Microfossil populations in the context of synsedimentary micrite deposition and acicular carbonate precipitation: Mesoproterozoic Gaoyuzhuang Formation, China

Precambrian Research 96 (1999) 183–208

Microfossil populations in the context of synsedimentary micrite deposition and acicular carbonate precipitation: Mesoproterozoic Gaoyuzhuang Formation, China L. Seong-Joo, S. Golubic * Biological Research Building, Boston University, Boston MA 02215, USA Received 6 July 1998; accepted 14 January 1999

Abstract Silicified stratiform stromatolites of the Mesoproterozoic Gaoyuzhuang Formation (1.4–1.5 Ga), China, contain well-preserved microfossils. The cherts also harbor varied synsedimentary precipitates and void-filling cements, replaced by early diagenetic silica minerals. These precipitates disclose microenvironments characterized by supersaturated solutions in protected, shallow depressions within an intertidal setting. The precipitates provided surfaces for selective microbial settlement, and rigid sediment matrix for microbial growth. Together with early silicification, the frequent precipitation events contributed to preservation of microfossils by reducing sediment compaction and shearing. Fossiliferous cherts display fine, flat and wavy lamination, characterized by an alternation of highly silicified, thin organic-rich layers with thick sediment-rich layers. Organic-rich layers are dominated either by coccoid or by filamentous microfossils, whereas sediment-rich layers contain abundant synsedimentary precipitates, within which the microfossils are preserved in their growth position. Four dominant microfossils Coccostratus dispergens n. gen. et sp., Eoentophysalis belcherensis, Eoschizothrix composita and Siphonophycus inornatum occur contiguously through several tens of laminae, and are identified as main frame-building biological components of Gaoyuzhuang stromatolites. Community composition, microbial density, distribution, orientation and developmental patterns of the frame-building microfossils are closely correlated with the changing depositional events of Gaoyuzhuang cherts, contrasting conditions of sedimentary kinetics with those of sedimentary stasis. Each assemblage of frame-building microfossils responded to sedimentation with different mechanisms to escape burial. High sedimentation rates correlate with scattered colonies of coccoids and with loose webs of predominantly upright filaments. Low sedimentation rates correlate with dense, laterally connected colonies of coccoids and with a change in filament orientation from vertical to horizontal. In multi-trichomous microfossil Eoschizothrix composita, low sedimentation rates are also accompanied with an increase in number of trichomes per filament. The observed morphological variability of the frame-building microfossils is explained by microbial development, reproduction and behavior by interactions between sedimentological and biological controls. © 1999 Elsevier Science B.V. All rights reserved. Keywords: Carbonate cements; Coccostratus dispergens n. gen. et sp.; Gaoyuzhuang Formation; Mesoproterozoic; Microbial fossils; Microfossils; Precipitates; Stromatolites

* Corresponding author. Present address: Bremen University, Postfach 330 440, D-28334, Bremen, Germany E-mail address: [email protected] (S. Golubic) 0301-9268/99/$ – see front matter © 1999 Elsevier Science B.V. All rights reserved. PII: S0 3 0 1- 9 2 68 ( 9 9 ) 0 00 0 4 -2

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1. Introduction Proterozoic silicified microfossils are most commonly preserved in thin organic layers of cherty stromatolites as components of ancient microbial mats. Paleontological research on silicified microfossils during the past three decades has produced an impressive inventory of microbial fossil forms and taxa (e.g. Schopf, 1968; Schopf and Blacic, 1971; Knoll, 1982; Mendelson and Schopf, 1982; Allison and Awramik, 1989; Knoll et al., 1991; Schopf and Klein, 1992; Sergeev et al., 1995). Several studies focused attention on the relationships between fossil forms and their depositional environment, as evident from the spatial orientation and distribution of microfossils, as well as attendant petrological and sedimentological data (e.g. Knoll and Golubic, 1979; Knoll, 1982). Accordingly, it was possible to classify microfossils as autochthonous builders and dwellers of ancient mats, and allochthonous elements (mostly planktonic) that were buried and preserved within the mat. This approach laid the foundation for paleoecological reconstruction, relating the ancient microorganisms to their synsedimentary context. However, the effort was often limited by poor preservation of the studied materials, so that such reconstruction left unresolved the questions of biological interactions with the sedimentation process, and organismal behavioral responses to the changes in sedimentation. Fossiliferous Gaoyuzhuang cherts are characterized by repeated episodes of intensive mineral precipitation, which are expressed as light, thick sediment-rich layers separated by dark, thin organic-rich layers. The microbial density, distribution, orientation and developmental patterns of constituent microfossils are repeatedly correlated with these changing depositional events. By relating fossil assemblages to enclosing synsedimentary microfabrics, we may understand the factors that controlled the distribution and development of stromatolite-building microbes, and understand how microorganisms behaved under different sedimentation regimes in a changing environment. In this paper, we describe the response of resident microorganisms to changing depositional events, including occurrences of a variety of synsedimen-

tary precipitates preserved in silicified carbonates. Dominant microorganisms that persist through several cycles of the depositional process and, thus, contribute to stromatolite architecture, have been recognized as frame-builders of the Gaoyuzhuang stromatolites.

2. Geological setting and materials Thick continuous and essentially unmetamorphosed, clastic and carbonate sedimentary successions of the Proterozoic Era are well developed along the margins of the North China Platform [e.g. see Xiao et al. (1997), fig. 1]. Among the best known and most complete successions is the Jixian section, located on the northeastern margin of the North China Platform, about 100 km northeast of Beijing. The Proterozoic sedimentary succession in the Jixian region (ca 9000 m thick) includes three groups in the ascending order: Changcheng, Jixian and Qingbaikou. It rests unconformably on the Archean metamorphosed Qianxi Group, and is overlain disconformably by Lower Cambrian sediments [see Zhang (1986b) fig. 2 for generalized stratigraphic column of the Jixian section]. The succession is oriented from northeast to southwest, and is considered to have been deposited in an aulacogen, along the northern margin of the North China Platform (Qian et al., 1985; Wang and Qiao, 1987). Proterozoic successions developed on the northwestern edge of the aulacogen are exposed in the Pangjapu region, Hebei Province, about 115 km northwest of Beijing. The succession in this region is very similar to one in the Jixian area, although the succession shows significantly less thickness (ca 2000 m) and is incomplete. The Wumishan Formation is the only formation of the Jixian Group present in the Pangjapu region; the entire uppermost Qingbaikou Group is missing. This succession (including two groups, Changcheng and Jixian) overlies unconformably the Archean metamorphosed rocks and is unconformably overlain by much younger Jurassic non-marine sediments ( Fig. 1). The Changcheng Group includes five formations in the ascending order: Changzhougou, Chuanlinggou, Tuanshanzhi, Dahongyu, and

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Fig. 1. Geologic map and location of the research area in northern China. Stromatolitic cherts were collected along the profile A–B (modified from Zhang, 1986a).

Gaoyuzhuang, comprising a ca 1500 m succession of Paleo- to Meso-proterozoic sedimentary rocks. It is disconformably overlain by the Wumishan Formation of the Jixian Group. Radiometric ages of the Gaoyuzhuang Formation have been provided from the Jixian section by the Laboratory of Isotopic Geology, Kweiyang Institute of Geochemistry, Academic Sinica (Zhong, 1977), Tianjin Institute of Geology and Mineral Resources (Chen et al., 1980), and by Yu and Zhang (1985). Most radiometric data were obtained from Pb–Pb isotope analyses of galena, yielding an average age of 1434±50 Ma. Depositional ages of the Gaoyuzhuang Formation have also been broadly constrained by radiometric data on the underlying (e.g. Dahongyu Formation) and overlying formations (e.g. Tieling Formation) in the Jixian region. The underlying Dahongyu Formation has been reliably dated by several methods in the range of 1620–1680 Ma, i.e. by the K– Ar method at 1621, 1643, and 1678 Ma (Zhong, 1977), by the U–Pb zircon method of extrusive trachytes at 1625±6 Ma (Lu and Li, 1991), and by a zircon Pb–Pb evaporation age of 1617±3 Ma (Cuvellier, 1992), which serve as the maximum age limit of the Gaoyuzhuang Formation. Its minimum

age limit is less constrained since there are no absolute radiometric data on the overlying Wumishan Formation. However, the upper age limit could be constrained by the overlying Hongshuizhuang Formation ( K–Ar ages at 1237 Ma; Xing et al., 1989), and the Tieling Formation [ K–Ar ages of glauconites at about 1185±50 Ma; Chen et al., 1980; Ar–Ar ages of glauconites at 1082±26 and 1171±22 Ma (Li, 1993)] of the Jixian Group. On the basis of the available radiometric data mentioned above and the stratigraphic position of the Gaoyuzhuang Formation in the Pangjapu region, the Gaoyuzhuang Formation is generally believed to have been deposited during the Mesoproterozoic Era at approximately 1500–1400 Ma. The Gaoyuzhuang Formation, divided into six members, comprises a thick succession (ca 900 m) of dolostones, dolomitic shales, siltstones, and manganiferous dolostones [see Zhang (1981,1986a) for lithology in details]. The first and second members (ca 200 m in thickness), which are the subject of the current study, contain laminated cherty dolostones with distinctive domal to columnar stromatolites developed above fossiliferous chert layers ( Fig. 2). A 10 to 20 m thick key bed

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Fig. 2. Stratigraphic column with detailed sampling section. Chert horizons are prefixed by ‘Gb’ and numbered; additional numbers identify individual rock samples. Arrows point to fossiliferous chert horizons.

of manganiferous dolostones marks the top of the second member of the Gaoyuzhuang Formation. Stromatolitic cherts occur as a few centimeter thick beds extending laterally up to several meters, or as isolated lenses, nodules or concretions within laminated dolostones. They were collected systematically from the base of the formation to the end of the second member, about 200 m above the base. A total of 45 rock samples were obtained from 11 localities collected at intervals of about 20 m vertically. Three to five chert samples were collected from the same stratigraphic horizon at each locality. 120 petrographic thin sections were

prepared from 45 chert samples. Sampling localities and the stratigraphic horizons of fossiliferous chert samples are shown in Fig. 2.

3. Fabrics Most cherts collected contain some microfossils, but those from two stratigraphic levels (Gb3 and 9), about 100 m apart from each other, exhibit considerable concentrations of in-situ-preserved assemblages of microfossils associated with synsedimentary fabrics ( Fig. 2, arrows). They are

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located in the middle of the first member (about 50 m from the base) and at the top of the second member (about 170 m from the base). General features of the studied fossiliferous cherts are similar to other Proterozoic silicified carbonates described in the literature. They consist of a flat to wavy fine lamination of alternating thin organicrich and thick sediment-rich layers. The organicrich layers contain prostrate microbial mats (20– 100 mm, up to 500 mm in thickness) composed of dense populations of coccoid and filamentous microfossils. These organic-rich layers are overlain by thicker sediment-rich layers (0.2–2.7 mm in thickness), containing various amounts of syndepositional precipitates (e.g. crystal fans) and voidfilling cements. The boundaries between light and dark laminae are often gradational. Each of the compared horizons (Gb3 and 9) is characterized by different microfabrics and by microfossil assemblages of different compositions. The cherts from the lower horizons (Gb3) display less silicified, and more dolomitized fabrics. Lamination is characterized by an alternation of highly silicified, irregularly crenulated, thin organic-rich layers with less-silicified, thick, organic-poor, dolosparite layers. Organic-rich layers are dominated by colonies of the coccoid Eoentophysalis belcherensis forming almost monospecific microbial mats, with only a few filamentous microfossils present. These layers show various degrees of post-depositional distortion and compaction. They are largely devoid of precipitated structures. The cherts from upper horizons (Gb9) display well-laminated and highly silicified fabrics with various synsedimentary precipitates and void-filling cements ( Fig. 3). Organic-rich layers are dominated either by coccoid or by filamentous microfossils. Three dominant microfossils, the coccoid Coccostratus dispergens n. gen. et sp., and the filamentous Eoschizothrix composita and Siphonophycus inornatum occur in different mat horizons within 15 mm of vertical distance in the same thin section. This dominance is repeated through several laminae. One dominant taxon may replace another gradually, or abruptly. Sedimentrich layers contain abundant synsedimentary precipitates (now silicified). Within these sediment-

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rich layers, the microfossils are preserved in growth position, without compaction. The cherts are composed mainly of microcrystalline quartz with minor components of megaquartz and length-fast fibrous chalcedony. Late diagenetic carbonate minerals (<30% in volume) occur as euhedral rhombohedra of dolomite, large masses of dolomite aggregates, and as large, fracture-filling calcite crystals. The chert matrix consists predominantly of microcrystalline quartz (1– 20 mm in size) both in organic- and sediment-rich layers, whereas fibrous chalcedony and megaquartz (20–100, up to 500 mm) are developed sporadically as isolated clusters, or as void-filling cements. Dolomite is present either as isolated patches of interlocking crystal mosaics or as single rhombohedra. Euhedral dolomite crystals (10– 200 mm) are scattered randomly throughout the fine-grained microquartz chert matrix. Some dolomite rhombohedra cut across crystal boundaries of chalcedonic or microquartz crystals and fabrics. Most rhombohedra preserved within the silica show no traces of corrosion, suggesting a late diagenetic origin. Isolated patches of dolomite aggregates consist of interlocking anhedra. Aggregates of hypidiotopic to xenotopic dolomite crystals may form coarse laminae immediately above silicified, organic-rich layers. These carbonate laminae are fabric-destructive, leaving no evidence of microfossils or any former depositional textures.

4. Synsedimentary precipitates Gaoyuzhuang cherts preserve evidence of abundant synsedimentary precipitates, which contributed directly to the construction of stromatolites. Episodes of intensive mineral precipitation are expressed as distinct, light, organic-poor horizons separated by dark organic-rich layers. Microfossils occur interspersed throughout these mineral-rich layers, however, at much lower densities and often differently grouped and oriented than in intervening organic-rich layers. There is no evidence of clastic carbonate or quartz grains, reworked microbial mats or other intraclasts. These observations indicate quiescent deposition at high mineral saturation levels of ambient waters. The stratiform

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Fig. 3. Silicified stromatolitic fabric of Gaoyuzhuang chert. Well-developed upward radiating precipitates are in the center, connected laterally with areas dominated by micritic matrix with minor precipitate inclusions. Thin, dark organic-rich layers, arching over larger precipitate fans, represent synoptic profiles. Scale bar is 2 mm.

cherty stromatolites of the Gaoyuzhuang Formation are, therefore, best interpreted as precipitated stromatolites, deposited in protected, shallow depressions within intertidal to supratidal environments. Synsedimentary precipitates are easily identifiable in petrographic thin sections by their gross morphology, size and internal texture. They include single and upward stacked, radiating crystal fans, flat to wavy crustose coatings, radiating spheroids and botryoid clusters. Fibrous texture with intralamination is the most prominent microfabric property of the silicified precipitates. The fibers are straight, radiating from point sources commonly arranged in zones or intralaminae [Fig. 4(A)]. The intralamination is an internal zonation of crystals superimposed on the radiating

texture, consisting of fine pigmented lines separated by thicker clear zones. They are expressed by different intensity in coloration of the containing fibers, which run perpendicular to the laminae [Fig. 4(B)]. Interpenetration of fibers occurs at the points of competing crystal growth at the intersection of two upward convex laminar curvatures [Fig. 4(B), arrow]. The intralaminae are isopachous, they run evenly, maintain their thickness laterally and show a high degree of upward inheritance [Fig. 4(C )]. This intralaminar zonation of crystals should not be confused with stromatolite laminae. Crystal intralaminae are variable in thickness, orders of magnitude finer, and denser (10– 40 mm, mean±standard deviation: 17.2±9.0 mm, n=160) than the stromatolitic lamination of organic-rich and sediment-rich layers (0.2–2.7 mm,

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Fig. 4. Internal fabrics of Gaoyuzhuang precipitates. (A) Arrangement of upward flattening fibrous intralaminae. (B) Growth competition of acicular crystals illustrated by interference and interpenetration of fibers (arrow). (C ) Adjacent columnar fans with extremely fine intralamination. The intralaminae are bent at the edges of the columns showing high upward inheritance. (D) Detail of lateral margin of a crystal fan showing textural difference between the precipitate ( left) and the surrounding matrix (right). ( E ) Another lateral margin with darkly pigmented contact. Scale bars are 100 mm in (A)–(C ), and 10 mm in (D) and (E ).

mean±standard deviation: 1.07±0.59 mm, n= 89). The matrix surrounding precipitates contains scattered organic remains, but does not have any definite texture. It is assumed that it originally consisted of fine, detrital carbonates, possibly derived from whiting micrite precipitated in the water column. The contacts between precipitates and the surrounding matrix are sharp with darker pigmented outlines. Lobed to bluntly serrated margins identify bundles of crystal fibers with compet-

ing epitaxial growth, underlining textural differences between precipitate and the matrix [Fig. 4(D)], often accompanied by compressed pigmented matter [Fig. 4( E )]. The precursor minerals of the precipitates, which are presently permeated and replaced by silica minerals, retain relic original outlines of former acicular crystals. They are most directly comparable with modern spherulitic or botryoidal aragonite cements (Ginsburg and James, 1976; Grammer et al., 1993; Verrecchia et al., 1995), and

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laminated carbonate crusts (Handford et al., 1984). Such laminated fibrous fabrics are almost identical with those of ‘ministromatolites’ described in detail by Hofmann and Jackson (1987), and of similar Precambrian precipitated structures (Grotzinger and Read, 1983; Grotzinger and Knoll, 1995; Kah and Knoll, 1996; Sami and James, 1996; Xiao et al., 1997). They are also comparable with cements occurring in Phanerozoic carbonates (Savard et al., 1996). The abiotic nature of similar radiating fans has been convincingly argued on the basis of observed crystal truncation (Grotzinger and Read, 1983; Xiao et al., 1997), interpenetration of adjacent fibrous crystals (Horodyski, 1975; Hofmann and Jackson, 1987; Xiao et al., 1997) and their angular cross-sections (Hofmann and Jackson, 1987). The extremely fine and even intralamination (color zonation) superimposed over radiating crystal fans is also a distinguishing feature of precipitated structures. Biological origins of similar structures as remains of bacteria, calcified algae or cyanobacterial sheaths have also been proposed (e.g. Hofmann, 1969; Bertrand-Sarfati, 1976; Walter and Awramik, 1979; Liang et al., 1984; Lanier, 1986). The radiating fibrous fabrics observed in Gaoyuzhuang cherts are consistent with an interpretation as abiotic carbonate precipitates, leaving open the possibility that nucleation of these crystals may have involved microorganisms or microbial products (see Section 4.4). Although scattered remains of coccoid and filamentous microfossils are incorporated within the radiating fan structures, there is little or no evidence for any impact on crystal growth. 4.1. Upward radiating crystal fans The most distinctive features among the Gaoyuzhuang precipitates are upward radiating crystal fans (Fig. 5). These fans occur as single, laterally joined or vertically stacked concretions, each about 1–1.5 mm wide and 1.5–2.7 mm high. The radiating fibers originate from point sources at the base of each fan spreading in straight lines upward and outward, whereas the intralaminae are displayed as a series of concentric, upward convex arches with a high inheritance. The upper

surfaces of fans are commonly coated with mats of coccoid microfossils, but the interiors are virtually fossil-free [Fig. 5(B)]. When vertically stacked, the fans produce composite columns, in which successive segments are commonly separated by a thin layer of coccoids (2–8 mm in diameter) that settled along thin micritic laminae [Fig. 5(A), arrow]. These coccoid settlements mark episodic interruptions in the precipitation process, accentuating the discontinuities in the growth of crystal fans. When precipitation resumed, coccoids were sealed at the bases of the next generation of fans. Fig. 5(A) illustrates a series of synoptic profiles with upward increasing topographic highs associated with crystal fans. This shows that precipitates accrete consistently at higher rates relative to the accumulation rates of micritic sediment to the left. The difference in the nature of the substrates (hard versus soft) correlates precisely with the settled microbiota, dominated by coccoid microfossils on the fans and by filamentous ones over the loose micritic matrix. Similar fans from Gaoyuzhuang cherts were described as ‘microstromatolites’ in an earlier study, and the coccoid microfossils in the fans were classified as Nanococcus vulgaris (Zhang et al., 1995; plate 4, fig. 4). Occurrences of coccoid microfossils along thin micritic laminae within such structures have led to conclusions that bacterial activity must have been involved in their formation (Lanier, 1986, 1988). However, the relationships observed in Gaoyuzhuang cherts, which show the same pattern [cf. Lanier (1988), fig. 8], indicate that the coccoids colonized the crystal surfaces after the fans were already formed, leaving the growth zones inside radiating fans virtually free of microfossils. Whether the colonized microfossils were involved in nucleation of the next level of fans above could not be determined. 4.2. Flat crustose coatings Microbial mats are sometimes coated with thin, sheet-like mineral crusts ( Fig. 6). These precipitates evenly encrust irregular sediment topography, draping over any relief in the underlying substrates. The internal fabric of these crusts is identical to those of other precipitates, but less divergent. The

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Fig. 5. Upward radiating crystal fans. (A) A stack of fan-shaped precipitates separated by thin layers of coccoid microfossils (arrow). The micritic matrix to the left contains multi-layered mats rich in filamentous microfossils. Note the synoptic profiles increasingly bending upwards to accommodate high precipitation rates of the fans. (B) A large upward radiating single fan with characteristic intralaminated fabric. The growth of the fan is capped by a dense coating of coccoid microfossils. Scale bars are 1 mm in (A), 100 mm in (B).

Fig. 6. Crustose coatings over microbial mats of coccoid microfossils. (A) Contiguous finely intralaminated crust over a layer of several spherulitic precipitates. (B) Regular finely intralaminated crust. Both crusts overlay microbial mats (below), and develop into a series of crystal fans (above). Scale bars are 100 mm.

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fibrous crystals are oriented more or less perpendicular to the substrate, rarely subdivided in upward diverging and interfering fiber clusters. Intralamination is extremely fine and laterally contiguous up to several millimeters [Fig. 6(A)]. Upward doming of the crust is locally favored, producing divergent fiber radiation like that observed in the fans. However, the overall tendency in the upward growth of the crust is in dampening of the irregularities. Fiber divergence and bending of intralaminae characterize only the margins of the crustal sections [Fig. 6(A) and (B)]. These coatings were observed to nucleate preferentially above the organic-rich laminae, and to originate from a large number of point sources [Fig. 6(A)]. There is no evidence of coccoid settlement on these crusts, indicating that they are brief episodes at the onset of high precipitation periods. They are commonly found beneath fans and other precipitates [Figs. 5(B) and 6(B)].

4.3. Spherulites and botryoids Precipitates of spheroidal shape with fibers radiating in all directions are found abundantly in the light stromatolitic laminae, either as isolated units or agglomerated in botryoid clusters. They range from 30 to 500 mm in diameter ( Fig. 7). The internal texture of spheroids and botryoids is the same as in the upward radiating fans and crustose coatings. However, they appear clearer, their intralamination is less pronounced and concentrically arranged, and they often contain characteristically shaped nuclei in their centers [Figs. 7(A) and 8). There is no evidence of cessation in crystal growth with intermittent settlement of coccoid microfossils as in the upward radiating fans. These observations suggest that the precipitation in spheroids advanced rapidly from nucleation centers located within sediments. The initial crystal growth was radial in all directions (including downward ), however; upward growth became favored in later stages, resulting in a domal fan morphology (Fig. 7). The presence of several small spheroids (ca 30 mm in size) was often detected at the bases of upward radiating fans [Fig. 5(B)] and crusts [Fig. 6(A)], indicating that spheroids and

Fig. 7. Spherulitic and botryoid precipitates. (A) A large spherulite developing from a central nucleation site into an upward radiating fan. The precipitate is free of microfossils but the surrounding matrix contains numerous upright Siphonophycus inornatum filaments. (B) Two botryoid clusters between two microbial mats composed of Coccostratus dispergens n.gen. et sp. Scale bars are 100 mm in (A), and 50 mm in (B).

botryoids represent early stages in the formation of fans and other forms of precipitates. 4.4. Nucleation of synsedimentary precipitates Crystal fans nucleated from distinct locations on the mat surfaces, from where they expanded

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Fig. 8. Nucleation centers in spheroid and botryoid clusters. (A) Several dark dumbbell-shaped crystal nuclei in the center of a botryoid cluster. (B) Detail of (A). The nuclei range from small dark granules (arrow) to dumbbell-shaped bursts and paired hemispheroids surrounded by halos (upper left). Late diagenetic dolomite crystals partially destroy the nuclei, same as in (H ). (C ) A crystallization nucleus in the shape of a radiating four-leaf rosette. Note the continuously radiating crystal fabric surrounding the nucleus. (D)–(I ) Development stages of dumbbell-shaped nuclei. (J ) A paired spheroid nucleus mimicking a dividing cell, surrounded by radiating fabric with multiple halos. Scale bar in (J ) is 100 mm for (A), and 10 mm for (B)–(J ).

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upward and outward as they grew. Nucleation centers are well developed inside spheroids and botryoid clusters beneath them, where they can be studied in detail ( Fig. 8). Several minute structures (5–15 mm across), quite distinct in shape, color and texture could be identified as actual crystallization nuclei [Fig. 8(A)]. They are distinguished as crystalline grains, rods, dumbbells, and paired hemispheres at the origins of radiating fibers. The color of these nuclei is darker than the surrounding matter, emphasizing their radial fibrous texture, and/or forming concentric halos around them [Fig. 8(B), upper left]. The simplest shapes are round to slightly elongated dark granules [Fig. 8(B), arrow and Fig. 8(D)], and small rods [Fig. 8( E )]. The more complex and the most common nuclei are dumbbell-shaped, composed of a short shaft with two opposing bursts of radiating fibers [Fig. 8(F )–(I )]. Paired hemispheres originate from the dumbbells by widening the radiation angle of fibers at both ends of the connecting shaft [Fig. 8(B) and (J )]. Nuclei of four-leaf rosettes form sometimes by intersecting two perpendicular dumbbells [Fig. 8(C )]. Radial microfabric emanating from these nuclei appears to be in optical continuity with the surrounding crystalline texture [Fig. 8(C ) and (J )], suggesting that they are indeed the organizational source of the subsequent progressive precipitation process that eventually formed crusts, botryoids and crystal fans. The observed Gaoyuzhuang nuclei are small structures similar in shape and size to silicified coccoid microfossils. Paired hemispherical nuclei, for example [Fig. 8(J )], resemble two dividing coccoid cells when observed at low power. However, higher magnification and resolution reveals that they lack clearly defined boundaries, such as envelopes or wall-like outlines characteristic of coccoid microfossils. Instead, they possess an open monomineralic texture, evenly distributed and continuing outward through the entire concretion around them. The patterns observed are consistent with the laws of crystal growth [see Golubic et al. (1999)], and there is no evidence of cellular structures incorporated in the Gaoyuzhuang nuclei. Similar nucleation and initial crystallization patterns are known from modern marine and hydro-

thermal settings. Their formation and origins have been reported in association with bacterial growth and activity in hypersaline settings (Buczynski and Chafetz, 1991; Chafetz and Buczynski, 1992), in conjunction with thermal spring cyanobacterial mats ( Farmer and Des Marais, 1994), and in association with dissolved and particulate organic matter (Guo and Riding, 1992). Bacterial and abiotic origins of such unusual crystal formations have both been promoted and contested [e.g. Buczynski and Chafetz (1991) versus Pentecost and Terry (1988)]. Templating of mineral deposits by organic matrices occurs intra- and extra-cellularly in eukaryotic and prokaryotic organisms. It was found to be species specific in cyanobacteria (Golubic and Campbell, 1981; Merz, 1992). On the other hand, crystallization patterns quite similar to those observed in Gaoyuzhuang precipitates have also been produced experimentally in purely chemical systems (Garcia-Ruiz, 1985; Bella and Garcia-Ruiz, 1986, 1987). The findings of these latter authors do not preclude biogenic influences on water chemistry leading to precipitation in ancient or modern natural settings, nor a possible role of organisms or organic compounds in triggering crystal nucleation. They prove, however, that biogenic influences are not required for formation of such unusual crystal shapes. The presence of pigmented matter within Gaoyuzhuang crystal nuclei raises the possibility that organic matter may have been involved in determining the location and timing of crystal nucleation [see Guo and Riding (1992)]. Some dumbbell-shaped structures contain a dark granulated bridge that connects the two hemispheres of the dumbbells [e.g. Fig. 8(G)]. The texture is reminiscent of that discussed by Knoll et al. (1988) as produced by diagenetic granularization or condensation of organic matter. Solubilization and mobilization of pigmented matter may account for the coloration along fine crystal fibers, with precipitation pulses producing faint concentric halos that sometimes surround these nuclei [Fig. 8(B) and (J )]. 4.5. Original void-structures Porosity of the original sediment is another distinctive feature of Gaoyuzhuang stromatolites

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Fig. 9. Cement-filled voids of the primary sediment porosity. (A) Stromatolitic laminae with different frequencies of voids presently filled with silica cements. Larger voids are vaulted (dome-shaped). Inset: chalcedonic botryoids lining a cavity. (B) A smaller void under cross-polarized light showing centripetal growth of length-fast chalcedony crystals starting from a rim of microquartz. (C ) A different void filled centripetally and sequentially from microquartz to large megaquartz. Scale bar in (A) is 2 mm for (A) and 160 mm for the inset. Scale bar in (C ) is 100 mm for (B) and (C ).

documented by the frequency of fenestrae, particularly within sediment-rich laminae. They are presently filled with early diagenetic silica cements (Fig. 9). The voids are in horizons parallel to lamination so that some stromatolite sections display an alternation of organic-rich and fenestral laminae [Fig. 9(A)]. The fenestral fills appear mostly featureless and translucent under plain transmitted light, devoid of any textural content. Neither synsedimentary precipitates nor microfossils were found in these spaces. Some voids are laterally elongated, asymmetrical with a flat bottom and vaulted top. Others are irregular in shape, isodiametric or even vertically elongated. The void outlines do not disturb either the growth pattern of microfossils, or the adjacent precipitate fabrics. Few void structures are observed within the precipitates. The void-filling cements, as revealed in crosspolarized light, are composed mainly of two silica mineral phases: length-fast chalcedony and megaquartz. Chalcedonic cements occur as bundles of radiating fibers. Some voids are rimmed by hemi-

spheric botryoid chalcedony, giving way to megaquartz toward the centers [Fig. 9(A), inset]. Other voids are lined by microcrystalline quartz and filled internally by centripetally oriented chalcedonic fibers [Fig. 9(B)], or the crystal size increases rapidly from the microquartz lining towards randomly oriented megaquartz crystals in the center of the void [Fig. 9(C )], suggesting a typical paragenic sequence of silica cements [see Hendry and Trewin (1995) and Hattori et al. (1996)]. The majority of the voids appear to be of primary origin, possibly resulting from gas production from bacterial decomposition of organic matter. Those occurring within precipitates may have resulted from early dissolution of the original minerals. The lack of relic structures of carbonate minerals, and the frequent presence of chalcedonic rims lining the voids argue against silica replacement of carbonate cements [see Knoll and Golubic (1979)], and suggest that silica precipitated directly into open spaces of a porous deposit. The occurrence of different mineral phases in adjacent voids

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may indicate different rates of silica precipitation during early diagenesis: megaquartz reflecting a slow rate of precipitation relative to a faster precipitation of chalcedonic cements. Whether silica cementation in voids occurred before, concurrently or after early diagenetic replacement of carbonate seen elsewhere in the sections remains unclear. In any case, these void structures must have been cemented early, before they could have collapsed under pressure and compaction by additional sediments. Void structures of similar shapes and distributions are known from various Proterozoic tidal flat silicified sediments (Oehler, 1978; Lo, 1980; Mendelson and Schopf, 1982; Nyberg and Schopf, 1984). Similar environmental constraints are valid for the Gaoyuzhuang Formation. Voids and blisters are common in modern microbial mats in intertidal environments; they may form from gases produced by bacterial decomposition of organic matter (Logan, 1974; Horodyski et al., 1977; Stal et al., 1985; Gerdes et al., 1994; Wachendo¨rfer et al., 1994). A positive correlation between microbial activity and sediment porosity has been established by comparing the conditions in modern mats with those of adjacent loose sediment ( Wachendo¨rfer et al., 1994). The frequency and density of void structures associated with Gaoyuzhuang microbial mats (Gb3 and 9) is significantly higher than those occurring in almost mat-free samples (Gb4, 5 and 6). Gas accumulation tends to uplift the overlying microbial mat layers, forming characteristic small domes. The shapes and distribution of voids in silicified ancient stromatolites are consistent with observations in modern mats. The vaulting of the void ceiling is consistent with deformations caused by gas pressure underneath coherent mat fabrics, whereas vertical voids may indicate gas escape passages through loose, less coherent sediment [Fig. 9(A)]. These observations suggest that void frequency, i.e. the original porosity in Gaoyuzhuang sediments, and the organic richness of indigenous mats have their origins in microbial growth and activity. It is, therefore, conceivable that the original porosity of a number of other Precambrian stromatolites may be viewed as a measure of microbial participation in their formation.

5. Stromatolitic lamination, sedimentary kinetics and frame-building microfossils Gaoyuzhuang cherts preserve successions of laminated sediments. Within this setting, a lamina represents the thinnest recognizable unit layer deposited under essentially a uniform set of environmental conditions. Accordingly, generation of a laminated structure in the rock required iterative changes in environmental variables, including physical and chemical conditions during the sedimentation process. Each lamina, in this context, represents a single time interval of sedimentary kinetics (deposition), whereas a bounding surface between laminae represents a discontinuity in the sedimentation process, i.e. a period of sedimentary stasis (non-deposition). Repeated alternation of depositional events followed by sedimentary pauses or periods of low deposition rate resulted in the buildup of laminated sedimentary sequences. In shallow marine and intertidal environments, such as the Gaoyuzhuang setting where colonization of microorganisms and establishment of microbial mats on sediment surfaces is favored, the sedimentary discontinuity planes become accentuated and color-coded by the accumulated organic matter — producing a stromatolitic structure. The organisms that successfully cope with the changing sedimentary regimes evolve particular developmental and behavioral strategies to avoid burial and re-colonize the ever changing sedimentary surfaces. Periods of low sedimentation rates and sedimentary pauses (sedimentary stasis) offer the opportunity for uninhibited growth and differentiation of microbial mats, which is recognized in the fossil as organic-rich layers of stromatolites. In contrast, periods of high sedimentation rates (sedimentary kinetics) permit only highly motile pioneer species to overcome these unstable states, and to respond behaviorally to the changes in sedimentary conditions (Seong-Joo and Golubic, 1999). Organisms responsible for construction, differentiation and functional interactions within microbial mat ecosystems have been recognized as matbuilders, with minor autochthonous components termed mat-dwellers ( Knoll, 1982). However, the success of a microbiota in occupying environments

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L. Seong-Joo, S. Golubic / Precambrian Research 96 (1999) 183–208 Table 1 Frame-building taxa in cherts of Gaoyuzhuang Formationa Taxon

Size (mm)

Occurrence Lower horizon

Coccoid frame-builders: Eoentophysalis belcherensis Coccostratus dispergens Filamentous frame-builders: Siphonophycus inornatum Eoschizothrix composita

inner: outer:

2-5 2-6.5 (3.9±0.7)

A

2-8 (4.3±1.4) 2.5-7.5 (4.6±0.8) 5-14.5

R

Organization Upper horizon

A

Encapsulated colonial Dispersed colonial

A A

Uni-trichomous Multi-trichomous

a A =abundant; R=rare; size as range (mean±standard deviation).

of changing sedimentary conditions depends on particular pioneer species being able to overcome burial and persist. These organisms maintain biological continuity through the changes in the sedimentation process, and can be recognized in the fossil as structural frame-builders. Unlike matbuilders, they are not restricted to organic-rich layers, but extend continuously from one lamina to another. Four distinctive frame-building assemblages are recognized in the Gaoyuzhuang cherts: two are dominated by coccoid and two by filamentous microfossils ( Table 1). Coccoid frame-builders include dispersed and encapsulated colonial forms, whereas filamentous ones include multi- and unitrichomous filamentous fossil assemblages. Dominant taxa of these four indigenous assemblage types evolved different survivorship strategies in coping with the changes in sedimentary conditions. They exhibit different settlement preferences, modes of growth and development, reproductive strategies, and behavior. Behavioral responses of microorganisms to changing sedimentary conditions are expressed in the fossil record as different growth forms, and as changes in orientation of microfossils relative to sedimentary features. 5.1. Coccoid frame-builders The simplest type of frame-builder is exhibited by dispersed colonial coccoids described here formally as a new fossil taxon Coccostratus dispergens n. gen. et sp. [Fig. 10, see Systematic paleontology

(Section 7)]. Populations of this microorganism are found abundantly in the upper horizons of the second member (Gb9). The colonies are prostrate, forming coherent wavy, crenulated or mamillate mats over sedimentary surfaces. Wart-like protuberances identify areas of intensive growth and mat expansion [Fig. 10(A)]. These upward convex cellular protuberances are sometimes clear in the centers and appear hollow. The upper, lightexposed surfaces of Coccostratus mats are always darker pigmented, similar to those of Eoentophysalis mats. Individual cell units are conspicuously spheroid in shape, ranging from 2– 6 mm in diameter [Fig. 10(B) and (C )]. They often occur in pairs or are equatorially constricted, apparently preserved while in the process of division. The narrow size distribution of these cell units indicates regularity of cell division by binary fission. Following division, daughter cells remain clumped together forming colonies different in size and irregular in shape. Cell units remain individually outlined, often adhering to each other, but without formation of common envelopes. They disperse easily, so that free unicells are often found scattered between, or ‘floating’ above, coherent colonies [Fig. 10(C )]. Distribution, colonization and growth of Coccostratus dispergens follow closely the synsedimentary changes in Gaoyuzhuang paleoenvironments. Dense coherent coatings cover stable sedimentary surfaces, when the sedimentation rates are low, composing organic-rich laminae [Fig. 10(A)]. High sedimentation rates are accom-

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Fig. 10. Coccoid frame-builder Coccostratus dispergens n. gen. et sp. (A) Typical mamillate microbial mat. Note the three subsequent organic-rich layers with upward increase in biomass. (B) Detail of the upper surface of the colony with several clusters of spherical cellular units. (C ) Dispersed individual units along the surface of the colony. (D) Two Coccostratus mats connected by a scatter of smaller colonies. Note vertical protuberances of the lower mat. The upper mat is interrupted by the growth of a large crystal fan. (E ) Burial-escaping Coccostratus population. The lower cluster is covered by a layer of sediment, permitting only a narrow cell series to protrude upward and form another colony on top. Scale bar in (A) is 100 mm for (A), and 120 mm for (D). Scale bar in (C ) is 10 mm for (C ), 12 mm for (B), and 50 mm for (E ).

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panied by formation of smaller colonies and loose individual cell units scattered throughout the sediment-rich laminae [Fig. 10(D)]. The colonization process during this period appears to be broken down into several minor steps separated by fine sediment. These small colonies form distinct patterns of upward convex cellular nests. High sedimentation rates may disrupt colony formation completely, resulting in sediment-rich horizons virtually free of coccoid colonies ( Fig. 7). Under favorable conditions, however, these organisms successfully escape burial by forming vertically arranged cellular rows through thicker fossil-free sediment layers, linking buried colonies with the newly established ones above [Fig. 10( E )]. This illustrates a unique mode of escaping sediment burial. At the onset of sedimentary pause, the released individual cells initiate new colonies by rapid successive cell division, and isolated small colonies grow and fuse laterally into dense colonial microbial mats forming a new organic-rich layer. Contiguous strata are again reconstituted in the next higher organic-rich lamina. Extensive precipitation occurs sporadically both in sediment-rich and organic-rich laminae [Figs. 7 and 10(D)]. Rapid crystal growth is always disruptive to microbial growth. However, the surfaces of crystal fans are rapidly overgrown by new Coccostratus layers [Fig. 7(B)]. It is likely that the capacity to escape sediment burial, and the continuous growth of this organism were limited. This deficiency appears compensated by reproductive efficiency. The ability to persist through sedimentary changes by re-colonizing sedimentary surfaces characterizes this organism as a framebuilder. Encapsulated colonial coccoids are represented by Eoentophysalis belcherensis Hofmann (Fig. 11). They are found in cherts of the lower horizons of Gaoyuzhuang Formation (Gb3). The lamination here is characterized by alternation of highly silicified, irregularly crenulated, thin organic-rich layers with less-silicified, thick, organic-poor, dolosparite layers. Organic-rich laminae within this sequence vary considerably with respect to their organic content, as well as in sedimentary fabrics [Fig. 11(A)–(C )]. The organic-rich layers contain laterally disconnected, diverse colonies of

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Eoentophysalis, ranging from globular, radiating hemispherical, to mushroom-like colonies. Laterally continuous mats are rare. The colonies of Eoentophysalis belcherensis typically contain hierarchically encapsulated cellular units wrapped in common envelopes of several orders. Groups of two, four or up to many individual cell units are found side by side [Fig. 11(D)]. This colony architecture is determined by the mode of cell division combined with intermittent production of flexible exopolymer envelopes (Golubic and Hofmann, 1976; Hofmann, 1976). The upper, illuminated surfaces of Eoentophysalis colonies are mamillate and darker pigmented, their interiors are lighter, sometimes hollow, with cellular units often arranged in vertical or radiating rows. Prominent sedimentary fabrics (e.g. crystal fans) are rare in this facies. Accordingly, it is not easy to infer a behavioral response to sedimentation by relating Eoentophysalis colonies with sedimentary fabrics. Thin horizontal crust-like precipitates occasionally form rigid layers that confine the growth of Eoentophysalis colonies [Fig. 11(C )]. The crusts are here interpreted as sudden, episodic carbonate precipitation events that partially harden the mats, analogous to precipitation described for mamillate mats of modern Entophysalis (Golubic, 1983, 1985). The associated colonies are predominantly mushroom-shaped with narrow stalks and expanded heads, with the crust positioned at the level of the colony stalks. The growth of colonies responded to the confinement by the crust, modifying the polarity of cellular units and affecting the shape of the colonies. The arrangements of cellular units in the mushroom heads are not different from those in typical mamillate colonies; however, those in the stalks are vertically stretched, often surrounded by diffluent, less clearly defined envelopes [Fig. 11( E ) and ( F )]. Cell envelopes in the core of the narrow stalks appear dissolved, apparently promoting upward stretching of the colony and cell escape. Such behavioral responses occur independently and synchronously in a large number of colonies along the thin crust horizons, illustrating a peculiar escaping mode to a common burial event, which appears to be specific to Eoentophysalis. Compared with Coccostratus dispergens

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Fig. 11. Coccoid frame-builder Eoentophysalis belcherensis in different sedimentary contexts. (A)–(C ) Eoentophysalis colonies of different shapes and sizes are separated by sediment. (D) Detail of colony surface showing encapsulated cellular units darkly pigmented on the upper surface. ( E ) and (F ) Mushroom-shaped colonies illustrating cases of burial escape. Note upward elongation and dissolution of envelopes in the stalk regions. Scale bar in (A) is 100 mm. Scale bar in (C ) is 50 mm for (B) and (C ). Scale bar in (F ) is 10 mm for (D)–(F ).

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described above, Eoentophysalis belcherensis as a frame-builder is apparently less efficient in coping with sediment burial. Gaoyuzhuang Eoentophysalis colonies are commonly restricted to thin organicrich layers forming laterally discontinuous microbial mats. Repeated colony formation throughout sediment-rich layers, often seen in Coccostratus mats, is rarely observed in Eoentophysalis mats. Even a small amount of sediment influx or an episodic thin precipitate seems to have impaired or terminated colony development. Under these conditions, Eoentophysalis may have recolonized new sediment surfaces by inoccula brought in by tidal currents, as is the case with its modern counterpart Entophysalis (Golubic, 1985). 5.2. Filamentous frame-builders Avoidance of unfavorable environmental changes in modern settings, including sediment burial, is accomplished most effectively by microbial motility. Gliding motility, a property of linear cellular series called trichomes, is common among modern filamentous cyanobacteria. It may be temporary as a means of dissemination of short trichomes (hormogonia), or may be retained as a permanent trichome property. Production of exopolysaccharides is always associated with gliding motility, often constructing firm tubular sheaths around trichomes. Exopolymer sheaths mark the traces of gliding trichomes as they are left behind in the sediment. Consequently, their presence and orientation in the sediment are the most useful tool for interpretation of movements and behavioral responses of ancient microorganisms [e.g. see Knoll and Golubic (1992)]. Two types of frame-building filamentous microfossil construct microbial mats in the Gaoyuzhuang cherts: uni-trichomous filaments classified as Siphonophycus inornatum Zhang Yun, 1981, and multi-trichomous ones described as Eoschizothrix composita Seong-Joo et Golubic, 1998. Both are found in the upper horizons (Gb9) of the second member of the studied Gaoyuzhuang sequence. They occur often in the same thin section and show the same orientational and distributional patterns as related to organic-rich and sedimentrich stromatolitic laminae [e.g. Fig. 5(A), left].

201

In organic-rich layers, the filaments are predominantly horizontal, forming densely interwoven networks. The filaments change orientation in sediment-rich layers to vertical ( Fig. 12(A)). This change in orientation is correlated remarkably well, layer by layer, with changes in the sedimentary context. Extensive and rapid formation of precipitates in the sediment-rich layers creates obstacles to filament passage. Avoidance of such obstacles by upward gliding trichomes is evidenced by their preserved sheaths, which are confined to areas between precipitates [Fig. 12(B)]. These upright filaments return to horizontal orientation near the top of the sediment-rich layer, forming another prostrate microbial mat. In the case of multi-trichomous filaments, this orientational pattern is accompanied by the change in the number of trichomes per filament: single trichome filaments prevail in sediment-rich layers, whereas multiple trichome filaments in organic-rich layers (Seong-Joo and Golubic, 1998). The observed correlation of microfossil distribution and orientation with the sedimentary context follows causalities that can be interpreted as follows. Development of prostrate mats with considerable accumulation of organic matter is possible as long as sedimentation rates remain low (or during periods of sedimentary pauses), whereas high sedimentation rates, including mineral precipitation, tend to bury or encase microbial mats. Motile trichomes escape burial by gliding upward toward to the new sediment surface, leaving vertically oriented sheaths behind. Thus, changes in filament orientation in Gaoyuzhuang fossil assemblages reflect behavioral responses of microorganisms to burial by sediment. Dependence of trichome orientation and organization on sedimentation rates is best expressed in the multi-trichomous microfossil Eoschizothrix composita (Seong-Joo and Golubic, 1998). Multitrichomous fossils are distinguished from unitrichomous ones by developing cable-like packaging of one to several inner sheaths surrounded by a common outer sheath. Low sedimentation rates in organic rich-laminae support complex microfossil populations comprised of various sheath morphotypes, ranging from simple tubules, concentrically inserted tubules, to bundles of two,

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Fig. 12. Uni-trichomous filamentous frame builder Siphonophycus inornatum. (A) Filaments changing their orientation. (B) Filaments avoiding large precipitates. Scale bars are 100 mm.

three or up to six tubules enclosed within a common outer sheath. The number of trichomes per filament is gradually reduced as the filaments change their orientation to erect in the overlying sediment-rich laminae where single tubes predominate. The shift in morphotypes is again gradually reversed at the top of each sediment-rich layer, constituting a transition to the next higher organicrich layer. The observed behavioral patterns, as deduced from filament orientation and organization of the multi-trichomous fossils, correspond closely to those observed in modern microbial mats, and are comparable to behavioral responses of multitrichomous cyanobacteria Schizothrix and Microcoleus to sediment burial ( Whale and Walsby, 1984; Golubic and Browne, 1996; Noffke et al., 1997; Seong-Joo and Golubic, 1998; SeongJoo et al., 1999). Full development of multitrichomous organization in modern (as in ancient microorganisms) requires time, so that their abundance, as well as increased number of trichomes per filament, reflect the duration of a sedimentary

pause or stasis. Only simple sheaths are produced and left behind when trichomes are forced to escape burial during high sedimentation rates. Alternations in fossil filament orientation have often been interpreted as a phototactic response of ancient trichomes exhibiting solar cyclicity ( Zhang, 1986a; Cao, 1991). These interpretations used modern cyanobacterium Phormidium hendersonii Howe as a model. In domal, laminated organic cushions of Phormidium hendersonii, the change in trichome orientation does not depend on sedimentation (Monty, 1976, 1979; Golubic et al., in press). The alternation of prostrate and erect filament orientation is a regular, autonomous phototactic response of gliding trichomes following a nocti-diurnal rhythm. Distribution of incorporated sediment particles within the structure is dictated by the microbial growth patterns: sediment particles accumulate by night when the trichomes are dormant; they become spaced by day, ‘diluted’ by active upright trichome growth and movement (Golubic and Focke, 1978). However, the changes in filament orientation

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observed in Gaoyuzhuang cherts, although superficially similar, cannot be explained using the Phormidium hendersonii model. In Gaoyuzhuang paleoenvironments, the conditions are reversed. The growth pattern of microorganisms responded and followed the changes in sedimentary regime: prostrate orientation of Gaoyuzhuang filaments correlates with low sedimentation rates, whereas the erect positioning of filaments correlates with high sedimentation rates because it is always found within thick sediment-rich layers.

6. Discussion A widely accepted definition of stromatolites as biosedimentary structures formed by microbial sediment trapping, binding, and/or mineral precipitation [Awramik and Margulis, cited in Walter (1976)] implies that microorganisms play an active role in stromatolite formation (or even control it). Such claims are difficult to document and verify in ancient stromatolites even if the presence of organisms within stromatolitic structures is established. If, however, a stromatolite is simply viewed as a laminated rock, its genesis may involve any organic or inorganic rhythmic depositional change. Such rhythms may be introduced by alternating physico-chemical or biological changes in the water column, the evidence of which was deposited in the sediment. Microfossils, if preserved in the sediment, are in that case allochthonous elements. Accordingly, their interpretational value in reconstructing paleoecological conditions during stromatolite genesis is limited. However, whenever chemical and biological processes operated in ancient benthic environments, as is the case with Gaoyuzhuang stromatolites, the microfossils preserved in situ represent the autochthonous microbiota, and their synsedimentary context reflects the properties of the immediate paleoenvironment in which they lived. Gaoyuzhuang stromatolitic structures were deposited in peritidal paleoenvironments, exhibiting evidence of frequent cyclic changes in water chemistry and sedimentation [see Walter et al. (1992)]. Sediment-rich laminae abound with

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almost pure mineral precipitates, including stacked upward radiating and intralaminated fans. Similar structures have been termed microstromatolites (Hofmann, 1969), ministromatolites ( Edhorn and Anderson, 1977), microdigitate stromatolites (Grotzinger and Read, 1983), and asperiform stromatolites (Grey and Thorn, 1985). This similarity extends at a much larger size scale to early Proterozoic rhythmic cements [e.g. see Grotzinger and Knoll (1995)]. It is conceivable that, under conditions with frequent precipitation events, as during the formation of Gaoyuzhuang stromatolites, the sedimentation process alone would have generated laminated structures [see Grotzinger (1990, 1994)]. However, in the case of Gaoyuzhuang stromatolites, the precipitation events were regularly punctuated by intermittent microbial growth. The indigenous precipitates formed instant hard substrates favored by ancient coccoids as settlement surfaces, whereas loose micritic grounds between precipitates became preferentially colonized by filamentous mat-forming microorganisms. In this way, different sedimentation processes influenced horizontal, substrate-related differentiation of microbial communities. Sedimentation processes imposed selective pressure on microorganismal growth, to which the microorganisms responded with different degrees of success, employing different behavioral strategies. The interplay between sedimentary processes and microbial growth followed reciprocal rhythms: low sedimentation rates permitted copious microbial growth with biological diversification, whereas high sedimentation rates suppressed microbial growth and challenged their survivorship strategies. Thus, the degree of success of microbial growth observed in Gaoyuzhuang stromatolitic cherts provides a measure for estimating the timing and rates of the associated sedimentary processes. In addition to accentuating discontinuities in the sedimentation process, Gaoyuzhuang microbial mats also bestow specific morphological properties to organic-rich laminae. These include dark pigmentation, growth protuberances, laminar waviness, lowered inheritance in superimposed laminar sequences, and other irregularities that distinguish

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biological structures from the physico-chemically constrained mineral morphologies. Sediment-rich and organic-rich laminae influence preservation of stromatolites differently. Organic-rich laminae are more prone to shearing and compactional deformations. However they are also preferred areas of early silicification which preserves microfossils [see Knoll (1985)]. Precipitates in sediment-rich laminae form an early, rigid support, resisting post-depositional shearing and compaction. When combined with early silicification, their presence favors preservation of entire microbial populations in their original spatial relationships. The case of Gaoyuzhuang cherty stromatolites illustrates advantages in studying in situ preserved microorganisms within their biological and synsedimentary contexts.

7. Systematic paleontology All fossil specimens illustrated in this paper are in oriented petrographic thin sections of Gaoyuzhuang cherts. Populations of the four dominant, frame-building assemblages were evaluated in terms of their variability derived from developments in the course of their life cycles and behavioral responses to environmental changes, as well as consequences of post-mortem degradation and post-depositional diagenesis. The treatment of these taxa is, therefore, approaching the criteria used in the study of modern microbial communities, which makes Recent-to-fossil comparisons more meaningful. Coccostratus dispergens is here formally described as a new fossil genus and species. The coordinates (x, y) refer to distances (in millimeters) from a referenced corner marked on the lower right of each thin section. Type materials and thin sections are deposited at the Biological Science Center, Boston University. Systematic descriptions for other dominant, frame-building taxa have been published elsewhere: Eoentophysalis belcherensis in Hofmann (1976); Siphonophycus inornatum in Knoll et al. (1991), and Eoschizothrix composita in Seong-Joo and Golubic (1998). Microfossils associated with assemblages dominated by these

frame-building Table 2. Domain Phylum Class Order Family Genus

microorganisms

are

listed

in

Bacteria Woese, Kandler and Wheelis, 1990 Cyanobacteria Stanier, 1977 Coccogoneae Thuret, 1875 Chroococcales Wettstein, 1924 Chroococcaceae Na¨geli, 1849 Coccostratus n. gen.

Type species Coccostratus dispergens n. sp. Diagnosis. Spheroid cell-like units forming layered colonies different in size. Colonies are irregular in shape, composed of individual spheroids that are clumped together without common envelopes. Laterally fused colonies form flat to wavy mats with billowy to mamillate, darkly pigmented upper surfaces. Individual cell-like units divide by binary fission starting with equatorial constriction that results in two attached spheroids. They disperse easily, so that free unicells or isolated small colonies are often found scattered between or above coherent colonies. Etymology. With reference to the conspicuous spherical shape and stratified distribution. Coccostratus dispergens n. sp. Fig. 10. Diagnosis. As for the genus. The species is characterized by cells, 2–6.5 mm in diameter (mean±standard deviation: 3.9±0.73; n=271). Etymology. With reference to the habit of easy dispersal of individual cells after reproduction. Type locality. Upper horizon (about 170 m above the base) of second member of Gaoyuzhuang Formation, located near the area of Pangjapu iron mine of Hebei Province, about 115 km northwest of Beijing, northern China. Type specimen. The population illustrated in Fig. 10(C ) is designated as type for this species; slide number Gb9-31, coordinates 21.2×13.4. Description. Individual cell-like units are conspicuously spheroid in shape. They occur often in pairs or are equatorially constricted, apparently preserved while in the process of division. Cell units remain individually outlined, tightly spaced, often adhering to each other within a colony, but maintaining their sphericity. Free unicells or loosely spaced small colonies are often found scattered above the mat, and sporadically in sediment-rich layers. Discussion. The populations of Coccostratus

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L. Seong-Joo, S. Golubic / Precambrian Research 96 (1999) 183–208 Table 2 Gaoyuzhuang taxa associated with frame-building microfossil assemblagesa Associated taxa

Coccoid microfossils: Archaeoellipsoides obesus Archaeoellipsoides sp. Clonophycus sp. Eoaphanocapsa sp. Eosynechococcus moorei Eosynechococcus brevis Myxococcoides grandis Myxococcoides cf. distola Myxococcoides sp. Palaeoanacystis sp. Sphaerophycus parvum Sphaerophycus sp. Tetraphycus sp. Filamentous microfossils: Siphonophycus robustum Siphonophycus kestron Siphonophycus capitaneum Oscillatoriopsis obtusa Oscillatoriopsis cf. amadeus Oscillatoriopsis sp. Palaeolyngbya barghoorniana Palaeolyngbya maxima Saccolyngbya qingshanensis Saccolyngbya sp. Cephalophytarion sp. Cyanonema sp. Veteronostocale sp.

Assemblages Eoentophysalis belcherensis

Coccostratus dispergens

Siphonophycus inornatum

Eoschizothrix composita

+ + +++ +++ ++ + +++ ++ + +++ ++ ++ ++

++ +

+ +

+

+

+ +

+ ++

+

+

+

+

+

+ +

+ +

+++ ++ + + + + ++ +

++ +

++ + +

+

+ + + +

+ + +

+ +

+ +

a Relative abundances are marked by +++ (abundant), ++ (common), and + (rare).

dispergens occur abundantly in the samples from upper horizons (Gb9), together with filamentous frame-building assemblages (e.g. Siphonophycus inornatum). It is evident that this taxon played a role in the construction of microbial mats, and possessed a capability to escape sediment burial by copious growth and cell dispersal. Genus Coccostratus describes colonial spheroids, abundant throughout organic as well as sediment-rich laminae in Gaoyuzhuang stromatolites, thus acting as a main frame-builder. Coccostratus is a benthic microorganism clearly distinguishable from other coccoid members of the Gaoyuzhuang assemblage that are considered to be either mat dwellers or allochthonous plankton elements buried in the

mat. Coccostratus mats are similar to those of Eoentophysalis belcherensis in microstructures and extracellular pigmentation on colony surfaces. It differs from Eoentophysalis belcherensis by the absence of distinct envelope encapsulation, reproduction, consequent colony formation and escaping mode to sediment burial. Like Eoentophysalis, the taxonomic affinity of Coccostratus is with coccoid cyanobacteria. Both taxa form microbial mats in intertidal settings and are protected from excessive illumination by extracellular lightinduced pigmentation, a phenomenon unique to cyanobacteria. The preservation sequences in both co-occurring paleotaxa are similar, so that the shape and organization of cellular units are repre-

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sented in the fossil by preserved envelopes. Collapsed remains of cells are occasionally preserved as granular inclusions within spheroid bodies. The persistent sphericity of Coccostratus is a property observed in modern marine Aphanocapsa species.

Acknowledgements We thank Dr Zhang Yun for guiding the field work and for enabling preparation of petrological thin sections, Dr J. Bertrand-Sarfati, Dr Andrew H. Knoll and Dr Malcolm Walter for critically reviewing the manuscript and valuable comments, and Dr Xiao Shuhai for helpful discussions on local geology. Field work was partially supported by a travel grant of Boston University.

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