The formation of microbial-metazoan bioherms and biostromes following the latest Permian mass extinction
Graphical abstract
Introduction
Lower Triassic rocks archive the aftermath of the latest Permian mass extinction, the most severe extinction of the Phanerozoic (e.g. McGhee et al., 2004; Stanley, 2016), and record the replacement of metazoan reefs with the widespread deposition of microbialites during the Early Triassic (e.g. Fagerstrom, 1987; Baud et al., 1997; Martindale et al., 2017). Several phases of microbialite formation occurred during the Early Triassic (Lehrmann, 1999; Pruss et al., 2006; Baud et al., 2007; Brayard et al., 2011; Kershaw et al., 2012), but the most widespread and abundant microbialites emerged in the immediate aftermath of the extinction, i.e. the Griesbachian (the first substage of the Triassic).
Based on petrographic studies, the microbialite-forming prokaryotes are thought to include cyanobacteria (Yang et al., 2011; Wu et al., 2014). Due to poor preservation and lack of morphologically distinct features, however, these taxonomic identifications are equivocal. To identify the benthic microbial community involved in the formation of microbialites, lipid biomarkers, i.e. molecular fossils, offer a more robust approach (Peckmann et al., 2004; Reitner et al., 2005; Orphan et al., 2008; Bühring et al., 2009; Heindel et al., 2015). Molecular fossils are a useful tool to reconstruct paleoecosystems, shedding light on the mode of primary production and food webs (e.g. Summons and Walter, 1990; Brocks et al., 2005; Peters et al., 2005). They have previously been used to characterize the environmental conditions associated with the latest Permian mass extinction in the Tethys, Panthalassa, and Boreal oceans (e.g. Grice et al., 2005; Hays et al., 2007; Cao et al., 2009; Nabbefeld et al., 2010; Chen et al., 2011), as well as the formation of post-extinction microbialites (e.g. Xie et al., 2005; Chen et al., 2011; Luo et al., 2013; Heindel et al., 2015). Studies of lipid biomarkers of Griesbachian microbialites are, however, restricted to sites from the Paleotethys in South China (e.g. Xie et al., 2005; Chen et al., 2011; Luo et al., 2013).
The formation mechanisms of Early Triassic microbialites are still under debate. These microbialites have been described as ‘disaster forms’ that either thrived following the partial relaxation of the ecological constraints that typically restricted them from unstressed, normal marine conditions (Schubert and Bottjer, 1992), or in harsh environments that were inhospitable to metazoans (Pruss et al., 2004). In these instances, microbialite formation was hypothesized to have been favored by the upwelling of carbonate-saturated, low-oxygen, and/or alkaline deep water that, moreover, may have suppressed grazing and bioturbation in the aftermath of the extinction (Pruss et al., 2004; Mata and Bottjer, 2011). Alternatively, sea-level changes, light penetration, and clastic input could have had a major controlling effect (Kershaw et al., 2012; Mata and Bottjer, 2012; Bagherpour et al., 2017). However, other studies have noted that the microbialite-forming microbial mats housed small (mostly just a few mm in size) metazoans, including ostracods, microconchids, bivalves, brachiopods, echinoids, crinoids, and gastropods that would have required well-oxygenated conditions (e.g. Payne et al., 2006; Yang et al., 2011, Yang et al., 2015; Forel et al., 2013a, Forel et al., 2013b; Tang et al., 2017; Foster et al., 2018). These observations led some authors to conclude that microbialite formation occurred in at least fluctuating oxic-anoxic conditions (Forel et al., 2013b; Tian et al., 2014). The metazoans are, however, rare (Yang et al., 2011), and Early Triassic microbialites have a low functional diversity (Foster and Twitchett, 2014; Foster et al., 2018). Even though metazoans have been recorded from microbialites, hitherto metazoans have not been attributed to reef building until the Olenekian (Pruss et al., 2007; Brayard et al., 2011; Marenco et al., 2012).
Our understanding of the formation mechanisms of post-extinction microbial-metazoan buildups is, therefore, incomplete. The main aim of this study is to analyze the lipid biomarker (molecular fossil) and invertebrate fossil records from Neotethyan platform margin sections in Turkey (Çürük Dag) and Iran (Kuh e Surmeh) that have hitherto not been studied. We aim to 1) identify the benthic microbial communities and to unravel the mechanisms of microbialite formation in the aftermath of the latest Permian mass extinction, 2) determine how prokaryotes and metazoans interacted in earliest reef-like ecosystems after a mass extinction, and 3) determine whether the occurrence of microbialites reflects a change in seawater chemistry (e.g. Riding and Liang, 2005), the extinction of grazing organisms and declining competition in stressed ecosystems favoring prokaryotes, or a combination of these. To achieve these goals, lipid biomarker data were combined with petrographic and paleontological records.
Section snippets
Geological setting
The sedimentary successions recorded in Kuh e Surmeh and Çürük Dag developed on wide carbonate platforms, along the southwestern margin of the Neotethys (Fig. 1). Today, Kuh e Surmeh is in the Zagros Mountains, Iran (28°32′16.6″N; 052°29′47.6″E), whereas during the Permian-Triassic interval it was located at approximately 20°S on the Arabian Carbonate Platform margin (Fig. 1). Çürük Dag is located in the Taurus Mountains (36°41′32.4″N, 030°27′40.1″E), southwestern Turkey, and was close to the
Lipid biomarker analysis
For lipid biomarker extraction, large (0.5 to 1 kg) samples of microbialites and non-microbial limestones were prepared using a decalcification procedure prior extraction (cf. Birgel et al., 2006). The advantage of the decalcification step is the liberation of the molecular fossils, which are tightly bound to the crystal lattice, enabling the recognition of organisms that were potentially involved in the precipitation process. In the laboratory, all weathered surfaces and veins were removed
Microbialites formed by oxygenic layered microbial mats in the photic zone at the seafloor
The lipid biomarkers detected in the samples comprise chiefly n-alkanes and isoprenoids for both sites (Fig. 4), whereas hopanes (pentacyclic triterpenoids) were found exclusively in Çürük Dag samples. All compounds, but especially isoprenoids were influenced by thermal stress (Rowland, 1990), as indicated by abundant pseudohomologues of head-to-tail linked isoprenoids, derived from the degradation of 2,6,10,14-tetramethylhexadecane (phytane) and 2,6,10,14,18-pentamethylicosane (regular PMI) to
Conclusions
Molecular fossils suggest that the thrombolites and stromatolites from Kuh e Surmeh (Iran) and Çürük Dag (Turkey) were formed by layered microbial mats dominated by cyanobacteria in the upper layers, with anoxygenic phototrophic bacteria and sulfate-reducing bacteria in deeper layers. Molecular fossils of halophilic archaea are interpreted to reflect input from the water column, and imply that the Neotethys Ocean experienced local and/or episodic hypersaline conditions. The Çürük Dag
Acknowledgments
We are grateful to the Geological Survey of Iran for great support during fieldwork, in particular, Hamid Karimi, who is acknowledged for his assistance and encouragement during fieldwork. Micha Horacek helped organizing the fieldwork. We thank Beatrix Bethke for her great assistance in the laboratory. This research was supported by KH's Marie Curie Intra European Fellowship (ET Microbialites 299293) within the 7th European Community Framework Program, and a University of Texas Distinguished
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KH and WJF contributed equally to the manuscript.