Geological context of Ediacaran deposits of the White Sea area
Due to the mild thermal history of Ediacaran deposits in the White Sea area, Ediacaran macrofossils co-occur there with extremely well preserved biomarkers22,23, offering a unique opportunity to assess the habitat and ecological preferences of these problematic organisms. The White Sea area offers localities with the most diverse and abundant Ediacara biota in the world, including various members of the White Sea, Avalon and Nama assemblages24,25,26,27. All sediments from the Lyamtsa and Zimnie Gory localities (Fig. 1) were originally deposited in shallow-marine environments and preserve evidence for persistent and pervasive microbial mats28.
The distribution of Ediacaran macrofossils within the White Sea area sections is largely controlled by taphonomy—the fossils are best preserved at the soles of sandstone layers, but less abundant fossils of poorer quality are scattered throughout the entire sedimentary succession25,27. To get a full picture about the distribution of primary producers in depositional environments associated with the Ediacara biota, samples collected from the entire section exposed in the studied localities were analysed for biomarkers (including 52 samples from fossiliferous intervals and six samples from adjacent stratigraphic levels devoid of fossils). Most organic geochemical studies analyse centimetre-scale sedimentary rock samples, thus averaging ecological signals across substantial periods of time, and potentially missing ecologically distinct endmembers. To ensure that we indeed capture the exact ecological environment of organisms of the Ediacara biota, we analysed sediments immediately beneath and above surfaces with Ediacara biota fossils at millimetre resolution. As organisms of the Ediacara biota are preserved in situ, biomarkers extracted from clay underneath the fossils represent the substrate they were living on. Sandstones above fossils normally represent storm deposited material28; biomarkers extracted from these sandstones presumably average the biomass of the local environment, but may also contain material transported from adjacent settings. Specifically, we analysed two surfaces in the Lyamtsa locality that contain abundant Dickinsonia, Parvancorina and Palaeopascichnus fossils, and well-studied surfaces in the Zimnie Gory, known as Z1(I) and Z11(XXII), which contain Andiva, Archaeaspinus, Armilifera, Aspidella, Brachina, Charniodiscus, Cyanorus, Cyclomedusa, Dickinsonia, Inaria, Ivovicia, Kimberella, Onega, Ovatoscutum, Paleophragmodictya, Paravendia, Parvancorina, Tamga, Temnoxa, Tribrachidium and Yorgia27.
Thus, this study looks at biomarkers representative of environments for a broad range of species of the Ediacara biota with variable feeding strategies, including burrowers (e.g. Sabellidita, Calyptrina)29,30, mat-scrapers (e.g. Andiva, Dickinsonia, Kimberella) and potentially filter- or osmotroph-feeding mat stickers (Arborea, e.g. Charniodiscus). It was impossible to obtain biomarker data from particular sections and time intervals that only contain a single assemblage of the Ediacara biota24 due to their high thermal maturity (e.g. Newfoundland, United Kingdom, or Namibian sections). However, allowing for some extrapolation, the data collected in the current study provide information about the local ecological environment of representative organisms of all three existing Ediacara biota assemblages, which otherwise occur in a wider temporal and palaeogeographic context.
Hopane/Sterane ratios and primary producers from the Tonian to Phanerozoic
To place the Ediacaran biomarkers from the White Sea area into a broad temporal context, Fig. 2 summarizes data for bacterial hopanes and algal steranes from the Tonian to the present. Based on biomarkers, bacteria were the only notable primary producers in Paleo- and Mesoproterozoic oceans31. Primitive eukaryotic sterane signatures emerged ~900–800 Ma ago15,32, although the overall H/S ratio remained high (70% of values are H/S > 29.5, and steranes are below detection limits in 43% of samples that contain hopanes). Moreover, it is unclear whether steranes in Tonian sediments are derived from algae or other organisms15. The first signs of unambiguous algal productivity occurred in a single sample assigned to the Cryogenian, around 650 Ma, and started to be a dominating signal from the very beginning of the Ediacaran, close to 635 Ma15,33. This ‘rise of algae’ was marked by an order-of-magnitude drop in H/S ratios and the emergence of a near-modern sterane diversity (Fig. 2a, b). Phanerozoic sediments, in contrast to the Tonian, mainly demonstrate continuously low H/S values, (H/S = 0.5–5 range accounts for 70% percentile with the mode at 1.3), indicating that algae have been key primary producers for the past 541 million years.
a The relative abundance of the sterane homologues cholestane (C27, green), ergostane (C28, blue) and stigmastane (C29, green). Size of the coloured areas reflects relative sterane abundances. b Evolution of the relative abundance of bacterial hopanes over eukaryotic steranes (H/S) through time (orange = Tonian and Cryogenian; yellow = Ediacaran (data from Oman and Siberia); blue = Phanerozoic); the scale goes from H/S ~ ∞ (with no steranes detected) to H/S = 0.25, converted from the S/H ratio values from 0 to 4 in Brocks et al.15. Histograms showing the abundance distribution of H/S values for different periods and locations: c Phanerozoic biomarker data reported in the literature; d Ediacaran of the South Oman Salt Basin and the Siberian platform; e Ediacaran of the White Sea area; f previous biomarker analyses on the Ediacaran of the EEP (localities are marked as orange circles on Fig. 1); g Tonian and Cryogenian biomarker data reported in the literature. Data from the EEP from Pehr et al.17, data for the White Sea this study, all other data recalculated from Brocks et al.15.
The Ediacaran, however, yields bitumens with H/S signatures resembling both the Tonian and Phanerozoic. Sediments from the Oman Salt Basin and the Siberian platform demonstrate H/S values similar to the Phanerozoic (Fig. 2c, d) (H/S = 0.75–1.4 range accounts for 70% percentile with the mode value 1.3). By contrast, bitumens from the Ediacaran interior seaway of the EEP17 include numerous elevated H/S values up to 119 (H/S = 1.5–12.5 range accounts for 70% percentile with several modes, and median value 7.7), values otherwise typical for the Tonian (Fig. 2f). It has been suggested17 that the elevated H/S values in the interior seaway of the EEP, just as those from the Tonian15,16, might reflect a strong predominance of bacteria among primary producers, potentially due to regionally oligotrophic conditions, thus highlighting a high spatial heterogeneity in primary producer communities in Ediacaran marine environments (though see Supplementary Note 2)17.
Based on the H/S data from global Ediacaran sediments, the Ediacara biota might have either inhabited newly established algae-rich environments15,16 or, conversely, thrived in nutrient-depleted ecosystems dominated by bacterial primary productivity akin to the Tonian or Mesoproterozoic17,20. If latter hypothesis is correct, then the diet and ecology of organisms of the Ediacara biota must have been very distinct from most Phanerozoic animals17,19,20, and it would invalidate the premise that the emergence of abundant algal food sources was crucial for the ecological success of eumetazoan animals. Biomarker data from sediments directly associated with Ediacara biota fossils can shed light on this dispute.
Primary producers at the Ediacara biota localities
The clay and sandstone material directly surrounding Ediacara biota fossils in the White Sea sections demonstrate low H/S ratios (H/S = 2.5–5) (Fig. 3). The overall H/S values from the whole set of White Sea area sediments vary slightly more broadly (H/S = 1–7 range accounts for 70% percentile with the mode value 3.3, n = 59; Fig. 2e). The H/S value for the only sample that has been reported from the Ediacara biota localities in Arctic Siberia (H/S = 2.7)34 falls near the mode value for the White Sea area, although it is impossible to judge whether this sample is representative of the whole section. These H/S values suggest that the Ediacara biota inhabited environments with near-modern fluxes of bacterial versus eukaryotic biomass (Fig. 3). Moreover, steranes of the White Sea area are strongly dominated by stigmastanes (C29 (%) = 75 ± 9% of C27–C29 sterane homologues; n = 59). The C29 predominance among steranes in the White Sea area is characteristic of Ediacaran biomarker signatures and likely reflects predominance of green algae among eukaryotes35. The mode of H/S value in the White Sea area is somewhat elevated in comparison to the Phanerozoic (Fig. 2c, e). This elevation may reflect a stronger relative contribution of planktonic cyanobacterial biomass than the average Phanerozoic, but is more likely associated with benthic cyanobacterial mats that are widespread in White Sea sediments and generally abundant in Ediacaran shallow-water environments36,37. Regardless, Ediacaran macroorganisms of the White Sea area inhabited environments that were orders of magnitude enriched in algal relative to bacterial food sources when compared with the Tonian, and in this respect similar to Phanerozoic marine habitats.
a Aspidella and Kimberella from the Z11(XXII) surface (Zimnie Gory, photo by E. Uryvaeva); b Andiva from the Z1(1) surface (Zimnie Gory), the surface also contains Archaeaspinus, Armilifera, Brachina, Charniodiscus, Cyanorus, Cyclomedusa, Dickinsonia, Inaria, Ivovicia, Kimberella, Onega, Paravendia, Parvancorina, Temnoxa, Tribrachidium, Yorgia27; c Dickinsonia (Lyamtsa); d Palaeopascichnus (Lyamtsa). n.m., not measurable.
Primary producers and early animal evolution
The rise of algae 650-635 Ma has changed the ecosystems on our planet forever, although the trigger for this phenomenon is unclear. It has been proposed that a potential increase in nutrient levels in the oceans at that time could have made algae more competitive relative to photosynthetic bacteria15,16, or alternatively that protistan eukaryotes or bacteriovorous sponge-grade animals effectively reduced bacterial biomass, thus providing ecospace for algae6,7,33,38,39,40. Whatever the causes for the proliferation of planktonic algae, their biomass may have fuelled the radiation of eumetazoan animals by increasing the efficiency of nutrient and energy transfer to higher trophic levels based on larger cells sizes compared with bacterial phytoplankton, and by supplying fast sinking food particles to benthic animal communities at the sea floor15,16. However, this is to ignore that microbial mats were present in the oceans long before algal food became available. With the discovery of a motile lifestyle among the earliest branching Eumetazoa (Placozoa and Ctenophora41), pervasive cyanobacterial mat coverage in well-oxygenated shallow-water environments would have provided ample resources for metazoan proliferation. Yet, the vast majority of extant eumetazoan animals prefers a eukaryote-dominated diet; with rare exceptions, eumetazoans are not sustained by purely bacterial food sources42,43. A preference for a eukaryotic diet may thus be the ancestral state of Eumetazoa, possibly due to the high nutritional quality of algal biomass.
Based on sedimentological evidence28 and biomarker data presented here, the Ediacara biota of the EEP inhabited well-mixed oxygenated shallow-water environments with levels of potential algal food supply comparable to the Phanerozoic. This observation in the White Sea area is consistent with a recent spatial analyses of ~570 Ma old Ediacaran ecosystems on the Avalon Peninsula, overlapping with the White Sea area taxonomically, that showed that competition for resources was not the driving factor for local Ediacaran communities44. Unlike previously predicted17,19,20, bacteria-dominated ecosystems in Ediacaran marine basins were generally not a cause of the unusual appearance and ecology of the Ediacara biota. Rather, the ecological and evolutionary bridge leading from a mid-Proterozoic bacteria-dominated world to the appearance of Phanerozoic animal-dominated ecosystems was paved with algae-rich environments akin to those preferred by modern eumetazoan animals. Although morphologically and possibly phylogenetically distinct from Phanerozoic animals, the large organisms of the Ediacara biota were a part of newly established nutrient and energy-rich environments that later hosted the Cambrian diversification of animal life.
Source: Ecology - nature.com
