Elsevier

Gondwana Research

Volume 61, September 2018, Pages 187-202
Gondwana Research

The formation of microbial-metazoan bioherms and biostromes following the latest Permian mass extinction

https://doi.org/10.1016/j.gr.2018.05.007Get rights and content

Highlights

  • Microbial-metazoan bioherms and biostromes in oxygenated and shallow environments

  • Bacteria, sponges, and microconchids lived synergistically to form bioherms.

  • Layered microbial mats favored carbonate precipitation.

Abstract

After the latest Permian mass extinction event, microbial mats filled the ecological niche previously occupied by metazoan reefs, resulting in widespread microbialites. This study focuses on the lipid biomarker (molecular fossil) and invertebrate fossil records from Neotethyan platform margin sections to understand microbial-metazoan bioherm formation. Here, we find that early Griesbachian thrombolitic and stromatolitic microbialites from Çürük Dag (Turkey) and Kuh e Surmeh (Iran) contain abundant lipid biomarkers, representing input from cyanobacteria, anoxygenic phototrophic bacteria, sulfate-reducing bacteria, and halophilic archaea. The biomarker inventory suggests that the microbialites were constructed by cyanobacteria-dominated microbial mats. Biomarkers of halophilic archaea are interpreted to reflect input from the water column, suggesting that the Neotethys experienced at least episodically hypersaline conditions. We also demonstrate that bacteria, possible keratose sponges (up to 50% of the carbonate is represented by the possible sponges), and microconchids lived synergistically to form microbial-metazoan bioherms in the immediate aftermath of the extinction along the western margin of the Neotethys. Abundant fossils of oxygen-dependent invertebrates (i.e. microconchids, bivalves, gastropods, brachiopods, and ostracods) and foraminifers were also found within these bioherms. The presence of invertebrates in conjunction with abundant molecular fossils of cyanobacteria indicates an oxygenated water column. Even though the presence of the biomarker isorenieratane in microbialites may considered as evidence for euxinic conditions in the water column, its absence in the background sediments rather points to a source organism belonging to the mat community. The new finding of bioherms built in part by metazoans suggests that reef ecosystems underwent a major turnover across the extinction event, and shortens the ‘metazoan reef gap’ to just the uppermost Changhsingian. During the Early Triassic, therefore, reefal ecosystems were able to recover in oxygenated settings since the earliest Griesbachian, albeit in an impoverished state.

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

References (125)

  • S. Crasquin-Soleau et al.

    The events of the Permian-Trias boundary: last survivors and/or first colonisers among the ostracods of the Taurides (southwestern Turkey)

    Comptes Rendus Palevol

    (2002)
  • K.S. Dawson et al.

    Molecular characterization of core lipids from halophilic archaea grown under different salinity conditions

    Organic Geochemistry

    (2012)
  • J.A. DeMello et al.

    Biodegradation and environmental behavior of biodiesel mixtures in the sea: an initial study

    Marine Pollution Bulletin

    (2007)
  • C. Dupraz et al.

    Microbial lithification in marine stromatolites and hypersaline mats

    Trends in Microbiology

    (2005)
  • G. Eglinton et al.

    Gas chromatographic—mass spectrometric studies of long chain hydroxy acids—II

    Tetrahedron

    (1968)
  • M.-B. Forel

    The Permian–Triassic mass extinction: ostracods (Crustacea) and microbialites

    Comptes Rendus Palevol

    (2013)
  • W.J. Foster et al.

    Environmental controls on the post-Permian recovery of benthic, tropical marine ecosystems in western Palaeotethys (Aggtelek Karst, Hungary)

    Palaeogeography Palaeoclimatology Palaeoecology

    (2015)
  • E. Friesenbichler et al.

    Sponge-microbial build-ups from the lowermost Triassic Chanakhchi section in southern Armenia: microfacies and stable carbon isotopes

    Palaeogeography Palaeoclimatology Palaeoecology

    (2018)
  • E. Gelpi et al.

    Hydrocarbons of geochemical significance in microscopic algae

    Phytochemistry

    (1970)
  • J. Haas et al.

    Biotic and environmental changes in the Permian–Triassic boundary interval recorded on a western Tethyan ramp in the Bükk Mountains, Hungary

    Global and Planetary Change

    (2007)
  • L.E. Hays et al.

    Evidence for photic zone euxinia through the end-Permian mass extinction in the Panthalassic Ocean (Peace River Basin, Western Canada)

    Palaeoworld

    (2007)
  • K. Heindel et al.

    Post-glacial microbialite formation in coral reefs of the Pacific, Atlantic, and Indian Oceans

    Chemical Geology

    (2012)
  • K. Heindel et al.

    Biogeochemical formation of calyx-shaped carbonate crystal fans in the subsurface of the Early Triassic seafloor

    Gondwana Research

    (2015)
  • F. Kenig et al.

    Occurrence and origin of mono-, di-, and trimethylalkanes in modern and Holocene cyanobacterial mats from Abu Dhabi, United Arab Emirates

    Geochimica et Cosmochimica Acta

    (1995)
  • S. Kershaw et al.

    A ?microbialite carbonate crust at the Permian–Triassic boundary in South China, and its palaeoenvironmental significance

    Palaeogeography Palaeoclimatology Palaeoecology

    (1999)
  • J. Köster et al.

    Mono-, di- and trimethyl-branched alkanes in cultures of the filamentous cyanobacterium Calothrix scopulorum

    Organic Geochemistry

    (1999)
  • G. Luo et al.

    Microbial-algal community changes during the latest Permian ecological crisis: evidence from lipid biomarkers at Cili, South China

    Global and Planetary Change

    (2013)
  • M. Martinez-Alonso et al.

    Diversity of anoxygenic phototrophic sulfur bacteria in the microbial mats of the Ebro Delta: a combined morphological and molecular approach

    FEMS Microbiology Ecology

    (2005)
  • S.A. Mata et al.

    Origin of Lower Triassic microbialites in mixed carbonate-siliciclastic successions: ichnology, applied stratigraphy, and the end-Permian mass extinction

    Palaeogeography Palaeoclimatology Palaeoecology

    (2011)
  • G.R. McGhee et al.

    Ecological ranking of Phanerozoic biodiversity crises: ecological and taxonomic severities are decoupled

    Palaeogeography Palaeoclimatology Palaeoecology

    (2004)
  • B. Nabbefeld et al.

    An integrated biomarker, isotopic and palaeoenvironmental study through the Late Permian event at Lusitaniadalen, Spitsbergen

    Earth and Planetary Science Letters

    (2010)
  • K.E. Peters et al.

    Effects of source, thermal maturity, and biodegradation on the distribution and isomerization of homohopanes in petroleum

    Organic Geochemistry

    (1991)
  • S.B. Pruss et al.

    A global marine sedimentary response to the end-Permian mass extinction: examples from southern Turkey and the western United States

    Earth-Science Reviews

    (2006)
  • R. Riding et al.

    Geobiology of microbial carbonates: metazoan and seawater saturation state influences on secular trends during the Phanerozoic

    Palaeogeography Palaeoclimatology Palaeoecology

    (2005)
  • S.J. Rowland

    Production of acyclic isoprenoid hydrocarbons by laboratory maturation of methanogenic bacteria

    Organic Geochemistry

    (1990)
  • R. Saito et al.

    Predominance of archaea-derived hydrocarbons in an Early Triassic microbialite

    Organic Geochemistry

    (2015)
  • A. Baud et al.

    Biotic response to mass extinction: the Lowermost Triassic microbialites

    Facies

    (1997)
  • A. Baud et al.

    Calcimicrobial cap rocks from the basal Triassic units: western Taurus occurrences (SW Turkey)

    Comptes Rendus Palevol

    (2005)
  • B.M. Bebout et al.

    UV B-induced vertical migrations of cyanobacteria in a microbial mat

    Applied and Environmental Microbiology

    (1995)
  • K. Becker et al.

    Unusual butane- and pentanetriol-based tetraether lipids in Methanomassiliicoccus luminyensis, a representative of the seventh order of methanogens

    Applied and Environmental Microbiology

    (2016)
  • J.M. Bernhard et al.

    Insights into foraminiferal influences on microfabrics of microbialites at Highborne Cay, Bahamas

    Proceedings of the National Academy of Sciences of the United States of America

    (2013)
  • M. Blumenberg et al.

    Biosynthesis of hopanoids by sulfate-reducing bacteria (genus Desulfovibrio)

    Environmental Microbiology

    (2006)
  • M. Blumer et al.

    Hydrocarbons of marine phytoplankton

    Marine Biology

    (1971)
  • T. Bosak et al.

    A likely role for anoxygenic photosynthetic microbes in the formation of ancient stromatolites

    Geobiology

    (2007)
  • J.S. Bowerbank

    A Monograph of the British Spongiidae

    (1864)
  • J.R. Bray et al.

    An ordination of the upland forest communities of southern Wisconsin

    Ecological Monographs

    (1957)
  • A. Brayard et al.

    Transient metazoan reefs in the aftermath of the end-Permian mass extinction

    Nature Geoscience

    (2011)
  • J.J. Brocks et al.

    Biomarker evidence for green and purple sulphur bacteria in a stratified Palaeoproterozoic sea

    Nature

    (2005)
  • S.I. Bühring et al.

    A hypersaline microbial mat from the Pacific Atoll Kiritimati: insights into composition and carbon fixation using biomarker analyses and a 13C-labeling approach

    Geobiology

    (2009)
  • K.R. Clarke et al.

    Primer v6: User Manual/Tutorial

    (2006)
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