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Radiation of Meso-Neoproterozoic and Early Cambrian protists inferred from the microfossil record of China
Palaeogeography, Palaeoclimatology, Palaeoecology 254 (2007) 350 – 361 www.elsevier.com/locate/palaeo
Radiation of Meso-Neoproterozoic and early Cambrian protists inferred from the microfossil record of China Yin Leiming ⁎, Yuan Xunlai Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China Accepted 5 March 2007
Abstract Marine protists can be affected by and reflect changes in the ecological environment. Based on available microfossil evidence from late Mesoproterozoic–Early Cambrian rocks of China, radiations of protists and related changes in ecological environments are discussed in the paper. Remarkable development of protists had occurred by as early as the Mesoproterozoic. Protist diversity significantly decreased in the middle Neoproterozoic due to disruption of the ecological environment that may have been caused by global glaciations. The Doushantuo microfossil assemblage records high diversity and radiation of protists during the early to middle Ediacaran. An acritarch assemblage of Asteridium–Comasphaeridium–Heliosphaeridium–Megathrix, which is contemporaneous with the lowermost Meishucunian small shelly fossil assemblage — Anabarites trisulcatus–Protohertzina anabarica, is widely distributed in the lowermost Cambrian strata of South China and the Tarim Basin and is useful for biostratigraphic correlation with Baltica and other areas. © 2007 Elsevier B.V. All rights reserved. Keywords: Radiation; Protists; Neoproterozoic; Early Cambrian; China
1. Summary of the organic-walled microfossil record In recent years, many microfossils, including animal embryos, larvae, eggs, cnidarian remains, and putative bilaterian animals, have been reported from phosphorite of the late Neoproterozoic Doushantuo Formation of South China. These fossils open a new window into life before the ‘Cambrian explosion’. Protists played fundamental roles in ancient ecosystems. Therefore, development and radiation of marine protists could be affected by and could reflect changes in the ecological environment. Remarkable radiations of ⁎ Corresponding author. E-mail address: [email protected] (Y. Leiming). 0031-0182/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2007.03.028
eukaryotes during the Neoproterozoic and Early Cambrian can be recognized on the basis of available microfossils of China and elsewhere of the world. In the Mesoproterozoic, various microorganisms, including protists, had already developed relatively high morphological diversity. Most previously known Mesoproterozoic microfossils are characterized by cyanobacteria-like coccoids and mat-building filaments, preserved in cherts (see summary by Knoll and Sergeev, 1995). However, organic-walled microfossils obtained from the shale of the Mesoproterozoic Ruyang Group (ca. 1300 Ma) of Shanxi, China include morphologically diverse forms, such as acanthomorphic acritarchs, netromorphic acritarchs, multicellular filaments and algal thalli (Yin, 1997; Xiao et al., 1997; Yin and Yuan, 2003b).
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According to their morphological features, organicwalled microfossils of the Ruyang Group can be categorized into several groups: 1) Sphaeromorphic acritarchs, such as Leiosphaeridia (Eisenack) Turner, 1984 (Fig. 1.5), Valeria lophostriata Jankauskas, 1982 (Fig. 1.4), Dictyosphaera delicata Hu and Fu, 1982 (Fig. 1.1), etc. 2) Netromorphic acritarchs, Spiromorpha segmentata (Prasad and Asher, 2001) emend. and comb. Yin et al. (2005) (Fig. 1.3), which is characterized by spiral stripes on vesicle wall. 3) Acanthomorphic acritarchs, Shuiyousphaeridium (Yan) emend. Yin, 1997 (Fig. 1.6) and Tappania Yin, 1997 (Fig. 1.2). 4) Other various and uncertain multicellular organic remains. Recent study undertaken by transmission electron microscope (TEM) and organic geochemistry reveals that Dictyosphaera delicata and Shuiyousphaeridium of the Mesoproterozoic Ruyang Group may be dinoflagellate-like eukaryotes, based on their multi-layered vesicle wall with interlocking polygonal plates and triaromatic dinosteranes extracted from the rock sample containing these acritarchs (Yin and Yuan, 2003b; Meng et al., 2005). These microfossils, as well as other acritarchs (e.g. Tappania), have been interpreted as probable fungi by Butterfield (2005). Butterfield's interpretation was based on morphological comparison of acritarchs from the early Neoproterozoic Wynniatt Formation of northwestern Canada and the late Mesoproterozoic Ruyang Group of North China. However, no specimens of Ruyang acanthomorphic acritarchs (Tappania and Shuiyousphaeridium) obtained by repeated palynological analysis show septate, branching processes, which were considered by Butterfield to be key fungal features. Moreover, the biomarker lanostene characteristic of non-photosynthetic multicellular organisms such as fungi has not been detected from extracts of whole rock sample containing abundant Shuiyousphaeridium and Dictyosphaera. In addition, Spiromorpha segmentata bears morphological similarity to the extant conjugating green alga-Spirotaenia; both have spindle-shaped cells and spiral striae on their cell walls. This morphological similarity suggests that sexual reproduction by conjugation may have originated in the late Mesoproterozoic. Furthermore, multicellular algae and ribbon-like thalli with spiral helical micro-tubes also appear in the Ruyang Group (Yin and Yuan, 2003b). The Ruyang microfossil assemblage provides palaeontological evidence to understand the diversification of
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eukaryotic kingdoms in the Mesoproterozoic (Knoll, 1992; Douzery et al., 2004). Similar microfossil assemblages have been discovered from Mesoproterozoic shale in Australia and India (Javaux et al., 2001; Prasad and Asher, 2001). The correlation of the Neoproterozoic successions between North China and South China has long been an unresolved issue because of their different tectonic histories. Early Neoproterozoic organic-walled microfossils of North China are dominated by sphaeromorphic acritarchs, including Leiosphaeridia (Fig. 2.2 and 2.7), Trachysphaeridium, Satka, Synsphaeridium (Fig. 2.9), Simia, as well as some germinating cyst-like forms [e.g. Germinosphaera (Fig. 2.11)] and acanthomorphic acritarchs, such as Trachyhystrichosphaera (Yin and Guan, 1999). Organic-walled microfossil assemblages from Neoproterozoic successions in transitional areas between North China and South China, i.e. in the Huainan district of Anhui Province, eastern Liaoning Province and eastern Jilin Province, are also dominated by various sphaeromorphic acritarchs, most of which are similar to those found in early Neoproterozoic strata of North China. However, some different forms, such as Pterospermopsimorpha insolita, P. pileiformis, Jilinella delicate, J. lepida, Larvimorpha mirusa (Fig. 2.4 and 2.5), Pololeptus biacris, P. rugosa (Fig. 1.1 and 1.3), and Strictosphaeridium rugosum (Fig. 2.10), occur only in these assemblages (Yin and Yuan, 2003a). In South China, above the Marinoan-age Nantuo diamictite, clastic rocks and carbonates of the Doushantuo and the Dengying Formations are widespread. A few specimens of possible algal fragments, named as Vendotaenia antiqua, Polyporata microporosa, P. obsoleta, have been reported from the pre-Cryogenian Liantuo Formation (Xing et al., 1985). Marine protists during Neoproterozoic glaciation were restricted by physical and chemical stresses. A microfossil assemblage has been obtained from manganese ore deposits and shale of the interglacial Datangpo Formation in eastern Guizhou and western Hunan provinces. Some cyanobacteria (Fig. 3.7, 3.10 and 3.11) and smaller vesicle acritarchs, such as Eozygion, Trachysphaeridium (Fig. 3.8), Gloeocapsomorpha, Leiominuscula (Fig. 3.5), Leiosphaeridia (Fig. 3.2, 3.6 and 3.9), Micrhystridium, Microconcentrica, Protosphaeridium, Sphaerocongregus (Fig. 3.1 and 3.3), and Synsphaeridium (Fig. 3.4), have been obtained from the Datangpo Formation (Yin, 1989, 1990). Broadly similar microfossil assemblages, including ?Dictyotidium, Leiosphaeridia, Protoleiosphaeridium, Sinianella, Sphaerocongregus, Stictosphaeridium, Trachysphaeridium, Trematosphaeridium, Vandalosphaeridium, and Siphonophycus, have also been discovered
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Fig. 1. Organic-walled microfossils from the Beidajian Formation of the late Mesoproterozoic Ruyang Group in Shanxi Province, China. 1. Dictyosphaera delicata Hu and Fu, 1982; 2. Tappania plana Yin, 1997; 3. Spiromorpha segmentata (Prasad and Asher, 2001) emend. and comb.Yin et al. (2005); 4. Valeria lophostriata Jankauskas, 1982; 5. Leiosphaeridia sp.; 6. Shuiyousphaeridium macroreticulatum (Du)Yan, emend. Yin, 1997; 7. Archaeoclada ramosa Hermann, 1989. ⁎Scale bar in 5 is 70 μm for 1, 20 μm for 2, 30 μm for 3, 97 μm for 4, 40 μm for 5, 79 μm for 6, 31 μm for 7.
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Fig. 2. Selected organic-walled microfossils from early Neoproterozoic sequences of North China. 1, 3. Pololeptus rugosa (Yin, C.) emend. and comb. Yin and Sun, 1993 from the Liulaobei Formation in Huainan region of Anhui Province. 2, 7. Leiosphaeridia kulgunica Jankauskas, 1980 from the Dongjia Formation in Lushan region of Henan Province. 4, 5. Larvimorpha mirasa Yin, 1987 from the Qinggouzi Formation in Hunjiang region of Jilin Province. 6. Leiosphaeridia asperata (Naumova) Lindgren, 1982 from the Liulaobei Formation in Huainan region of Anhui Province. 8. Polythrichoides lineatus (Hermann) emend. Knoll et al., 1991 from the Liulaobei Formation in Huainan region of Anhui Province. 9. Synsphaeridium sp. From the Dongjia Formation in Lushan region of Henan Province. 10. Strictosphaeridium rugosum Yin, 1987 from the Qinggouzi Formation in Hunjiang region of Jilin Province. 11. Germinosphaera unispinosa Mikhailova, 1986 from the Dongjia Formation in Lushan region of Henan Province. ⁎Scale bar in 11 is 18 μm for 1, 2, 3; 12 μm for 4, 5; 17 μm, for 6, 19 μm for 7, 13 μm for 8, 21 μm for. 9, 30 μm for 10, 51 μm for 11.
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Fig. 3. Microfossils from the Datangpo Formation (the Nantuo interglacial interval) in eastern Guizhou and western Hunan provinces. 1, 3. Sphaerocongregus? sp. From the Datangpo Formation in Huayuan region of Hunan Province. 2, 6, 9. Leiosphaeridia sp. from the Datangpo Formation in Huayuan region of Hunan Province. 4. Synsphaeridium sp. from the Datangpo Formation in Huayuan region of Hunan Province. 5. Leiominuscula sp. from the Datangpo Formation in Songtao region of Guizhou Province. 7, 10, 11. Permineralized coccoid microfossils from the Datangpo Formation in Songtao region of Guizhou Province. 8. Trachysphaeridium? laufeldii Vidal, 1976 from the Datangpo Formation in Huayuan region of Hunan Province. ⁎Scale bar in 5 is 14 μm for 2, 19 μm for 4, 15 μm for 5, 22 μm for 6, 14 μm for 8, 13 μm for 9.
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Fig. 4. Permineralized microfossils from the terminal Neoproterozoic Doushantuo Formation of South China. 1. Meghystrichosphaeridium perpectum (Kolosova)comb. Zhang et al., 1998 from the Doushantuo Formation in Weng'an region of Guizhou Province. 2. Apodastoides basileus Zhang et al., 1998 from the Doushantuo Formation in Yichang region of Hubei Province. 3. Papillamembrana compta (Spjeldnaes) emend. Vidal, emend. Zhang et al., 1998 from the Doushantuo Formation in Yichang region of Hubei Province. 4. Eotylotopalla dactylos Zhang et al., 1998 from the Doushantuo Formation in Yichang region of Hubei Province. 5, 7. Meghystrichosphaeridium chandianensis (Chen and Liu) emend. Zhang et al., 1998 from the Doushantuo Formation in Weng'an region of Guizhou Province. 6. Distosphaera speciosa Zhang et al., 1998 from the Doushantuo Formation in Weng'an region of Guizhou Province. ⁎ Scale bar in 1 is 90 μm for 1, 37 μm for 2, 79 μm for 3, 17 μm for 4, 51 μm for 5, 17 μm for 6, 179 μm for 7.
from the Nantuo Formation in western Hubei Province (Zang, 1992). At present, no microfossils have been found from the “cap” carbonate unit overlying the Nantuo tillites, al-
though late Neoproterozoic tillites and overlying strata in the Yangtze Gorges region and at Lantian, Xiuning County, South Anhui Province have been carefully investigated by palaeontologists.
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Fig. 5. Microfossils from Neoproterozoic–Early Cambrian transitional sequences. 1, 2. Megathrix longus (Yin, L.) emend. Yin et al. (2005) from the Yurtus Formation in Aksu–Wushi area of Xinjiang Province. 3. Comasphaeridium annulare (Wang) comb. Yin et al. (2005) from the Xishanblaq Formation in Quruqtagh area of Xijiang Province. 4. Asteridium tornatum (Volkova) Moczydłowska, 1991 from the Xishanblaq Formation in Quruqtagh area of Xijiang Province. 5, 6. Heliosphaeridium cf. lubomlense (Kirjanov) Moczydłowska, 1991 from the Xishanblaq Formation in Quruqtagh area of Xijiang Province. 7, 8, 9. Eupoikilofusa cloudiiYin, 1987 from the Gouhou Formation in Huinan region of Anhui Province. ⁎Scale bar in 7 is 65 μm for 1, 2; 15 μm for 3, 8 μm for 4, 8.8 μm for 5, 11 μm for 6, 25 μm for 7, 11 μm for 8, 13 μm for 9.
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Deposited after the Nantuo glaciation, the Ediacaranage Doushantuo Formation of South China is a well known fossiliferous stratigraphic sequence throughout the world. The Doushantuo Formation in the Yangtze Gorge region, Guizhou, Jiangxi and Hubei provinces contains organic-walled microfossils represented by large (normally N100 μm in size) acanthomorphic acritarchs. Fig. 4 shows some large acanthomorphic acritarchs, including Apodastoides (Fig. 4.2), Eotylotopalla (Fig. 4.4), Distosphaera (Fig. 4.6), Meghystrichosphaeridium (Fig. 4.1, 4.5 and 4.7), Papillamembrana (Fig. 4.3). Their morphological features, e.g. organic wall, occasionally excystment-like opening, membranous envelope, seem to indicate that they are more closely related to microphytoplankton rather than microzooplankton (Yin et al., 1999). However, further research may prove that some large acritarch forms might be the remains of microzooplankton. In addition, the remains of multicellular thallophytes and tissue-like fossils, e.g. Retinarites, Prototrichoides, etc., have been described from the Doushantuo Formation in central Guizhou (Zhang, 1989; Zhang and Yuang, 1992; Xiao et al., 1998; Zhang et al., 1998) and the Yangtze Gorges district (Yin and Li, 1978; Yin, 1987). The same large acanthomorphic acritarchs have been reported from equivalent successions in the Amadeus Basin of central Australia (Zang and Walter, 1989), Svalbard (Knoll and Ohta, 1988), Siberia (Kolosova, 1991), southern Norway (Vidal, 1990), and the Lesser Himalaya, India (Tiwari and Knoll, 1994). Although taxonomic identification for these late Neoproterozoic large complex acritarchs is still controversial, they would be potential index fossils for the correlation of late Neoproterozoic successions at regional and intercontinental scales (Zhang et al., 1998; Grey et al., 2003; Moczyd3owska, 2005). More recently, three-dimensionally preserved animal embryos (Xiao et al., 1998; Li et al., 1998), eumetazoans and putative bilaterian animals (Chen et al., 2004 have been reported from the phosphorites of the Doushantuo Formation in Guizhou Province, China. These fossils imply that some microzooplankton and other animal forms might have existed in the marine environment of the late Neoproterozoic, although controversies about the interpretation of these fossils continue. In the overlying Dengying Formation, the acritarch assemblage is dominated by sphaeromorphic acritarchs. It is noted that nearly all large acanthomorphic acritarchs, which occur in cherts and phosphorites of the Doushantuo Formation, are absent from the acritarch assemblage of the Dengying Formation. Only small (b 15 μm) acanthomorphic specimens occur in the top of the formation. In
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South China and the Tarim Basin, a unit of black chert and phosphorite outcrops at the base of many sub-trilobite Cambrian successions. This unit contains the Asteridium–Comasphaeridium (Fig. 5.3) – Heliosphaeridium (Fig. 5.5 and 5.6) – Megathrix (Fig. 5.1 and 5.2) assemblage which can be correlated to the lowermost Meishucunian small shelly fossil assemblage — Anabarites trisulcatus–Protohertzina anabarica(Yin, 1987; Yao et al., 2005). These new biostratigraphic data help to clarify the acritarch zonation in the Lower Cambrian strata and to facilitate biostratigraphic correlation between China and Baltica. Megathrix was originally identified as a filamentous cyanobacterium based on material from the basal Cambrian Tianzhushan Member in the Yangtze Gorges area, Hubei Province (Yin, 1987). Recent study indicates that Megathrix tubes branch dichotomously and bear centrally perforated tabulae. Therefore, it has been speculated that Megathrix may be an animal rather than a filamentous cyanobacterium (Yao et al., 2005). In addition, Eupoikilofusa cloudii (Fig. 5.7, 5.8 and 5.9) – an acritarch form similar to Dactylofusa cabottii in displaying spindle shape and with spiral ridge-like stripes on its wall – has been discovered from shales of the Gouhou Formation (Yin, 1987), which is overlain by the lower Cambrian Houjiashan Formation in Huainan district of northern Anhui Province. If the interpretation that D. cabottii is a euglenoid fossil (Gray and Boucot, 1989) is correct, this implies that Eupoikilofusa cloudii may also belong to the euglenids which could be traced to the Neoproterozoic–Cambrian transition. 2. Discussion As summarized above, organic-walled microfossils known from late Mesoproterozoic, Neoproterozoic, and Early Cambrian rocks of China are morphologically diverse. They represent the evolutionary course of marine protists during a long geological interval (more than 1000 million years). It appears likely that the evolution of marine protists and other organisms was closely related to geographic, environmental and geologic events. Late Mesoproterozoic rocks in the Yanshan area of the North China Platform are characterized by interbeds of carbonate and clastic rocks of the Hongshuizhuang Formation and the Tieling Formation. Moderately diverse acritarchs, including polygonal and polyhedral forms (e.g. Triangumorpha, Quadratimorpha, Anguloplanina, Tetraedirixium, Octaedryxium, boat-like forms, irregular forms, and filamentous forms such as Siphonophycus, Manicosiphoninema, Jixiania, and Oscillatoriopsis) occur in these two formations (see Xing et al., 1985;
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Zhu et al., 1993). However, acanthomorphic and other morphologically complex acritarchs seen in the Mesoproterozoic Ruyang Group along the Zhongtiaoshan area do not appear in late Mesoproterozoic rocks of the Yanshan area. In terms of tectonic setting, the Zhongtiaoshan area is in the northern slope of the eastern Qinling Mountains and belongs to the Mesoproterozoic active continental margin between the North China and the South China platforms (Jia et al., 1988). On the basis of recent tectonic data, it has been suggested that South China was adjacent to Australia in the late Mesoproterozoic and broke away from Australia in early Neoproterozoic time (ca. 820–690 Ma) (Wang and Li, 2003; Ling et al., 2003). Therefore, it is possible that differences in paleogeographic position, climatic belts and environmental conditions between the Yanshan area of the North China Platform and the Zhongtiaoshan area of eastern Qinling continental margin could have directly influenced the taxonomic composition of late Mesoproterozoic marine protists. Organic-walled microfossils of the Ruyang Group in Shanxi, China reveal that unicellular eukaryotes not only had complex cellular physiology and morphology, but also evolved sexual reproduction in the Mesoproterozoic; Spiromorpha segmentata from the Ruyang Group shows some morphological similarities to extant conjugated green algae. Sexual reproduction may have triggered eukaryotic diversification as recorded in the Ruyang microfossil assemblage (Yin, 1997; Yin and Yuan, 2003a,b) and broadly equivalent microfossil assemblage from Australia (Javaux et al., 2001, 2004), India (Prasad and Asher, 2001) and Siberia (Javaux et al., 2004). Thus, eukaryotes already possessed cytoskeletal architecture, multi-layered vesicle wall, and sexual reproduction in the Mesoproterozoic. Recent study using ion microscope analysis of carbon isotope ratios of individual specimens of Dictyosphaera delicata extracted from the Ruyang Group, indicates that high carbon dioxide levels existed in the Mesoproterozoic atmosphere, after the pervasive oxygenation event that occurred before 2.2 to 2.0 billion years ago (Kaufman and Shuhai, 2003). An oxygenated hydrosphere in the late Mesoproterozoic is also consistent with the appearance of diverse eukaryotic fossils in the Ruyang Group and equivalent strata. Early Neoproterozoic acritarchs commonly exhibit lower diversity, being dominated by sphaeromorphic forms, with some germinating cyst-like forms such as Germinosphaera (Fig. 2.11), and a few acanthomorphic forms such as Trachyhystrichosphaera. Some Mesoproterozoic acanthomorphic forms like Shuiyousphaeridium, and Tappania do not occur in early Neoproterozoic acritarch assemblages.
Probably related to stressful physical and chemical conditions, such as low temperature, high concentrations of nutrients or salinity fluctuations, caused by an influx of glacial meltwater during widespread glaciation (Snowball Earth events) (Kirschvink, 1992; Hoffman et al., 1998), organic-walled microfossils obtained from early Neoproterozoic interglacial black shale and manganese ore deposits are typically small, single leiosphaerids and blue-green algal colonies (Fig. 3; Yin, 1990). After the terminal Proterozoic Nantuo glaciation, eukaryotic life eventually embraced the arrival of a favorable environment. The return to warm climate after glaciation, nutrient influx with glacial meltwater, oceanic upwelling triggered by break-up of the ‘Rodinia’ supercontinent, and oxygen rise provided opportunities for the rapid development and radiation of eukaryotic organisms. As Knoll (2003) stated: “the eukaryote-rich rocks of the Doushantuo Formation will not only illuminate the rise of nucleated organisms but hint, as well, of further biological transformation about to begin” (Knoll, 2003; p.142). Diversification of marine protists during the late Neoproterozoic is represented by the Doushantuo microfossil assemblage. So far, nearly 50 morphological species of large complex acritarchs have been described from the late Neoproterozoic Doushantuo Formation. The Doushantuo eukaryotes were not the first to evolve, as eukaryotes had already been preserved in Mesoproterozoic rocks in China, Australia and India. In fact, some of these Mesoproterozoic acritarchs already qualify as large complex acritarchs; Shuiyousphaeridium from the Ruyang Group is about 150 μm and can be up to 300 μm in diameter. However, it is unclear why so many large complex acritarchs occur in the late Neoproterozoic Doushantuo Formation. In order to maintain suspension and to deter predators, marine protists usually increase the ratio of surface area to volume through process development (Walsby and Reynolds, 1980; Sournia, 1982; Sarjeant et al., 1987). Alternatively, competition for nutrition and living space may have played a role in the late Neoproterozoic diversification of eukaryotes. At the Neoproterozoic–Cambrian transition, various ecological perturbations may have occurred in South China due to tectonic movements and environmental changes. As a result, different microfossil assemblages occur in different regions. For example, in South China, basal Cambrian black cherts and phosphorites contain abundant small acanthomorphic acritarchs (e.g. Asteridium (Fig. 5.4), Heliosphaeridium and Comasphaeridium) and the tubular microfossil Megathrix. However, Eupoikilofusa cloudii with spiral striae on the vesicle surface along with some simple sphaeromorphs occur in shales of the Gouhou Formation in the Huainan area. Such
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different preservation and distribution of microplanktonic fossils in different regions reflect a remarkable variation in depositional conditions or ecological–environmental partitioning during Neoproterozoic–Cambrian transition. 3. Summary Based on available acritarch data from Neoproterozoic and Early Cambrian rocks in China, several conclusions can be made with regard to the evolution of microplankton: 1) The multi-layered structure of cell walls (or vesicle walls), cytoskeletal architecture (appearance of remarkable spine-like processes) and excystment structures that together characterize typical eukaryotic organisms evolved in the Mesoproterozoic. Biogeochemical analysis informs us that possible primitive dinoflagellates may have evolved in the Mesoproterozoic, too. In addition, conjugated green algae with sexual reproduction may have also evolved at the same time, based on morphological comparison between Spiromorpha segmentata and extant Spirotaenia. 2) Membranous fragments with microscopic tubes and annular-helical thickening from the Mesoproterozoic Ruyang Group suggest that multicellular algae with the possible function of resisting drought may have arisen as early as the Mesoproterozoic. 3) During the Neoproterozoic glacial interval (“snowball” events), cyanobacteria and a few eukaryotic protists survived in stressed environments with anomalous salinity, caused by influx of glacial meltwater and low temperatures. 4) The Neoproterozoic glaciations (“snowball” events) were followed by global warming, oceanic upwelling, increased nutrient supply, and extraordinary evolutionary development of microplankton. The Doushantuo microfossil assemblage records this evolutionary event. 5) Just before the “Cambrian explosion”, the abundance and diversity of acritarchs significantly declined and no large complex acritarchs (large acanthomorphic acritarchs) occur in the terminal Precambrian Dengying Formation. 6) An acritarch assemblage of Asteridium–Comasphaeridium–Heliosphaeridium–Megathrix, contemporaneous with the lowermost Meishucunian small shelly fossil assemblage — Anabarites trisulcatus– Protohertzina anabarica, is widely distributed in lowermost Cambrian strata of South China and the Tarim Basin; it provides a means for biostratigraphic correlation with Baltica and other areas.
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Radiation of Meso-Neoproterozoic and early Cambrian protists inferred from the microfossil record of China Yin Leiming ⁎, Yuan Xunlai Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China Accepted 5 March 2007
Abstract Marine protists can be affected by and reflect changes in the ecological environment. Based on available microfossil evidence from late Mesoproterozoic–Early Cambrian rocks of China, radiations of protists and related changes in ecological environments are discussed in the paper. Remarkable development of protists had occurred by as early as the Mesoproterozoic. Protist diversity significantly decreased in the middle Neoproterozoic due to disruption of the ecological environment that may have been caused by global glaciations. The Doushantuo microfossil assemblage records high diversity and radiation of protists during the early to middle Ediacaran. An acritarch assemblage of Asteridium–Comasphaeridium–Heliosphaeridium–Megathrix, which is contemporaneous with the lowermost Meishucunian small shelly fossil assemblage — Anabarites trisulcatus–Protohertzina anabarica, is widely distributed in the lowermost Cambrian strata of South China and the Tarim Basin and is useful for biostratigraphic correlation with Baltica and other areas. © 2007 Elsevier B.V. All rights reserved. Keywords: Radiation; Protists; Neoproterozoic; Early Cambrian; China
1. Summary of the organic-walled microfossil record In recent years, many microfossils, including animal embryos, larvae, eggs, cnidarian remains, and putative bilaterian animals, have been reported from phosphorite of the late Neoproterozoic Doushantuo Formation of South China. These fossils open a new window into life before the ‘Cambrian explosion’. Protists played fundamental roles in ancient ecosystems. Therefore, development and radiation of marine protists could be affected by and could reflect changes in the ecological environment. Remarkable radiations of ⁎ Corresponding author. E-mail address: [email protected] (Y. Leiming). 0031-0182/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2007.03.028
eukaryotes during the Neoproterozoic and Early Cambrian can be recognized on the basis of available microfossils of China and elsewhere of the world. In the Mesoproterozoic, various microorganisms, including protists, had already developed relatively high morphological diversity. Most previously known Mesoproterozoic microfossils are characterized by cyanobacteria-like coccoids and mat-building filaments, preserved in cherts (see summary by Knoll and Sergeev, 1995). However, organic-walled microfossils obtained from the shale of the Mesoproterozoic Ruyang Group (ca. 1300 Ma) of Shanxi, China include morphologically diverse forms, such as acanthomorphic acritarchs, netromorphic acritarchs, multicellular filaments and algal thalli (Yin, 1997; Xiao et al., 1997; Yin and Yuan, 2003b).
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According to their morphological features, organicwalled microfossils of the Ruyang Group can be categorized into several groups: 1) Sphaeromorphic acritarchs, such as Leiosphaeridia (Eisenack) Turner, 1984 (Fig. 1.5), Valeria lophostriata Jankauskas, 1982 (Fig. 1.4), Dictyosphaera delicata Hu and Fu, 1982 (Fig. 1.1), etc. 2) Netromorphic acritarchs, Spiromorpha segmentata (Prasad and Asher, 2001) emend. and comb. Yin et al. (2005) (Fig. 1.3), which is characterized by spiral stripes on vesicle wall. 3) Acanthomorphic acritarchs, Shuiyousphaeridium (Yan) emend. Yin, 1997 (Fig. 1.6) and Tappania Yin, 1997 (Fig. 1.2). 4) Other various and uncertain multicellular organic remains. Recent study undertaken by transmission electron microscope (TEM) and organic geochemistry reveals that Dictyosphaera delicata and Shuiyousphaeridium of the Mesoproterozoic Ruyang Group may be dinoflagellate-like eukaryotes, based on their multi-layered vesicle wall with interlocking polygonal plates and triaromatic dinosteranes extracted from the rock sample containing these acritarchs (Yin and Yuan, 2003b; Meng et al., 2005). These microfossils, as well as other acritarchs (e.g. Tappania), have been interpreted as probable fungi by Butterfield (2005). Butterfield's interpretation was based on morphological comparison of acritarchs from the early Neoproterozoic Wynniatt Formation of northwestern Canada and the late Mesoproterozoic Ruyang Group of North China. However, no specimens of Ruyang acanthomorphic acritarchs (Tappania and Shuiyousphaeridium) obtained by repeated palynological analysis show septate, branching processes, which were considered by Butterfield to be key fungal features. Moreover, the biomarker lanostene characteristic of non-photosynthetic multicellular organisms such as fungi has not been detected from extracts of whole rock sample containing abundant Shuiyousphaeridium and Dictyosphaera. In addition, Spiromorpha segmentata bears morphological similarity to the extant conjugating green alga-Spirotaenia; both have spindle-shaped cells and spiral striae on their cell walls. This morphological similarity suggests that sexual reproduction by conjugation may have originated in the late Mesoproterozoic. Furthermore, multicellular algae and ribbon-like thalli with spiral helical micro-tubes also appear in the Ruyang Group (Yin and Yuan, 2003b). The Ruyang microfossil assemblage provides palaeontological evidence to understand the diversification of
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eukaryotic kingdoms in the Mesoproterozoic (Knoll, 1992; Douzery et al., 2004). Similar microfossil assemblages have been discovered from Mesoproterozoic shale in Australia and India (Javaux et al., 2001; Prasad and Asher, 2001). The correlation of the Neoproterozoic successions between North China and South China has long been an unresolved issue because of their different tectonic histories. Early Neoproterozoic organic-walled microfossils of North China are dominated by sphaeromorphic acritarchs, including Leiosphaeridia (Fig. 2.2 and 2.7), Trachysphaeridium, Satka, Synsphaeridium (Fig. 2.9), Simia, as well as some germinating cyst-like forms [e.g. Germinosphaera (Fig. 2.11)] and acanthomorphic acritarchs, such as Trachyhystrichosphaera (Yin and Guan, 1999). Organic-walled microfossil assemblages from Neoproterozoic successions in transitional areas between North China and South China, i.e. in the Huainan district of Anhui Province, eastern Liaoning Province and eastern Jilin Province, are also dominated by various sphaeromorphic acritarchs, most of which are similar to those found in early Neoproterozoic strata of North China. However, some different forms, such as Pterospermopsimorpha insolita, P. pileiformis, Jilinella delicate, J. lepida, Larvimorpha mirusa (Fig. 2.4 and 2.5), Pololeptus biacris, P. rugosa (Fig. 1.1 and 1.3), and Strictosphaeridium rugosum (Fig. 2.10), occur only in these assemblages (Yin and Yuan, 2003a). In South China, above the Marinoan-age Nantuo diamictite, clastic rocks and carbonates of the Doushantuo and the Dengying Formations are widespread. A few specimens of possible algal fragments, named as Vendotaenia antiqua, Polyporata microporosa, P. obsoleta, have been reported from the pre-Cryogenian Liantuo Formation (Xing et al., 1985). Marine protists during Neoproterozoic glaciation were restricted by physical and chemical stresses. A microfossil assemblage has been obtained from manganese ore deposits and shale of the interglacial Datangpo Formation in eastern Guizhou and western Hunan provinces. Some cyanobacteria (Fig. 3.7, 3.10 and 3.11) and smaller vesicle acritarchs, such as Eozygion, Trachysphaeridium (Fig. 3.8), Gloeocapsomorpha, Leiominuscula (Fig. 3.5), Leiosphaeridia (Fig. 3.2, 3.6 and 3.9), Micrhystridium, Microconcentrica, Protosphaeridium, Sphaerocongregus (Fig. 3.1 and 3.3), and Synsphaeridium (Fig. 3.4), have been obtained from the Datangpo Formation (Yin, 1989, 1990). Broadly similar microfossil assemblages, including ?Dictyotidium, Leiosphaeridia, Protoleiosphaeridium, Sinianella, Sphaerocongregus, Stictosphaeridium, Trachysphaeridium, Trematosphaeridium, Vandalosphaeridium, and Siphonophycus, have also been discovered
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Fig. 1. Organic-walled microfossils from the Beidajian Formation of the late Mesoproterozoic Ruyang Group in Shanxi Province, China. 1. Dictyosphaera delicata Hu and Fu, 1982; 2. Tappania plana Yin, 1997; 3. Spiromorpha segmentata (Prasad and Asher, 2001) emend. and comb.Yin et al. (2005); 4. Valeria lophostriata Jankauskas, 1982; 5. Leiosphaeridia sp.; 6. Shuiyousphaeridium macroreticulatum (Du)Yan, emend. Yin, 1997; 7. Archaeoclada ramosa Hermann, 1989. ⁎Scale bar in 5 is 70 μm for 1, 20 μm for 2, 30 μm for 3, 97 μm for 4, 40 μm for 5, 79 μm for 6, 31 μm for 7.
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Fig. 2. Selected organic-walled microfossils from early Neoproterozoic sequences of North China. 1, 3. Pololeptus rugosa (Yin, C.) emend. and comb. Yin and Sun, 1993 from the Liulaobei Formation in Huainan region of Anhui Province. 2, 7. Leiosphaeridia kulgunica Jankauskas, 1980 from the Dongjia Formation in Lushan region of Henan Province. 4, 5. Larvimorpha mirasa Yin, 1987 from the Qinggouzi Formation in Hunjiang region of Jilin Province. 6. Leiosphaeridia asperata (Naumova) Lindgren, 1982 from the Liulaobei Formation in Huainan region of Anhui Province. 8. Polythrichoides lineatus (Hermann) emend. Knoll et al., 1991 from the Liulaobei Formation in Huainan region of Anhui Province. 9. Synsphaeridium sp. From the Dongjia Formation in Lushan region of Henan Province. 10. Strictosphaeridium rugosum Yin, 1987 from the Qinggouzi Formation in Hunjiang region of Jilin Province. 11. Germinosphaera unispinosa Mikhailova, 1986 from the Dongjia Formation in Lushan region of Henan Province. ⁎Scale bar in 11 is 18 μm for 1, 2, 3; 12 μm for 4, 5; 17 μm, for 6, 19 μm for 7, 13 μm for 8, 21 μm for. 9, 30 μm for 10, 51 μm for 11.
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Fig. 3. Microfossils from the Datangpo Formation (the Nantuo interglacial interval) in eastern Guizhou and western Hunan provinces. 1, 3. Sphaerocongregus? sp. From the Datangpo Formation in Huayuan region of Hunan Province. 2, 6, 9. Leiosphaeridia sp. from the Datangpo Formation in Huayuan region of Hunan Province. 4. Synsphaeridium sp. from the Datangpo Formation in Huayuan region of Hunan Province. 5. Leiominuscula sp. from the Datangpo Formation in Songtao region of Guizhou Province. 7, 10, 11. Permineralized coccoid microfossils from the Datangpo Formation in Songtao region of Guizhou Province. 8. Trachysphaeridium? laufeldii Vidal, 1976 from the Datangpo Formation in Huayuan region of Hunan Province. ⁎Scale bar in 5 is 14 μm for 2, 19 μm for 4, 15 μm for 5, 22 μm for 6, 14 μm for 8, 13 μm for 9.
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Fig. 4. Permineralized microfossils from the terminal Neoproterozoic Doushantuo Formation of South China. 1. Meghystrichosphaeridium perpectum (Kolosova)comb. Zhang et al., 1998 from the Doushantuo Formation in Weng'an region of Guizhou Province. 2. Apodastoides basileus Zhang et al., 1998 from the Doushantuo Formation in Yichang region of Hubei Province. 3. Papillamembrana compta (Spjeldnaes) emend. Vidal, emend. Zhang et al., 1998 from the Doushantuo Formation in Yichang region of Hubei Province. 4. Eotylotopalla dactylos Zhang et al., 1998 from the Doushantuo Formation in Yichang region of Hubei Province. 5, 7. Meghystrichosphaeridium chandianensis (Chen and Liu) emend. Zhang et al., 1998 from the Doushantuo Formation in Weng'an region of Guizhou Province. 6. Distosphaera speciosa Zhang et al., 1998 from the Doushantuo Formation in Weng'an region of Guizhou Province. ⁎ Scale bar in 1 is 90 μm for 1, 37 μm for 2, 79 μm for 3, 17 μm for 4, 51 μm for 5, 17 μm for 6, 179 μm for 7.
from the Nantuo Formation in western Hubei Province (Zang, 1992). At present, no microfossils have been found from the “cap” carbonate unit overlying the Nantuo tillites, al-
though late Neoproterozoic tillites and overlying strata in the Yangtze Gorges region and at Lantian, Xiuning County, South Anhui Province have been carefully investigated by palaeontologists.
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Fig. 5. Microfossils from Neoproterozoic–Early Cambrian transitional sequences. 1, 2. Megathrix longus (Yin, L.) emend. Yin et al. (2005) from the Yurtus Formation in Aksu–Wushi area of Xinjiang Province. 3. Comasphaeridium annulare (Wang) comb. Yin et al. (2005) from the Xishanblaq Formation in Quruqtagh area of Xijiang Province. 4. Asteridium tornatum (Volkova) Moczydłowska, 1991 from the Xishanblaq Formation in Quruqtagh area of Xijiang Province. 5, 6. Heliosphaeridium cf. lubomlense (Kirjanov) Moczydłowska, 1991 from the Xishanblaq Formation in Quruqtagh area of Xijiang Province. 7, 8, 9. Eupoikilofusa cloudiiYin, 1987 from the Gouhou Formation in Huinan region of Anhui Province. ⁎Scale bar in 7 is 65 μm for 1, 2; 15 μm for 3, 8 μm for 4, 8.8 μm for 5, 11 μm for 6, 25 μm for 7, 11 μm for 8, 13 μm for 9.
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Deposited after the Nantuo glaciation, the Ediacaranage Doushantuo Formation of South China is a well known fossiliferous stratigraphic sequence throughout the world. The Doushantuo Formation in the Yangtze Gorge region, Guizhou, Jiangxi and Hubei provinces contains organic-walled microfossils represented by large (normally N100 μm in size) acanthomorphic acritarchs. Fig. 4 shows some large acanthomorphic acritarchs, including Apodastoides (Fig. 4.2), Eotylotopalla (Fig. 4.4), Distosphaera (Fig. 4.6), Meghystrichosphaeridium (Fig. 4.1, 4.5 and 4.7), Papillamembrana (Fig. 4.3). Their morphological features, e.g. organic wall, occasionally excystment-like opening, membranous envelope, seem to indicate that they are more closely related to microphytoplankton rather than microzooplankton (Yin et al., 1999). However, further research may prove that some large acritarch forms might be the remains of microzooplankton. In addition, the remains of multicellular thallophytes and tissue-like fossils, e.g. Retinarites, Prototrichoides, etc., have been described from the Doushantuo Formation in central Guizhou (Zhang, 1989; Zhang and Yuang, 1992; Xiao et al., 1998; Zhang et al., 1998) and the Yangtze Gorges district (Yin and Li, 1978; Yin, 1987). The same large acanthomorphic acritarchs have been reported from equivalent successions in the Amadeus Basin of central Australia (Zang and Walter, 1989), Svalbard (Knoll and Ohta, 1988), Siberia (Kolosova, 1991), southern Norway (Vidal, 1990), and the Lesser Himalaya, India (Tiwari and Knoll, 1994). Although taxonomic identification for these late Neoproterozoic large complex acritarchs is still controversial, they would be potential index fossils for the correlation of late Neoproterozoic successions at regional and intercontinental scales (Zhang et al., 1998; Grey et al., 2003; Moczyd3owska, 2005). More recently, three-dimensionally preserved animal embryos (Xiao et al., 1998; Li et al., 1998), eumetazoans and putative bilaterian animals (Chen et al., 2004 have been reported from the phosphorites of the Doushantuo Formation in Guizhou Province, China. These fossils imply that some microzooplankton and other animal forms might have existed in the marine environment of the late Neoproterozoic, although controversies about the interpretation of these fossils continue. In the overlying Dengying Formation, the acritarch assemblage is dominated by sphaeromorphic acritarchs. It is noted that nearly all large acanthomorphic acritarchs, which occur in cherts and phosphorites of the Doushantuo Formation, are absent from the acritarch assemblage of the Dengying Formation. Only small (b 15 μm) acanthomorphic specimens occur in the top of the formation. In
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South China and the Tarim Basin, a unit of black chert and phosphorite outcrops at the base of many sub-trilobite Cambrian successions. This unit contains the Asteridium–Comasphaeridium (Fig. 5.3) – Heliosphaeridium (Fig. 5.5 and 5.6) – Megathrix (Fig. 5.1 and 5.2) assemblage which can be correlated to the lowermost Meishucunian small shelly fossil assemblage — Anabarites trisulcatus–Protohertzina anabarica(Yin, 1987; Yao et al., 2005). These new biostratigraphic data help to clarify the acritarch zonation in the Lower Cambrian strata and to facilitate biostratigraphic correlation between China and Baltica. Megathrix was originally identified as a filamentous cyanobacterium based on material from the basal Cambrian Tianzhushan Member in the Yangtze Gorges area, Hubei Province (Yin, 1987). Recent study indicates that Megathrix tubes branch dichotomously and bear centrally perforated tabulae. Therefore, it has been speculated that Megathrix may be an animal rather than a filamentous cyanobacterium (Yao et al., 2005). In addition, Eupoikilofusa cloudii (Fig. 5.7, 5.8 and 5.9) – an acritarch form similar to Dactylofusa cabottii in displaying spindle shape and with spiral ridge-like stripes on its wall – has been discovered from shales of the Gouhou Formation (Yin, 1987), which is overlain by the lower Cambrian Houjiashan Formation in Huainan district of northern Anhui Province. If the interpretation that D. cabottii is a euglenoid fossil (Gray and Boucot, 1989) is correct, this implies that Eupoikilofusa cloudii may also belong to the euglenids which could be traced to the Neoproterozoic–Cambrian transition. 2. Discussion As summarized above, organic-walled microfossils known from late Mesoproterozoic, Neoproterozoic, and Early Cambrian rocks of China are morphologically diverse. They represent the evolutionary course of marine protists during a long geological interval (more than 1000 million years). It appears likely that the evolution of marine protists and other organisms was closely related to geographic, environmental and geologic events. Late Mesoproterozoic rocks in the Yanshan area of the North China Platform are characterized by interbeds of carbonate and clastic rocks of the Hongshuizhuang Formation and the Tieling Formation. Moderately diverse acritarchs, including polygonal and polyhedral forms (e.g. Triangumorpha, Quadratimorpha, Anguloplanina, Tetraedirixium, Octaedryxium, boat-like forms, irregular forms, and filamentous forms such as Siphonophycus, Manicosiphoninema, Jixiania, and Oscillatoriopsis) occur in these two formations (see Xing et al., 1985;
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Zhu et al., 1993). However, acanthomorphic and other morphologically complex acritarchs seen in the Mesoproterozoic Ruyang Group along the Zhongtiaoshan area do not appear in late Mesoproterozoic rocks of the Yanshan area. In terms of tectonic setting, the Zhongtiaoshan area is in the northern slope of the eastern Qinling Mountains and belongs to the Mesoproterozoic active continental margin between the North China and the South China platforms (Jia et al., 1988). On the basis of recent tectonic data, it has been suggested that South China was adjacent to Australia in the late Mesoproterozoic and broke away from Australia in early Neoproterozoic time (ca. 820–690 Ma) (Wang and Li, 2003; Ling et al., 2003). Therefore, it is possible that differences in paleogeographic position, climatic belts and environmental conditions between the Yanshan area of the North China Platform and the Zhongtiaoshan area of eastern Qinling continental margin could have directly influenced the taxonomic composition of late Mesoproterozoic marine protists. Organic-walled microfossils of the Ruyang Group in Shanxi, China reveal that unicellular eukaryotes not only had complex cellular physiology and morphology, but also evolved sexual reproduction in the Mesoproterozoic; Spiromorpha segmentata from the Ruyang Group shows some morphological similarities to extant conjugated green algae. Sexual reproduction may have triggered eukaryotic diversification as recorded in the Ruyang microfossil assemblage (Yin, 1997; Yin and Yuan, 2003a,b) and broadly equivalent microfossil assemblage from Australia (Javaux et al., 2001, 2004), India (Prasad and Asher, 2001) and Siberia (Javaux et al., 2004). Thus, eukaryotes already possessed cytoskeletal architecture, multi-layered vesicle wall, and sexual reproduction in the Mesoproterozoic. Recent study using ion microscope analysis of carbon isotope ratios of individual specimens of Dictyosphaera delicata extracted from the Ruyang Group, indicates that high carbon dioxide levels existed in the Mesoproterozoic atmosphere, after the pervasive oxygenation event that occurred before 2.2 to 2.0 billion years ago (Kaufman and Shuhai, 2003). An oxygenated hydrosphere in the late Mesoproterozoic is also consistent with the appearance of diverse eukaryotic fossils in the Ruyang Group and equivalent strata. Early Neoproterozoic acritarchs commonly exhibit lower diversity, being dominated by sphaeromorphic forms, with some germinating cyst-like forms such as Germinosphaera (Fig. 2.11), and a few acanthomorphic forms such as Trachyhystrichosphaera. Some Mesoproterozoic acanthomorphic forms like Shuiyousphaeridium, and Tappania do not occur in early Neoproterozoic acritarch assemblages.
Probably related to stressful physical and chemical conditions, such as low temperature, high concentrations of nutrients or salinity fluctuations, caused by an influx of glacial meltwater during widespread glaciation (Snowball Earth events) (Kirschvink, 1992; Hoffman et al., 1998), organic-walled microfossils obtained from early Neoproterozoic interglacial black shale and manganese ore deposits are typically small, single leiosphaerids and blue-green algal colonies (Fig. 3; Yin, 1990). After the terminal Proterozoic Nantuo glaciation, eukaryotic life eventually embraced the arrival of a favorable environment. The return to warm climate after glaciation, nutrient influx with glacial meltwater, oceanic upwelling triggered by break-up of the ‘Rodinia’ supercontinent, and oxygen rise provided opportunities for the rapid development and radiation of eukaryotic organisms. As Knoll (2003) stated: “the eukaryote-rich rocks of the Doushantuo Formation will not only illuminate the rise of nucleated organisms but hint, as well, of further biological transformation about to begin” (Knoll, 2003; p.142). Diversification of marine protists during the late Neoproterozoic is represented by the Doushantuo microfossil assemblage. So far, nearly 50 morphological species of large complex acritarchs have been described from the late Neoproterozoic Doushantuo Formation. The Doushantuo eukaryotes were not the first to evolve, as eukaryotes had already been preserved in Mesoproterozoic rocks in China, Australia and India. In fact, some of these Mesoproterozoic acritarchs already qualify as large complex acritarchs; Shuiyousphaeridium from the Ruyang Group is about 150 μm and can be up to 300 μm in diameter. However, it is unclear why so many large complex acritarchs occur in the late Neoproterozoic Doushantuo Formation. In order to maintain suspension and to deter predators, marine protists usually increase the ratio of surface area to volume through process development (Walsby and Reynolds, 1980; Sournia, 1982; Sarjeant et al., 1987). Alternatively, competition for nutrition and living space may have played a role in the late Neoproterozoic diversification of eukaryotes. At the Neoproterozoic–Cambrian transition, various ecological perturbations may have occurred in South China due to tectonic movements and environmental changes. As a result, different microfossil assemblages occur in different regions. For example, in South China, basal Cambrian black cherts and phosphorites contain abundant small acanthomorphic acritarchs (e.g. Asteridium (Fig. 5.4), Heliosphaeridium and Comasphaeridium) and the tubular microfossil Megathrix. However, Eupoikilofusa cloudii with spiral striae on the vesicle surface along with some simple sphaeromorphs occur in shales of the Gouhou Formation in the Huainan area. Such
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different preservation and distribution of microplanktonic fossils in different regions reflect a remarkable variation in depositional conditions or ecological–environmental partitioning during Neoproterozoic–Cambrian transition. 3. Summary Based on available acritarch data from Neoproterozoic and Early Cambrian rocks in China, several conclusions can be made with regard to the evolution of microplankton: 1) The multi-layered structure of cell walls (or vesicle walls), cytoskeletal architecture (appearance of remarkable spine-like processes) and excystment structures that together characterize typical eukaryotic organisms evolved in the Mesoproterozoic. Biogeochemical analysis informs us that possible primitive dinoflagellates may have evolved in the Mesoproterozoic, too. In addition, conjugated green algae with sexual reproduction may have also evolved at the same time, based on morphological comparison between Spiromorpha segmentata and extant Spirotaenia. 2) Membranous fragments with microscopic tubes and annular-helical thickening from the Mesoproterozoic Ruyang Group suggest that multicellular algae with the possible function of resisting drought may have arisen as early as the Mesoproterozoic. 3) During the Neoproterozoic glacial interval (“snowball” events), cyanobacteria and a few eukaryotic protists survived in stressed environments with anomalous salinity, caused by influx of glacial meltwater and low temperatures. 4) The Neoproterozoic glaciations (“snowball” events) were followed by global warming, oceanic upwelling, increased nutrient supply, and extraordinary evolutionary development of microplankton. The Doushantuo microfossil assemblage records this evolutionary event. 5) Just before the “Cambrian explosion”, the abundance and diversity of acritarchs significantly declined and no large complex acritarchs (large acanthomorphic acritarchs) occur in the terminal Precambrian Dengying Formation. 6) An acritarch assemblage of Asteridium–Comasphaeridium–Heliosphaeridium–Megathrix, contemporaneous with the lowermost Meishucunian small shelly fossil assemblage — Anabarites trisulcatus– Protohertzina anabarica, is widely distributed in lowermost Cambrian strata of South China and the Tarim Basin; it provides a means for biostratigraphic correlation with Baltica and other areas.
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