Large spinose microfossils in Ediacaran rocks as resting stages of early animals

Abstract

Large (>100 m), profusely ornamented microfossils comprise a distinctive paleontological component of sedimentary rocks deposited during the Ediacaran Period (635-542 million years ago). Smaller spinose fossils in Paleozoic rocks have commonly been interpreted as algal cysts or phycomata, but the Ediacaran populations differ from modern algal analogs in size, shape, ultrastructure, and internal contents. In contrast, cysts formed during the diapause egg-resting stages of many metazoans share features of size, ornamentation, and internal contents with large ornamented Ediacaran microfossils (LOEMs). Moreover, transmission electron microscopic observations of animal-resting cysts reveal a 3-layer wall ultrastructure comparable to that of LOEM taxa. Interpretation of these distinctive Ediacaran microfossils as resting stages in early metazoan life cycles offers additional perspectives on their functional morphology and stratigraphic distribution. Based on comparisons with modern marine invertebrates, the recalcitrant life stage represented by LOEMs is interpreted as an evolutionary response to prolonged episodes of bottom water anoxia in Ediacaran shelf and platform environments. As predicted by this hypothesis, the later Ediacaran disappearance of LOEM taxa coincides with geochemical evidence for a marked decline in the extent of oxygen-depleted waters impinging on continental shelves and platforms. Thus, the form, diversity, and stratigraphic range of LOEMs illuminate life cycle evolution in early animals as influenced by the evolving redox state of the oceans.acritarchs ͉ Diapause egg cysts ͉ origin of metazoans ͉ paleoenvironment

Earth’s oxygen cycle and the evolution of animal life

“…Proterozoic marine environments would have been characterized by O 2 levels that departed strongly from background mean pO 2 , and the oxygen demand and marine habitat of different life history stages could present physiological bottlenecks that are currently poorly known for basal metazoan organisms. Indeed, microfossil evidence for metazoan life stages adapted for large-scale dispersal across inhospitable environments may represent a paleontological signal for such ecosystem oxygen stress during the Late Proterozoic (24). In this light, our results strongly suggest that the distribution of O 2 within the ocean−atmosphere system played a significant role in structuring evolutionary innovation and ecological success among early animals.…”

Rare earth elements and carbon isotope geochemistry of the Doushantuo Formation in South China: Implication for middle Ediacaran shallow marine redox conditions

“…Ediacaran acanthomorphs have long been regarded as the resting cysts of various unicellular phytoplanktonic algae [41]. However, recent studies have shown that they may have more diverse affinities, and some of them may be animal resting cysts [6,42].…”

“…Cohen et al [6] interpreted the large Ediacaran acanthomprphs as animal resting cysts, and proposed that their evolutionary rise in the early Ediacaran Period was an ecological response to bottom water anoxia, and their disappearance in the late Ediacaran Period was due to the pervasive oxygenation of continental shelves. Whether Ediacaran acanthomorphs are dormant cysts of protists or animals, it is clear that they must have spent at least part of their life cycle resting in the benthic realm [43].…”

“…Indeed, the Ediacaran fossil record shows a significant biotic turnover in shallow shelf environments during the middle Ediacaran Period, with the early Ediacaran biota characterized by globally distributed acanthomorphic acritarchs [3], and the late Ediacaran ones by classical Ediacara megafossils [4]. Previous researchers have argued that this turnover may have been driven by a middle Ediacaran glaciation event [5], predation pressure from macrophagous metazoans [3], or the oxygenation of continental shelves that released the ecological impetus for the development of acanthomorphic resting stages [6]. Integrated paleobiological and geochemical data from the Doushantuo Formation in the Yangtze Gorges area suggest that this turnover is coincident with a pronounced negative δ 13 C carb excursion that is correlated with the Shuram excursion [7], and thus may be related to shallow water anoxia resulting from upwelling of deep marine waters.…”

The Lantian biota: A new window onto the origin and early evolution of multicellular organisms

“…Subsequently, a large number of animal embryo fossils have also been found in the lower Doushantuo Formation (~632 Ma) in the Yangtze Gorges area [82,83]. It has been argued that some large acanthomorphic acritarchs from Ediacaran successions in Australia, Eastern European Platform, and Siberia may represent diapause eggs of early animals as well [84]. Because a complete ontogenetic sequence of the Weng'an embryo fossils is still a matter of debate [30,85], alternative interpretations-including green algae, giant sulfur bacteria, and mesomycetozoan-like protists-have been proposed to account for the morphologies of the Weng'an fossils [30,[86][87][88], but so far animal embryos remain the most plausible interpretation for these fossils [28,31,82,89].…”