, v. 11, p. 571586.Google Scholar
Battison, L., and Brasier, M.D., 2012, Remarkably preserved prokaryote and eukaryote microfossils within 1 Ga-old lake phosphates of the Torridon Group, NW Scotland: Precambrian Research, v. 196–197, p. 204217.Google Scholar
Becker, B., 2013, Snow ball earth and the split of Streptophyta and Chlorophyta: Trends in Plant Sciences, v. 18, p. 180183.Google Scholar
Beers, C.D., 1948, Excystment in the ciliate Bursaria truncatella : Biological Bulletin, v. 94, p. 8698.CrossRefGoogle ScholarPubMed
Beers, C.D., 1966, The excystment process in the ciliate Nassula ornata Ehrbg.: Journal of Protozoology, v. 13, p. 7983.CrossRefGoogle ScholarPubMed
Beghin, J., Storme, J.-Y., Blanpied, C., Gueneli, J., Brocks, J., Poulton, S., and Javaux, E.J., inreview, Microfossils from the late Mesoproterozoic (1.1 Ga) Atar/El Mreïti Group, Taoudeni Basin, Mauritania, northwestern Africa: Precambrian Research.Google Scholar
Berney, C., and Pawlowski, J., 2006, A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record: Proceedings of the Royal Society, London, v. 273B, p. 18671872.Google Scholar
Bertrand-Sarfati, J., and Walter, M.R., 1981, Stromatolite biostratigraphy: Precambrian Research, v. 15, p. 353371.CrossRefGoogle Scholar
Betts, P.G., and Gilles, D., 2006, The 1800–1100 Ma tectonic evolution of Australia: Precambrian Research, v. 144, p. 92125.Google Scholar
Blades-Eckelbarger, P.I., and Marcus, N.H., 1992, The origin of cortical vesicles and their role in egg envelope formation in the spiny eggs of a calanoid copepod, Centropages velificatus : Biological Bulletin, v. 182, p. 4153.Google Scholar
Blanton, R.L., Fuller, D., Iranfar, N., Grimson, M.J., and Loomis, W.F., 2000, The cellulose synthase gene of Dictyostelium : Proceedings of the National Academy of Sciences, USA, v. 97, p. 23912396.Google Scholar
Bosak, T., Knoll, A.H., and Petroff, A.P., 2013, The meaning of stromatolites: Annual Review of Earth and Planetary Sciences, v. 41, p. 2144.Google Scholar
Boyle, R.A., Clark, J.R., Poulton, S.W., Shields-Zhou, G., Canfield, D.E., and Lenton, T.M., 2013, Nitrogen cycle feedbacks as a control on euxinia in the mid-Proterozoic ocean: Nature Communications, Article 4:1533, doi: 10.1038/ncomms2511.Google Scholar
Brocks, J.J., Love, G.D., Summons, R.E., Knoll, A.H., Logan, G.A., and Bowden, S., 2005, Biomarker evidence for green and purple sulfur bacteria in an intensely stratified Paleoproterozoic ocean: Nature, v. 437, p. 866870.Google Scholar
Butterfield, N.J., 2000, Bangiomorpha pubescens n. gen., n. sp.: Implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes: Paleobiology, v. 26, p. 386404.2.0.CO;2>CrossRefGoogle Scholar
Butterfield, N.J., 2004, A vaucherian alga from the Middle Neoproterozoic of Spitsbergen: implications for the evolution of Proterozoic eukaryotes and the Cambrian explosion: Paleobiology, v. 30, p. 231252.2.0.CO;2>CrossRefGoogle Scholar
Butterfield, N.J., 2005a, Probable Proterozoic fungi: Paleobiology, v. 31, p. 165182.2.0.CO;2>CrossRefGoogle Scholar
Butterfield, N.J., 2005b, Reconstructing a complex Early Neoproterozoic eukaryote, Wynniatt Formation, Arctic Canada: Lethaia, v. 38, p. 155169.Google Scholar
Butterfield, N.J., 2009, Modes of pre-Ediacaran multicellularity: Precambrian Research, v. 173, p. 201211.Google Scholar
Butterfield, N.J., 2015, Early evolution of the Eukaryota: Palaeontology, v. 58, p. 517.CrossRefGoogle Scholar
Butterfield, N.J., Knoll, A.H., and Swett, K., 1994, Paleobiology of the Neoproterozoic Svanbergfjellet Formation, Spitsbergen: Fossils and Strata, v. 34, p. 184.CrossRefGoogle Scholar
Chernikova, D., Motamedi, S., Csueroes, M., Koonin, E.V., and Rogozin, I.B., 2011, A late origin of the extant eukaryotic diversity: divergence time estimates using rare genomic changes: Biology Direct, v. 6, Article Number: 26, doi: 10.1186/1745-6150-6-26.CrossRefGoogle ScholarPubMed
Cohen, P.A., and Knoll, A.H., 2012, Neoproterozoic scale microfossils from the Fifteen Mile Group, Yukon Territory: Journal of Paleontology, v. 86, p. 775800.CrossRefGoogle Scholar
Cohen, P.A., Kodner, R., and Knoll, A.H., 2009, Large spinose acritarchs in Ediacaran rocks as animal resting cysts: Proceedings of the National Academy of Sciences, USA, v. 106, p. 65196524.Google Scholar
Colbath, G.K., and Grenfell, H.R., 1995, Review of biological affinities of Paleozoic acid-resistant, organic-walled eukaryotic algal microfossils (including “acritarchs”): Review of Palaeobotany and Palynology, v. 86, p. 287314.CrossRefGoogle Scholar
Cotter, K., 1997, Neoproterozoic microfossils from the Officer Basin, Western Australia: Alcheringa, v. 21, p. 247270, doi: 10.1080/03115519708619166.CrossRefGoogle Scholar
Cotter, K.L., 1999, Microfossils from Neoproterozoic Supersequence 1 of the Officer Basin, Western Australia: Alcheringa, v. 23, p. 6386.Google Scholar
De Leeuw, J.W., Vesteegh, J.M., and van Bergen, P.F., 2006, Biomacromolecules of algae and plants and their fossil analogues: Plant Ecology, v. 182, p. 209233.Google Scholar
de Vries, S.T., Pryer, L.L., and Fry, N., 2008, Evolution of Neoarchaean and Proterozoic basins of Australia: Precambrian Research, v. 166, p. 3953.Google Scholar
Dong, L., Xiao, S., Shen, B., and Zhou, C., 2008, Silicified Horodyskia and Palaeopascichnus from upper Ediacaran cherts in South China: tentative phylogenetic interpretation and implications for evolutionary stasis: Journal of the Geological Society, v. 165, p. 367378.CrossRefGoogle Scholar
Douzery, E.J.P., Snell, E.A., Bapteste, E., Delsuc, F., and Philippe, H., 2004, The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils?: Proceedings of the National Academy of Sciences, v. 101, p. 1538615391.CrossRefGoogle ScholarPubMed
Downie, C., and Sarjeant, W.A.S., 1963, On the interpretation and status of some hystrichosphere genera: Palaeontology, v. 6, p. 8396.Google Scholar
Dutkiewicz, A., Volk, H., Ridley, J., and George, S., 2003, Biomarkers, brines and oil in the Mesoproterozoic, Roper Superbasin, Australia: Geology, v. 31, p. 981984.CrossRefGoogle Scholar
Eisenack, A., 1958, Tasmanites Newton 1875 und Leiosphaeridia n.g. als Gattungen der Hystrichosphaeridea: Palaeontographica Abteilug A, v. 110, p. 119.Google Scholar
Eisenack, A., 1965, Mikrofossilien aus dem Silur Gotlands. Hystrichosphären, Problematika: Neues Jahrburch für Geologie und Paläontologie Abhandlungen, v. 122, p. 257274.Google Scholar
Eme, L., Sharpe, S.C., Brown, M.W., and Roger, A.J., 2014, On the age of eukaryotes: Evaluating evidence from fossils and molecular clocks: Cold Spring Harbor Perspectives in Biology, v. 6, doi: 10.1101/cshperspect.a016139.Google Scholar
Fedonkin, M.A., and Yochelson, E.L., 2002, Middle Proterozoic (1.5 Ga) Horodyskia moniliformis Yochelson and Fedonkin, the oldest known tissue-grade colonial eukaryote: Smithsonian Contributions to Paleobiology, v. 94, p. 129.CrossRefGoogle Scholar
Floudas, I., et al., 2012, The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes: Science, v. 336, p. 17151719, doi: 10.1126/science.1221748.Google Scholar
Foissner, W., Mueller, H., and Agatha, S., 2007, A comparative fine structural and phylogenetic analysis of resting cysts in oligotrich and hypotrich Spirotrichea (Ciliophora): European Journal of Protistology, v. 43, p. 295314.Google Scholar
Golovenok, M.K., and Belova, M.Y., 1986, The Riphean microflora in the cherts from the Malgin Formation in the Yudoma-Maya basin: Paleontological Journal, v. 2, p. 8590.Google Scholar
Golubic, S., Sergeev, V.N., and Knoll, A.H., 1995, Mesoproterozoic Archaeoellipsoides: akinetes of heterocystous cyanobacteria: Lethaia, v. 28, p. 285298.CrossRefGoogle ScholarPubMed
Graham, L.E., and Wilcox, L.W., 2000, Algae: Upper Saddle River NJ, Prentice Hall, 640 p.Google Scholar
Grey, K., and Williams, I.R., 1990, Problematic bedding-plane markings from the Middle Proterozoic Manganese Subgroup, Bangemall Basin, Western Australia: Precambrian Research, v. 46, p. 307327.Google Scholar
Grotzinger, J.P., and Knoll, A.H., 1999, Proterozoic stromatolites: evolutionary mileposts or environmental dipsticks?: Annual Review of Earth and Planetary Science, v. 27, p. 313358.Google Scholar
Guilbaud, R., Poulton, S.W., Butterfield, N.J., Zhu, M., and Shields-Zhou, G.A., 2015, Global transition to ferruginous conditions in the early Neoproterozoic oceans: Nature Geosciences, v. 8, p. 466470.Google Scholar
Heckman, D.S., Geiser, D.M., Eidell, B.R., Stauffer, R.L., Kardos, N.L., and Hedges, S.B., 2001, Molecular Evidence for the Early Colonization of Land by Fungi and Plants: Science, v. 293, p. 11291133.CrossRefGoogle ScholarPubMed
Hedges, B.S., Blair, J.E., Venturi, M.L., and Shoe, J.L., 2004, A molecular timescale of eukaryote evolution and the rise of complex multicellular life: BMC Evolutionary Biology, v. 4, article 2, doi: 10.1186/1471-2148-4-2.CrossRefGoogle ScholarPubMed
Hermann, T.N., 1974, Finds of massive accumulation of trichomes in the Riphean, in Timofeev, B.V., ed., Microfitofossilii Proterozoia I Rannego Paleozoia SSSR: Leningrad, Nauka, p. 610.Google Scholar
Hermann, T.N., 1990, Organic world one billion years ago: Leningrad, Nauka, 50 p. [in Russian with English summary]Google Scholar
Hermann, T.N., and Podkovyrov, V.N., 2012, Fungal Remains from the Late Riphean: Paleontological Journal, v. 40, p. 207214.CrossRefGoogle Scholar
Hofmann, H.J., 1999, Global distribution of the Proterozoic sphaeromorph acritarch Valeria lophostriata (Jankauskas): Acta Micropaleontologica Sinica, v. 16, p. 215224.Google Scholar
Hofmann, H.J., and Jackson, G.D., 1994, Shale-facies microfossils from the Proterozoic Bylot Supergroup, Baffin Island, Canada: Paleontological Society Memoir, v. 37, p. 139.Google Scholar
Horodyski, R.J., 1980, Middle Proterozoic shale-facies microbiota from the Lower Belt Supergroup, Little Belt Mountains, Montana: Journal of Paleontology, v. 54, p. 649663.Google Scholar
Horodyski, R.J., 1993, Paleontology of Proterozoic shales and mudstones: examples from the Belt Supergroup, Chuar Group and Pahrump Group, western USA: Precambrian Research, v. 61, p. 247278.Google Scholar
Horodyski, R.J., and Donaldson, J.A., 1980, Microfossils from the Middle Proterozoic Dismal Lakes Groups, Arctic Canada: Precambrian Research, v. 11, p. 125159.Google Scholar
Horodyski, R.J., and Donaldson, J.A., 1983, Distribution and Significance of Microfossils in Cherts of the Middle Proterozoic Dismal Lakes Group, District of Mackenzie, Northwest Territories, Canada: Journal of Paleontology, v. 57, p. 271283.Google Scholar
Hu, Y., and Fu, J., 1982, Micropalaeoflora from the Gaoshanhe Formation of the Upper Precambrian in Luonan of Shaanxi Province and its stratigraphic significance: Bulletin Xi’an Institute Geology and Mineral Resources, Chinese Academy of Geological Sciences, v. 4, p. 102113.Google Scholar
Hu, G., Zhao, T., and Zhou, Y., 2014, Depositional age, provenance and tectonic setting of the Proterozoic Ruyang Group, southern margin of the North China Craton: Precambrian Research, v. 246, p. 296318.Google Scholar
Ishida, K., and Hara, Y., 1994, Taxonomic studies on the Chlorarachniophyta Chlorarachnion globosum sp. nov.: Phycologia, v. 33, p. 351358.CrossRefGoogle Scholar
Jackson, M.J., and Raiswell, R., 1991, Sedimentology and carbon-sulfur geochemistry of the Velkerri Formation, a mid-Proterozoic potential oil source in northern Australia: Precambrian Research, v. 54, p. 81108.CrossRefGoogle Scholar
Jackson, M.J., Sweet, I.P., Page, R.W., and Bradshaw, B.E., 1999, The South Nicholson and Roper Groups: evidence for the early Mesoproterozoic Roper Superbasin, in Bradshaw, B.E., and Scott, D.L., eds., Integrated Basin Analysis of the Isa Superbasin using Seismic, Well-log, and Geopotential Data: An Evaluation of the Economic Potential of the Northern Lawn Hill Platform: Canberra, Australia, Australian Geological Survey Organisation Record 1999/19. [unpaginated] Google Scholar
Jankauskas, T.V., 1979a, Nizhnerifeiskie mikrobioty Iuzhnogo Urala (Lower Riphean microbiotas of the southern Urals): Akademii Nauk SSSR, Doklady (Proceedings of the USSR Academy of Sciences), v. 247, p. 14651467. [In Russian]Google Scholar
Jankauskas, T.V., 1979b, Srednerifeyski microbiota Yuzhnogo Urala i Bashkirskogo Priural’ya (Middle Riphean microbiota of the southern Urals and the Ural region in Bashkiria): Akademii Nauk SSSR, Doklady (proceedings of the USSR Academy of Sciences), v. 248, p. 190193. [in Russian]Google Scholar
Jankauskas, T.V., 1982, Mikrofossilii rifeya Yuzhnogo Urala [Microfossils of the Riphean of the South Urals], in Keller, B.M., ed., Stratotype of the Riphean: Paleontology and Paleomagnetics: Moscow, Nauka, p. 84120.Google Scholar
Jankauskas, T.V., Mikhailova, N., and Hermann, T.N., 1989, Mikrofossilii dokembriya SSSR (Precambrian microfossils of the USSR): Leningrad, Trudy Instituta Geologii i Geochronologii Dokembria SSSR Akademii Nauk. Nauka, 188 p. [In Russian]Google Scholar
Javaux, E.J., 2006, The early eukaryote fossil record, in Jékely, G., ed., Evolution of the Eukaryotic Endomembrane System and Cytoskeleton: Austin, Texas, Landes Biosciences Publishers, p. 119.Google Scholar
Javaux, E.J., 2011, Evolution of early eukaryotes in Precambrian oceans, in Gargaud, M., Lopez-Garcia, P., and Martin, H., eds., Origins and Evolution of Life: an astrobiology perspective: Cambridge, UK, Cambridge University Press, p. 414449.Google Scholar
Javaux, E.J., and Marshall, C.P., 2006, A new approach in deciphering early protist paleobiology and evolution: combined microscopy and microchemistry of single Proterozoic acritarchs: Review of Palaeobotany and Palynology, v. 139, p. 115.Google Scholar
Javaux, E.J., Knoll, A.H., and Walter, M.R., 2001, Ecological and morphological complexity in early eukaryotic ecosystems: Nature, v. 412, p. 6669.Google Scholar
Javaux, E.J., Knoll, A.H., and Walter, M.R., 2003, Recognizing and interpreting the fossils of early eukaryotes: Origins of Life and Evolution of the Biosphere, v. 33, p. 7594.Google Scholar
Javaux, E.J., Knoll, A.H., and Walter, M.R., 2004, TEM evidence for eukaryotic diversity in mid-Proterozoic oceans: Geobiology, v. 2, p. 121132.Google Scholar
Javaux, E.J., Marshall, C.P., and Bekker, A., 2010, Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits: Nature, v. 463, p. 934938.CrossRefGoogle ScholarPubMed
Jékely, G., 2006, Evolution of the Eukaryotic Endomembrane System and Cytoskeleton: Advances in Experimental Medicine and Biology, v. 607: Austin, Texas, Landes Biosciences Publishers, 145 p.Google Scholar
Johnston, D.T., Farquhar, J., Summons, R.E., Shen, Y., Kaufman, A.J., Masterson, A.L., and Canfield, D.E., 2008, Sulfur isotope biogeochemistry of the Proterozoic McArthur Basin: Geochimica et Cosmochimica Acta, v. 72, p. 42784290.Google Scholar
Johnston, D.T, Wolfe-Simon, F., Pearson, A., and Knoll, A.H., 2009, Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth’s middle age: Proceedings of the National Academy of Sciences, USA, v. 106, p. 1692516929.Google Scholar
Johnston, D.T, Poulton, S., Dehler, C., Porter, S., Husson, J., and Canfield, D.E., 2010, An emerging picture of Neoproterozoic ocean chemistry: Insights from the Chuar Group, Grand Canyon, USA: Earth and Planetary Science Letters, v. 290, p. 6473.CrossRefGoogle Scholar
Johnston, D.T., Goldberg, T., Poulton, S.W., Sergeev, V.N., Podkovyrov, V., Vorob’eva, N.G., Bekker, A., and Knoll, A.H., 2012, Late Ediacaran redox stability and metazoan diversification: Earth and Planetary Science Letters, v. 335–336, p. 2535.Google Scholar
Kaufman, A.J., and Xiao, S., 2003, High CO2 levels in the Proterozoic atmosphere estimated from analyses of individual microfossils: Nature, v. 425, p. 279282.Google Scholar
Kendall, B., Creaser, R.A., Gordon, G.W., and Anbar, A.D., 2009, Re-Os and Mo isotope systematics of black shales from the Middle Proterozoic Velkerri and Wollogorang Formations, McArthur Basin, northern Australia: Geochimica et Cosmochimica Acta, v. 73, p. 25342558.CrossRefGoogle Scholar
Kenrick, P., and Vinther, J., 2006, Chaetocladus gracilis n. sp., a non-calcified Dasycladales from the Upper Silurian of Skåne, Sweden: Review of Palaeobotany and Palynology, v. 142, p. 153160.CrossRefGoogle Scholar
Knoll, A.H., 2014, Paleobiological perspective on early eukaryotic evolution: Cold Spring Harbor Perspectives in Biology, doi: 10.1101/cshperspect.a016121.Google Scholar
Knoll, A.H., and Golubic, S., 1992, Living and Proterozoic cyanobacteria, in Schidlowski M., Golubic, S., and Kimberley, M.M., eds., Early Organic Evolution: Implications for Mineral and Energy Resources: Berlin, Springer-Verlag, p. 450462.CrossRefGoogle Scholar
Knoll, A.H., and Lahr, D.J.G., 2016, Fossils, feeding, and the evolution of complex multicellularity, in Niklas, K.J., Newman, S., and Bonner, J.T., eds., Multicellularity, Origins and Evolution, The Vienna Series in Theoretical Biology: Boston, Massachusetts Institute of Technology, p. 116.Google Scholar
Knoll, A.H., and Swett, K., 1985, Micropalaeontology of the Late Proterozoic Veteranen Group, Spitsbergen: Palaeontology, v. 28, p. 451473.Google Scholar
Knoll, A.H., Swett, K., and Mark, J., 1991, Paleobiology of a Neoproterozoic tidal flat/lagoonal complex: the Draken Conglomerate Formation, Spitsbergen: Journal of Paleontology, v. 65, p. 531570.Google Scholar
Knoll, A.H., Javaux, E.J., Hewitt, D., and Cohen, P., 2006, Eukaryotic organisms in Proterozoic oceans: Philosophical Transactions of the Royal Society, London, v. 361B, p. 10231038.Google Scholar
Knoll, A.H., Wörndle, S., and Kah, L., 2013, Covariance of microfossil assemblages and microbialite textures across a late Mesoproterozoic carbonate platform: Palaios, v. 28, p. 453470.Google Scholar
Kodner, R., Knoll, A.H., and Summons, R.E., 2009, Phylogenetic investigation of the aliphatic, non-hydrolyzable biopolymer algaenan, with a focus on the green algae: Organic Geochemistry, v. 40, p. 854862.Google Scholar
Kralik, M., 1982, Rb–Sr age determinations on Precambrian carbonate rocks of the Carpentarian McArthur Basin, Northern Territories, Australia: Precambrian Research, v. 18, p. 157170.Google Scholar
Lamb, D.M., Awramik, S.M., Chapman, D.J., and Zhu, S., 2009, Evidence for eukaryotic diversification in the similar to 1800 million-year-old Changzhougou Formation, North China: Precambrian Research, v. 173, p. 93104.Google Scholar
Lan, Z., Li, X., Chen, Z.Q., Li, Q., Hofmann, A., Zhang, Y., Liu, Y., Tang, G., Ling, X., and Li., J., 2014, Diagenetic xenotime age constraints on the Sanjiaotang Formation,Luoyu Group, southern margin of the North China Craton: Implications for regional stratigraphic correlation and early evolution of eukaryotes: Precambrian Research, v. 251, p. 2132.Google Scholar
Lepot, K., Compère, P., Gérard, E., Namsaraev, Z., Verleyen, E., Tavernier, I., Hodgson, D.A., Vyverman, W., Gilbert, B., Wilmotte, A., and Javaux, E.J., 2014, Organic and mineral imprints in fossil photosynthetic mats of an East Antarctic lake: Geobiology, v. 12, p. 424450.Google Scholar
LoDuca, S.T., Kluessendorf, J., and Mikulic, D.G., 2003, A new noncalcified dasycladalean alga from the Silurian of Wisconsin: Journal of Paleontology, v. 77, p. 956962.Google Scholar
Lopez-Garcia, P., and Moreira, D., 2015, Open Questions on the Origin of Eukaryotes: Trends in Ecology and Evolution, v. 30, p. 697708.Google Scholar
Lücking, R., Huhndorf, S., Pfister, D.H., Plata, E.R., and Lumbsch, H.T., 2009, Fungi evolved right on track: Mycologia, v. 101, p. 810822.Google Scholar
Luo, Q.-L., 1991, New data on the microplants from Changlongshan Formation of Upper Precambrian in western Yanshan Range: Tianjin Instute of Geology and Mineral Resources, v. 25, p. 107118.Google Scholar
Lydon, J.W., 2007, Geology and metallogeny of the Belt-Purcell Basin, in Goodfellow, W.D., ed., Mineral Deposits of Canada: A Synthesis of Major Deposit-Types, District Metallogeny, the Evolution of Geological Provinces, and Exploration Methods: Geological Association of Canada, Mineral Deposits Division, Special Publication No. 5, p. 581–607.Google Scholar
Maithy, P.K., 1975, Microorganisms from the Bushimay System (Late Precambrian) of Kanshi, Zaire: The Paleobotanist, v. 22, p. 133149.Google Scholar
Marshall, C.P., Javaux, E.J., Knoll, A.H., and Walter, M.R., 2005, Combined micro-Fourier transform infrared (FTIR) spectroscopy and micro-Raman spectroscopy of Proterozoic acritarchs: a new approach to palaeobiology: Precambrian Research, v. 138, p. 208224.Google Scholar
Melida, H., Sandoval-Sierra, J.V., Dieguez-Uribeondo, J., and Bulone, V., 2013, Analyses of extracellular carbohydrates in oomycetes unveil the existence of three different cell wall types: Eukaryotic Cell, v. 12, p. 194203.Google Scholar
Mitra, A., et al., 2016, Defining Planktonic Protist Functional Groups on Mechanisms for Energy and Nutrient Acquisition: Incorporation of Diverse Mixotrophic Strategies: Protist, v. 167, p. 106120.Google Scholar
Moczydłowska, M., Landing, E., Zang, W., and Palacios, T., 2011, Proterozoic phytoplankton and timing of Chlorophyte algae origins: Palaeontology, v. 54, p. 721733.Google Scholar
Muir, M.D., 1976, Proterozoic microfossils from the Amelia Dolomite, McArthur Basin, Northern Territory: Alcheringa, v. 1, p. 143158.Google Scholar
Muir, M.D., 1979, A sabkha model for the deposition of part of the Proterozoic McArthur Group of the Northern Territory, and its implications for mineralization: BMR Journal of Australian Geology and Geophysics, v. 4, p. 149162.Google Scholar
Müller, M., Mentel, M., van Hellemond, J.J., Henze, K., Woehle, K., Gould, S.B., Yu, R.-Y., van der Giezen, R.M., Tielens, A.G.M., and Martin, W.F., 2012, Biochemistry and evolution of anaerobic energy metabolism in eukaryotes: Microbiology and Molecular Biology Reviews, v. 76, p. 444495.Google Scholar
Nagovitsin, K., 2009, Tappania-bearing association of the Siberian platform: Biodiversity, stratigraphic position and geochronological constraints: Precambrian Research, v. 173, p. 137145.Google Scholar
Nagovitsin, K.E., Stanevich, A.M., and Kornilova, T.A., 2010, Stratigraphic setting and age of the complex Tappania-bearing Proterozoic fossil biota of Siberia: Russian Geology and Geophysics, v. 51, p. 11921198.Google Scholar
Nagy, R.M., Porter, S.M., Dehler, C.M., and Shen, Y., 2009, Biotic turnover driven by eutrophication before the Sturtian low-latitude glaciation: Nature Geoscience, v. 2, p. 415418.Google Scholar
Naumova, S.N., 1949, Spory nizhnego kembriya [spores from the Lower Cambrian]: Izvestiya Akademiy Nauk, v. 4, p. 4956.Google Scholar
Naumova, S.N., 1960, Spore-pollen assemblages in the Riphean and Lower Cambrian deposits of the USSR: Proceedings of the 21st International Geological Congress, Reports of Soviet Scientists, v. 8, p. 109117. [in Russian]Google Scholar
Oehler, D.Z., 1978, Microflora of the middle Proterozoic Balbirini Dolomite (McArthur Group) of Australia: Alcheringa, v. 2, p. 269309.Google Scholar
Parfrey, L., Lahr, D., Knoll, A.H., and Katz, L.A., 2011, Estimating the timing of early eukaryotic diversification with multigene molecular clocks: Proceedings of the National Academy of Sciences, USA, v. 108, p. 1362413629.Google Scholar
Peat, C.J., Muir, M.D., Plumb, K.A., McKirdy, D.M., and Norwick, M.S., 1978, Proterozoic microfossils from the Roper Group, Northern Territory, Australia: BMR Journal of Australian Geology and Geophysics, v. 3, p. 117.Google Scholar
Peng, Y., Bao, H., and Yuan, X., 2009, New morphological observations for Paleoproterozoic acritarchs from the Chuanlinggou Formation, North China: Precambrian Research, v. 168, p. 223232.Google Scholar
Peterson, K.J., and Butterfield, N.J., 2005, Origin of the Eumetazoa: Testing ecological predictions of molecular clocks against the Proterozoic fossil record: Proceedings of the National Academy of Sciences, USA, v. 102, p. 95479552.CrossRefGoogle ScholarPubMed
Planavsky, N.J., McGoldrick, P., Scott, C.T., Li, C., Reinhard, C.T., Kelly, A.E., Chu, X., Bekker, A., Love, G.D., and Lyons, T.W., 2011, Widespread iron-rich conditions in the mid-Proterozoic ocean: Nature, v. 477, p. 448452.Google Scholar
Porter, S., 2006, The Proterozoic fossil record of heterotrophic eukaryotes, in Xiao, S., and Kaufman, A.J., eds. Neoproterozoic Geobiology and Paleobiology: Dordrecht, The Netherlands, Springer, p. 121.Google Scholar
Porter, S., and Riedmann, L.A., inpress, Systematics of organic-walled microfossils from the ~780–740 Ma Chuar Group, Grand Canyon, Arizona: Journal of Paleontology.Google Scholar
Porter, S., Meisterfeld, R., and Knoll, A., 2003, Vase-shaped microfossils from the Neoproterozoic Chuar Group, Grand Canyon: a classification guided by modern testate amoebae: Journal of Paleontology, v. 77, p. 409429, doi: http://dx.doi.org/10.1017/S0022336000044140.2.0.CO;2>CrossRefGoogle Scholar
Prasad, B., and Asher, R., 2001, Acritarch biostratigraphy and lithostratigraphic classification of Proterozoic and Lower Paleozoic sediments (Pre-unconformity sequence) of Ganga Basin, India: Paleontographica Indica, v. 5, 151 p.Google Scholar
Prasad, B., Uniyal, S.N., and Asher, R., 2005, Organic-walled microfossils from the Proterozoic Vindhyan Supergroup of Son Valley, Madhya Pradesh, India: Palaeobotanist, v. 54, p. 1360.Google Scholar
Ray, J.S., Martin, M.W., Veizer, J., and Bowring, S.A., 2002, U–Pb zircon dating and Sr isotope systematics of the Vindhyan Supergroup, India: Geology, v. 30, p. 131134.Google Scholar
Reinhard, C.T., Planavsky, N.J., Robbins, L.J., Partin, C.A., Gill, B.C., Lalonde, S.V., Bekker, A., Konhauser, K.O., and Lyons, T.W., 2013, Proterozoic ocean redox and biogeochemical stasis: Proceedings of the National Academy of Sciences, USA, v. 110, p. 53575362.Google Scholar
Richards, T.A., and Talbot, N.J., 2013, Horizontal gene transfer in osmotrophs: playing with public goods: Nature Reviews Microbiology, v. 11, p. 720727.Google Scholar
Riedman, L.A., and Porter, S.M., inpress, High morphological diversity of organic-walled microfossils from the Neoproterozoic Alinya Formation, Officer Basin, Australia: Journal of Paleontology.Google Scholar
Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M., and Stanier, R.Y., 1979, Generic assignments, strain histories and properties of pure cultures of cyanobacteria: Journal of General Microbiology, v. 111, p. 161.Google Scholar
Saga, Y., and Yanagisawa, K., 1982, Macrocyst development in Dictvostelium discoideum. 1. Induction of synchronous development by giant cells and biochemical analysis: Journal of Cell Science, v. 55, p. 341352.Google Scholar
Samuelsson, J., 1997, Biostratigraphy and paleobiology of early Neoproterozoic strata of the Kola Peninsula, northwest Russia: Norsk Geologisk Tidsskrift, v. 77, p. 16192.Google Scholar
Samuelsson, J., and Butterfield, N., 2001, Neoproterozoic fossils from the Franklin Mountains, northwestern Canada: stratigraphic and palaeobiological implications: Precambrian Research, v. 107, p. 235251.CrossRefGoogle Scholar
Samuelsson, J., Dawes, P.R., and Vidal, G., 1999, Organic-walled microfossils from the Proterozoic Thule Supergroup, Northwest Greenland: Precambrian Research, v. 96, p. 123.Google Scholar
Schepeleva, E.D., 1960, Nakhodki sinezelenykh vodoroslej v nizhnekembrijskikh otlozheniyakh Leningradskoj oblasti [Finds of blue-green algae in Lower Cambrian deposits of the Leningrad region]. in., Problemy Neftyanoj Geologii i Voprosy Metodiki Laboratornykh Issledovanij: Moscow, Nauka, p. 170172.Google Scholar
Schiffbauer, J.D., and Xiao, S., 2009, Novel application of focused ion beam electron microscopy (FIB-EM) in preparation and analysis of microfossil ultrastructures: a new view of complexity in early eukaryotic organisms: Palaios, v. 24, p. 616626.Google Scholar
Scholz, M.J., Weiss, T.L., Jinkerson, R.E., Jing, J., Roth, R., Goodenough, U., Posewitz, M.C., and Gerkene, H.G., 2014, Ultrastructure and composition of the Nannochloropsis gaditana cell wall: Eukaryotic Cell, v. 13, p. 14501464.Google Scholar
Schopf, W., 1968, Microflora of the Bitter Springs Formation, late Precambrian, central Australia: Journal of Paleontology, v. 42, p. 651688.Google Scholar
Schopf, J.W., 1992, Atlas of representative Proterozoic microfossils, in Schopf, J.W., and Klein, C., eds., The Proterozoic Biosphere: Cambridge, Cambridge University Press, p. 10571117.Google Scholar
Schopf, J.W., and Blacic, J., 1971, Microorganisms from the Bitter Springs Formation (Late Precambrian) of the North-Central Amadeus Basin, Australia: Journal of Paleontology, v. 45, p. 925960.Google Scholar
Sergeev, V.N., 1992, Silicified Microfossils of the Precambrian and Cambrian in the Urals and central Asia: Moscow, Nauka, 139 p. [in Russian]Google Scholar
Sergeev, V.N., 2006, Precambrian Microfossils in Cherts : Their Paleobiology, Classification, and Biostratigraphic Usefulness: Moscow, Geos, 280 p. [in Russian]Google Scholar
Sergeev, V.N., and Lee, S.-J., 2001, Microfossils from Cherts of the Middle Riphean Svetlyi Formation, the Uchur-Maya Region of Siberia, and Their Stratigraphic Significance: Stratigraphic Geological Correlation, v. 9, p. 312.Google Scholar
Sergeev, V.N., and Lee, S.-J., 2006, Real Eukaryotes and Precipitates First Found in the Middle Riphean Stratotype, Southern Urals: Stratigraphy and Geological Correlation, v. 14, p. 118.Google Scholar
Sergeev, V.N., Knoll, A.H., and Grotzinger, J.P., 1995, Paleobiology of the Mesoproterozoic Billiakh Group, Anabar Uplift, Northeastern Siberia: Paleontological Society Memoir, v. 39, 37 p.Google Scholar
Sergeev, V.N., Semikhatov, M.A., Fedonkin, M.A., and Vorob’eva, N.G., 2010, Principal stages in evolution of Precambrian organic world: 2. The late Proterozoic: Stratigraphy and Geological Correlation, v. 18, p. 561592.Google Scholar
Sergeev, V.N, Knoll, A.H., Vorob’eva, N., and Sergeeva, N., 2016, Microfossils from the lower Mesoproterozoic Kaltasy Formation, East European Platform: Precambrian Research, v. 278, p. 87107, doi: 10.1016/j.precamres.2016.03.015.Google Scholar
Shen, Y., Knoll, A.H., and Walter, M.R., 2003, Evidence for low sulphate and deep water anoxia in a mid-Proterozoic marine basin: Nature, v. 423, p. 632635.CrossRefGoogle Scholar
Sperling, E.A., Rooney, A.D., Hays, L., Sergeev, V.N., Vorob’eva, N.G., Sergeeva, N.D., Selby, D., Johnston, D.T., and Knoll, A.H., 2014, Redox heterogeneity of subsurface waters in the Mesoproterozoic ocean: Geobiology, v. 12, p. 373386.Google Scholar
Stanevich, A.M., Maksimova, E.N., Kornilova, T.A., Gladkochub, D.P., Mazukabzov, A.M., and Donskaya, T.V., 2009, Microfossils from the Arymas and Debengde Formations, the Riphean of the Olenek Uplift: Age and presumable nature: Stratigraphy and Geological Correlation, v. 17, p. 2035.Google Scholar
Strother, P.K., Knoll, A.H., and Barghoorn., E.S., 1983, Microorganisms from the late Precambrian Narssârssuk Formation, north-western Greenland: Palaeontology, v. 26, p. 132.Google Scholar
Strother, P., Battison, L., Brasier, M.D., and Wellman, C.H., 2011, Earth’s earliest non-marine eukaryotes: Nature, v. 473, p. 505509.Google Scholar
Stüeken, E.E., 2013, A test of the nitrogen-limitation hypothesis for retarded eukaryote radiation: Nitrogen isotopes across a Mesoproterozoic basinal profile: Geochimica et Cosmochimica Acta, v. 20, p. 121139.Google Scholar
Su, W., Li, H., Xu, L., Jia, S., Geng, J., Zhou, H., Wang, Z., and Pu, H.-Y., 2012, Luoyu and Ruyang Group at the south margin of the North China Craton (NCC) should belong in the Mesoproterozoic Changchengian System: direct constraints from the LA-MC-ICPMS U-Pb age of the tuffite in the Luoyukou Formation, Ruzhou, Henan, China: Geological Survey and Research, v. 35, p. 96108.Google Scholar
Sugitani, K., Mimura, K., Takeuchi, M., Lepot, K., Ito, S., and Javaux, E.J., 2015, Early evolution of large micro-organisms with cytological complexity revealed by microanalyses of 3.4 Ga organic-walled microfossils: Geobiology, v. 13, p. 522545.Google Scholar
Talyzina, N., and Moczydłowska, M., 2000, Morphological and ultrastructural studies of some acritarchs from the Lower Cambrian Lukati Formation, Estonia: Review of Palaeobotany and Palynology, v. 112, p. 121.Google Scholar
Tang, Q., Pang, K., Yuan, X., Wan, B., and Xiao, S., 2015, Organic-walled microfossils from the Tonian Gouhou Formation, Huaibei region, North China Craton, and their biostratigraphic implications: Precambrian Research, v. 266, p. 296318.Google Scholar
Timofeev, B.V., 1959, Dreveneyshaya flora Pribaltiki i ee stratigraficheskoe znachenie (Oldest flora of the Baltic area and its stratigraphic significance): Trudy Vsesoyuznogo Neftyanogo Nauchno-Issle-dovatel’skogo Geologorazvedochnogo Instituta (VNIGRI), v. 129, 320 p. [in Russian]Google Scholar
Timofeev, B.V., 1966, Mikropaleofitologicheskoe isslodovanie drevnikh svit (Microphytological investigations of ancient formations): Akademiya Nauk SSSR, Nauka, Moscow, 147 p. [in Russian]Google Scholar
Timofeev, B.V., Hermann, T.N., and Mikhailova, N.S., 1976, Mikrofitofossilii Dokembriia, Kembriia i Ordovika (Plant Microfossils of the Precambrian, Cambrian, and Ordovician): Leningrad, Scientific Institute of Precambrian Geology and Geochronology, 106 p. [in Russian]Google Scholar
Tomitani, A., Knoll, A.H., Cavanaugh, C.M., and Ohno, T., 2006, The evolutionary diversification of cyanobacteria: Molecular–phylogenetic and paleontological perspectives: Proceedings of the National Academy of Sciences, v. 103, p. 54425447.Google Scholar
Turner, R.E., 1984, Acritarchs from the type area of the Ordovicain Caradoc Series, Shropshire, England: Palaeontographica, Abteiling B, v. 190, p. 87157.Google Scholar
Verni, F., and Rosati, G., 2011, Resting cysts: a survival strategy in Protozoa Ciliophora: Italian Journal of Zoology, v. 78, p. 134145.Google Scholar
Vidal, G., and Ford, T.D., 1985, Microbiotas from the late Proterozoic Chuar Group (northern Arizona) and Uinta Mountain Group (Utah) and their chronostratigraphic implications: Precambrian Research, v. 28, p. 349389.Google Scholar
Vidal, G., and Siedlecka, A., 1983, Planktonic, acid-resistant microfossils from the Upper Proterozoic strata of Barents Sea region of Varanger Peninsula, East Finnmark, Northen Norway: Norges Geologiske undersøkelse Bulletin, v. 382, p. 4579.Google Scholar
Vorob’eva, N.G., Sergeev, V.N., and Yu, P., 2015, Kotuikan Formation assemblage: a diverse organic-walled microbiota in the Mesoproterozoic Anabar succession, northern Siberia: Precambrian Research, v. 256, p. 201222.Google Scholar
Waterbury, J.M., and Stanier, R.Y., 1978, Patterns of growth and development in pleurocapsalean cyanobacteria: Microbiological Reviews, v. 42, p. 244.Google Scholar
Walter, M.R., Krylov, I.N., and Muir, M.D., 1988, Stromatolites from Middle and Late Proterozoic sequences in the McArthur and Georgina Basins and the Mount Isa Province, Australia: Alcheringa, v. 12, p. 79106.Google Scholar
Walter, M.R., Du, R.L., and Horodyski, R.J., 1990, Coiled carbonaceous megafossils from the Middle Proterozoic of Jixian (Tianjin) and Montana: American Journal of Science, v. 290A, p. 133148.Google Scholar
Xiao, S.H., Knoll, A.H., Kaufman, A.J., Yin, L.M., and Zhang, Y., 1997, Neoproterozoic fossils in Mesoproterozoic rocks? Chemostratigraphic resolution of a biostratigraphic conundrum from the North China Platform: Precambrian Research, v. 84, p. 197220.Google Scholar
Xiao, S.H., Yuan, X.L., Steiner, M., and Knoll, A.H., 2002, Macroscopic carbonaceous compressions in a terminal Proterozoic shale: A systematic reassessment of the Miaohe biota, south China: Journal of Paleontology, v. 76, p. 347376.Google Scholar
Xing, Y., and Liu, K., 1973, On Sinian microflora in Yenliao region of China and its geographic significance: Acta Geologica Sinica, v. 1, p. 164.Google Scholar
Yang, E.C., Boo, S.M., Battacharya, D., Saunders, G.W., Knoll, A.H., Fredericq, S., Graf, L., and Yoon, H.S., 2016, Divergence times estimates and the evolution of major lineages in the florideophyte red algae: Scientific Reports, 2016 Feb 19;6:21361, doi: 10.1038/srep21361.Google Scholar
Yin, L.M., 1997, Acanthomorphic acritarchs from Meso-Neoproterozoic shales of the Ruyang Group, Shanxi, China: Review of Palaeobotany and Palynology, v. 98, p. 1525.Google Scholar
Yin, L., and Yuan, X., 2007, Radiation of Meso-Neoproterozoic and Early Cambrian protists inferred from the microfossil record of China: Palaeogeography, Palaeoclimatology, Palaeoecology, v. 254, p. 350361.Google Scholar
Yin, L.M., Yuan, X.L., Meng, F.W., and Hu, J., 2005, Protists of the Upper Mesoproterozoic Ruyang Group in Shanxi Province, China: Precambrian Research, v. 141, p. 4966.Google Scholar
Yoon, H.S., Hackett, J.D., Ciniglia, C., Pinto, G., and Bhattacharya, D., 2004, A molecular timeline for the origin of photosynthetic eukaryotes: Molecular and Biological Evolution, v. 21, p. 809818.Google Scholar
Yuan, X., Chen, Z., Xiao, S., Zhou, C.M., and Hua, H., 2011, An early Ediacaran assemblage of macroscopic and morphologically differentiated eukaryotes: Nature, v. 470, p. 390393.Google Scholar
Xiao, S., Knoll, A.H., Kaufman, A.J., Yin, L., and Zhang, Y., 1997, Neoproterozoic fossils in Mesoproterozoic rocks? Chemostratigraphic resolution of a biostratigraphic conundrum from the North China Platform: Precambrian Research, v. 84, p. 197220.Google Scholar
Zhang, Y., 1981, Proterozoic stromatolite microfloras of the Gaoyuzhuang Formation (Early Sinian: Riphean), Hebei, China: Journal of Paleontology, v. 55, p. 485506.Google Scholar
Figure 0

Figure 1 The Roper Group, showing location, facies distribution and stratigraphic column (modified from Javaux et al., 2001).

Figure 1

Figure 2 Photographs of Roper organic-walled microfossils: (1–11) Blastanosphaira kokkoda n. gen. n. sp.; (2) specimen starting budding; (3) specimen showing an elongate expansion; (4) specimen showing circular opening; (6) the bottom specimen’s wall is peeling off the vesicle; (8) thick folds between attached specimens; (5–8) specimens showing multiple budding; (11) SEM picture showing details of granular wall. (12–13) Chlorogloeaopsis contexta. (14) Coneosphaera artica. (15) Dictyosphaera delicata. (16–18) Eomicrocystis magilca: (17) detail of (16) showing oval cells and absence of external envelope. Scale bar in (1) is: (1, 2, 8, 9, 10) 13 µm; (3, 14, 16, 18) 20 µm; (4, 13, 17) 10 µm; (5) 80 µm; (6, 7) 15 µm; (11) 500 nm; (12) 50 µm. Slides and England coordinates are (1) U5 569.1 m .2 Q42, (2, 3) U5 569.1 m .2 Q40/2, (4) U5 569.1 m .2 R43, (5) U5 569.1 m .2 R/S42, (6) U5 569.1 m .2 R43, (7–10) U5 536.6 m .2 P33, (12, 13) U6 240.2 m .2 S16, (14) A82/3 311.3 m O5/2, (15) GG1 48.75 m .2 J43/4, (16) U5 125.1 m .2 N33/2, (18) U6 230.8 m H16.

Figure 2

Figure 3 Size frequency distribution of leiospheres: (1) Size frequency distribution of all Leiosphaeridia crassa/jacutica (dark-, medium-, and light-brown walls); (2) Size frequency distribution of dark-brown Leiosphaeridia crassa/jacutica; (3) Size frequency distribution of medium-brown Leiosphaeridia crassa/jacutica; (4) Size frequency distribution of light-brown Leiosphaeridia crassa/jacutica; (5) Size frequency distribution of all Leiosphaeridia minutissima/tenuissima (medium- and light-brown walls); (6) Size frequency distribution of light-brown Leiosphaeridia minutissima/tenuissima; (7) Size frequency distribution of medium-brown Leiosphaeridia minutissima/tenuissima.

Figure 3

Figure 4 Photographs of Roper organic-walled microfossils (color figures are available in the online version of this paper): (1) cf. Gemmuloides doncooki. (2, 3) Leiosphaeridia atava. (4) Light-brown Leiosphaeridia crassa/jacutica. (5) Medium-brown Leiosphaeridia crassa/jacutica. (6) Dark-brown Leiosphaeridia crassa/jacutica. (7) Light-brown Leiosphaeridia minutissima/tenuissima. (8) Medium-brown Leiosphaeridia minutissima/tenuissima. (9) Leiosphaeridia ternata. (10–12) Leiosphaeridia sp., (11) showing details of wall texture of specimen in (10). Scale bar in (1) is: (1) 85 µm; (2) 12 µm; (3) 15 µm; (4) 14 µm; (5) 17 µm; (6) 10 µm; (7–8) 6 µm; (9) 90 µm; (10) 30 µm; (11) 60 µm; (12) 10 µm. Slides and England coordinates are (1) U6 230.8 m .2 L2Y/1; (2) U6 305.1 m.2A O26 ¾; (3) U6 305.1 m.2A U37/1; (4, 7) U6 230.8 m .2 H46/G46 (area); (5) U6 240.2 m .2 O34/3; (6) U6 305.1 m .2A T26/1; (8) U6 305.1 m .2A U20; (9) U5 125.1 m; (10, 11) U6 305.1 m 2A N20; (12) U6 230.8 m.2 S24/2.

Figure 4

Figure 5 Photographs of Roper organic-walled microfossils: (1–4) Lineaforma lineata: (2) showing hollow extremity of specimen in (1), (3) specimen in situ in thin section. (5) Paleolyngbya catenata. (6–9) Satka favosa: (6) showing medial split and hollow interior, (8) showing hollow interior. (10) Siphonophycus kestron (bottom specimen) and S. typicum (top specimen). (11) Siphonophycus robustum. (12) Siphonophycus septatum. (13) Siphonophycus thulenema. (14) Squamosphaera colonialica. (15) Symplassophaeridium sp, (16–18) Synsphaeridium spp. Scale bar in (1) is: (1) 60 µm; (2) 100 µm; (3) 50 µm; (4) 110 µm; (5, 7) 15 µm; (6, 8) 20 µm; (9) 40 µm; (10, 13) 20 µm; (11, 12) 10 µm; (14) 50 µm; (15, 16) 33 µm; (17, 18) 15 µm. Slides and England coordinates are (1, 2) U5 125.1 m C13/3; (3) thin section 3785a R47/1; (4) A82/3 328.35 m.3 N41/4; (5) U5 130.5 ker E21; (6) U6 240.8 m .2 K23/3; (7) U6 305.1 m . E29; (8) U6 230.8 m.2 F14; (9) U6 230.8 m .2 J26/4; (10) U6 240.2 m .2 Z27/2; (11) U5 125.1 m .2 X48/4; (12) GG1 340.2 m.3 M13; (13) U6 240.2 m .2 Q18/3; (14) A82/3 328.35 m .3 K/L35; (15) A82/3 311.3 m .2 O5/2; (16) U5 125.1 m .2 R34/3; (17) A82/3 311.3 m .2 H40/4; (18) U5 151.3 m .2 Q/R29.

Figure 5

Figure 6 Photographs of Roper organic-walled microfossils: (1–15) Tappania plana: arrow in (1) showing furcating process, arrows in (2–4) showing septae in processes, (3) showing details from specimen in (2), arrow in (11) showing the area of locally grouped small processes shown in (12), arrow in (15) shows open neck-like expansion, suggesting excystment structure. (16) Tortunema sp. (17, 18) Trachytrichoides sp.: (18) showing details of cells morphology in filaments in (17). Scale bar in (1) is: (1, 2) 40 µm; (3, 11) 10 µm; (4, 8, 14) 20 µm; (5, 9, 16, 17) 30 µm; (6, 10, 12, 15, 18) 15 µm; (7) 27 µm; (13) 25 µm. Slide and England finder coordinates: (1) GG1 340.2 m .3 B X36/2, (2, 3) GG1 340.2 m .2 A J47/2, (4) GG1 340.2 m .3B T40/2, (5) GG1 340.2 m .2A E28/4, (6) U5 151.3 m .2 Q28/3, (7) GG1 326.2 m .2 V33/1, (8) U5 151.3 m .2 Y14/2, (9) GG1 340.2 m .3 H26/2, (10) GG1 326.2 m .3 F39/1, (11, 12) GG1 340.2 m .2 E17/1, (13) GG1 326.2 m .2 Y28/4, (14) GG1 340.2 m .3 O19/1, (15) U5 130.5 m .2 U9, (16) A82/3 379.1M G57/0, and (17) U6 240.2 m .2B J34/1.

Figure 6

Figure 7 Photographs of Roper organic-walled microfossils: (1–4) Valeria lophostriata: (1) showing half enrolled vesicle following medial split, (2) showing start of medial split, (3, 4) showing wall ornamentation by characteristic concentric striations. (5, 6) Unnamed form A, large compartmentalized colonial forms. (7, 8) Unnamed form B, opaque spheromorph, (8) showing details of folds at periphery. (9) Unnamed form C, spheromorphs connected by a filamentous expansion. (10) Unnamed form D, spheromorph with a filamentous expansion. (11) Unnamed form E, large smooth thick brittle spheromorph. (12) Unnamed form F, large filament in indented sheath. Scale bar in (1) is: (1) 100 µm, (2, 4, 8) 25 µm, (3) 10 µm, (5) 70 µm, (6) 120 µm, (7) 45 µm, (9) 18 µm, (10, 15) 30 µm, (11) 80 µm, and (12) 55 µm. Slide and England finder coordinates: (1) U6 305.1 m .2A S41, (2) U6 230.8 m .2 N27/2, (4) U6 233.6 B45/0, (5) U6 305.1 m .2A O/N39, (6) U6 305.1 m B45/1, (7) GG1 340.2 m .3B U30, (9) U5 125.1 m .2 M41/3, (10) GG1 326.2 m .2 E20/1, (11) U6 240.2 m .2U27/2, (12) U5 436.7 m .2 S51.

Figure 7

Figure 8 Paleoecological distribution of selected microfossils in the Roper Group.

Figure 8

Figure 9 Comparison of Roper age with molecular clock estimates for the divergences of crown group green algae, photosynthetic eukaryotes, and crown group eukaryotes. Circle, diamond and triangles are the mean ages for the origin of crown group algae, plastid, crown group eukaryotes, respectively, and the dark gray, medium gray and white rectangles represent the errors on estimates, respectively.

Figure 9

Figure 10 Biological innovations in early eukaryotes inferred from preserved microfossils (modified from Javaux, 2011).