End-Permian terrestrial disturbance followed by the complete plant devastation, and the vegetation proto-recovery in the earliest-Triassic recorded in coastal sea sediments

https://doi.org/10.1016/j.gloplacha.2021.103621Get rights and content

Highlights

  • Vegetation collapses occurred twice before and at the end-Permian marine extinction.

  • They were followed by the complete plant devastation in the Permian.

  • A subsequent vegetation proto-recovery occurred in dozens of kyr after the EPE.

  • Timing of the proto-recovery varied among areas.

  • Cyanobacterial blooms occurred during those times of environment deterioration.

Abstract

The Permian−Triassic mass extinction was the most severe biotic crisis of the past 540 million years, eliminating 80–90% of species in the ocean and ~ 70% of land-based vertebrate families. Researchers have debated whether terrestrial vegetation collapse occurred before or after the marine extinction, or if they were synchronous. We analyzed the ratios of normal alkanes of terrestrial plant origin to total normal alkanes (terrestrial plant index) as well as those of pristane to phytane, which are affected by terrestrial plant inflow and ocean redox, in shallow marine, terrestrial lagoon, and central deep-ocean sedimentary rocks from China, Italy, India, and Japan to elucidate the terrestrial vegetation history. Interpretation of pristane/phytane ratios was conducted through comparison with other seawater redox indices. Both proxies indicate that two terrestrial vegetation collapses occurred, before and at the end-Permian marine extinction in the coastal sea environment, followed by the complete plant devastation, and a subsequent terrestrial vegetation proto-recovery in the earliest Triassic. The two proxies showed opposite patterns in a terrestrial lagoon setting section, and those from a central deep-ocean setting indicate that little terrestrial plant material reached the central ocean. These differing responses of the pristane/phytane ratios among geographical settings are consistent with natural phenomena, indicating that the method proposed in this study results in valid reconstruction of vegetation changes. Cyanobacterial blooms occurred from the end-Permian vegetation collapse until after the massive plant-soil erosion, suggesting that terrestrial ecosystem disturbance caused deterioration of the environment for eukaryotic algae in the coastal sea and terrestrial lagoon.

Introduction

Mass extinctions, which are characterized by a fundamental restructuring of marine and terrestrial ecosystems, have long garnered attention. They reflect the complex feedback mechanisms among environmental change and biotic evolution (Knoll et al., 2007; Sun et al., 2012; Song et al., 2013; Benton and Newell, 2014). The Permian–Triassic (P–Tr) mass extinction was the largest biocrisis of the Phanerozoic era, for causing a series of faunal and floral destabilization episodes that continued for ~5 Myr into the subsequent Triassic Period (Looy et al., 2001; Sun et al., 2012; Chen and Benton, 2012; Hochuli et al., 2016; Chen et al., 2019; Chu et al., 2020, Chu et al., 2021).

Since 1998, five major uranium–lead (Usingle bondPb) geochronological studies have attempted to determine the timing and duration of the extinction (Bowring et al., 1998; Mundil et al., 2001, Mundil et al., 2004; Shen et al., 2011; Burgess et al., 2014). Burgess et al. (2014) constrained the geochronological age of the end-Permian mass extinction (EPE) as 251.941 ± 0.037 Ma (Bed 25 at Meishan). This major extinction episode was followed by the earliest Triassic extinction (ETE) near the ash bed (Bed 28) at 251.880 ± 0.031 Ma in the Meishan section from South China (Song et al., 2013; Burgess et al., 2014; Chen et al., 2015). The entire extinction interval was ~63 kyr, spanning from the EPE in the Clarkina meishanensis Zone to the ETE in the Isarcicella staeschei Zone (Shen et al., 2011; Song et al., 2013; Burgess et al., 2014; Chen et al., 2015), and the second extinction event occurred in a limited area of eastern south China, including the Meishan and Huangzhishan sections (Chen et al., 2002, Chen et al., 2009b, Chen et al., 2015; Huang et al., 2011; Song et al., 2013).

Massive volcanism associated with the formation of the Siberian Traps igneous province is considered a likely driver of the biotic crisis (e.g., Burgess and Bowring, 2015) based on the coincidence of the pyroclastic eruption at 251.901 ± 0.061 Ma (Burgess et al., 2014), laterally extensive sills at 251.907 ± 0.067 Ma (Burgess et al., 2017), and the mass extinction with high Ni concentration (Rampino et al., 2017; Kaiho et al., 2001; Rampino et al., 2017; Burger et al., 2019), suggesting that plume volcanism (Sobolev et al., 2011) occurred at 251.880 ± 0.031 Ma (Burgess and Bowring, 2015) or 251.939 ± 0.031 Ma (Shen et al., 2019). However, these ages have errors of 30 to 70 kyr. Many studies have reported mercury spikes at the end-Permian extinction horizon and debated their possible sources (volcanism or plant soils) (e.g. Sanei et al., 2012; Grasby et al., 2013, Grasby et al., 2019; Wang et al., 2018, Wang et al., 2019; Chen et al., 2018; Shen et al., 2019; Chu et al., 2020; Dal Corso et al., 2020). Coinciding spikes of coronene and mercury indicate precisely synchronous occurrences of volcanism and mass extinction events (Kaiho et al., 2020), as mercury spikes can be caused by volcanism or mass extinction (Grasby et al., 2019; Dal Corso et al., 2020), whereas coronene is not formed due to mass extinctions, but instead due to volcanism and asteroid impacts (Kaiho et al., 2020). The Siberian eruptions may have caused dust clouds and acid aerosols, which would have blocked out sunlight, thereby causing short-term cooling and disrupting photosynthesis both on land and in the photic zone of the ocean, leading to food chain collapse (White, 2002). The blocking of sunlight may also have caused global cooling followed by global warming due to carbon dioxide release from the Siberian eruptions (White, 2002). Theses eruptions may have caused local acid rain when the aerosols washed out of the atmosphere (Schmidt et al., 2015). These global and local climatic impacts may have killed land plants as well as marine benthic and planktonic organisms (Benton, 2018).

The terrestrial mass extinction is evidenced by the mass disappearance of the Gigantopteris megaflora, reduction of palynomorphs, and the last occurrences of plant remains and abundant charcoal fossils of Changhsingian age in South China (Yu et al., 2015; Zhang et al., 2016; Cui et al., 2017). The distinct negative shift of δ13Corg and lithofacies indicate that a dramatic collapse of the soil system occurred, which is associated with rapid deforestation and climatic warming and drying (Zhang et al., 2016; Wu et al., 2020). The marked shifts in the δ13C curve follow the trends of the δ18O records, which suggest that the severe environmental disturbances and terrestrial ecological crisis started during the Changhsingian age (Hochuli et al., 2016; Shen et al., 2018). Rapid climatic drought and die-off of the Glossopteris and Gigantopteris, rapid disappearance of rooted plant life, and dramatic changes in the terrestrial sedimentary environments of South Africa (Ward et al., 2000), North China (Wang and Chen, 2001), Greenland (Twitchett et al., 2001), and Antarctica (Retallack, 2005) suggest a global event. A recent study demonstrated that the collapse of the austral Permian Glossopteris occurred prior to Ni enrichment, corresponding to the EPE and the minimum of δ13Corg (Fielding et al., 2019).

The diversity of terrestrial vegetation significantly decreased prior to the EPE worldwide, and remained at low levels throughout the entire Early Triassic (Retallack et al., 1996; Benton and Newell, 2014; Yu et al., 2015; Zhang et al., 2016; Vajda et al., 2020). Herbaceous lycopsids and/or bryophytes dominated the terrestrial vegetation between the Griesbachian to Smithian (Looy et al., 1999; Galfetti et al., 2007a, Galfetti et al., 2007b; Hochuli et al., 2010; Kurschner and Herngreen, 2010; Hermann et al., 2011; Saito et al., 2013). The terrestrial ecosystem underwent an abrupt change, and woody conifers became dominant over the Smithian–Spathian interval (Galfetti et al., 2007a, Galfetti et al., 2007b; Hochuli et al., 2010; Kurschner and Herngreen, 2010; Hermann et al., 2011; Saito et al., 2013; Zhang et al., 2019). The switch from herbaceous vegetation to woody coniferous vegetation marked the recovery of terrestrial vegetation, which occurred globally within ~2 Myr after the end-Permian crisis (Galfetti et al., 2007a, Galfetti et al., 2007b; Hochuli et al., 2010; Kurschner and Herngreen, 2010; Hermann et al., 2011; Saito et al., 2013).

Terrestrial vegetation collapse has been suggested to have impacted the food chain, leading to vertebrate extinctions (Smith and Ward, 2001). The vertebrate turnover has been interpreted as coinciding with the marine mass extinction event (Ward et al., 2005). Gastaldo et al. (2015) noted that the terrestrial mass extinction occurred before the marine mass extinction based on a Dicynodon-Lystrosaurus assemblage zone older than the marine extinction event. In the marine ecosystem, the sudden disappearance of reef system, a rapid temperature increase of 8–10 °C (Joachimski et al., 2012, Joachimski et al., 2019), and the occurrence of abundant microbialites (Kershaw et al., 2012; Fang et al., 2017; Wu et al., 2017; Chen et al., 2019), suggest that the EPE involved synchronous in marine and terrestrial extinctions (Zhang et al., 2016). The soil erosion event coincided with the EPE, but detailed studies in Meishan, South China, and Bulla, Italy, showed that the soil erosion event preceded the marine extinction event by thousands of years (Kaiho et al., 2016a; Zhou et al., 2017). Recent strontium isotopic and microfacies studies also indicate that terrestrial devegetation or enhanced terrestrial input occurred thousands of years before the marine EPE (Dudás et al., 2017; Tian et al., 2019). Terrestrial ecological disturbance, indicated by the presence of charcoal, occurred during the decrease in δ13Corg associated with the mass extinction in terrestrial sections from South China (Chu et al., 2020). Terrestrial ecosystem collapse twice, once dozens of kyr before and again during the main mass extinction, which correspond to the terrestrial ecological disturbance (Chu et al., 2020; Biswas et al., 2020). Both events coincided with volcanic eruption events evidenced by coincidental coronene and mercury spikes (Kaiho et al., 2020).

Vegetation loss may have occurred prior to the EPE due to aerosol formation in the stratosphere related to Siberian volcanism (Kaiho et al., 2016b, Kaiho et al., 2020), but the association between these events has not yet been confirmed. This possibility depends critically on the relative timing of marine and terrestrial ecosystem collapses and differences in the biotic response between hemispheres (Kaiho et al., 2020), yet previous studies have focused on either the marine or the terrestrial collapse alone, with few attempts to correlate the marine and terrestrial crises (Wignall et al., 2020; Biswas et al., 2020). Vegetation loss could have induced a soil erosion event, which in turn could have increased supply of nutrients leading to eutrophication in nearby shallow seawater (a death-by-siltation mechanism following the collapse of terrestrial biomass; Algeo et al., 2011; Song et al., 2015; Kaiho et al., 2016a, Kaiho et al., 2016b; Vajda et al., 2020). However, the siltation that the marine extinction was caused by increased sediment supply following the collapse of terrestrial vegetation, is not supported, because the boundary interval in paralic Permian−Triassic boundary (PTB) sections of south-western China saw a shut-down of clastic influx with carbonates (including microbialites) replacing mudstones (Wignall et al., 2020).

We studied marine P−Tr boundary sections from China, Italy, India, and Japan, all of which were located at paleolatitudes of 5–15°N and 35°S, to reconstruct the sequence of events surrounding the collapse of terrestrial ecosystems throughout this major crisis interval (Fig. 1).

Section snippets

Geological and stratigraphic settings

We investigated eight sedimentary sections that record the P–Tr interval; namely, the inner-shelf shallow-platform carbonate facies of the Palaeotethys Ocean at Bulla, Italy; a terrestrial lagoon at Xiaohebian, South China; restricted platform facies at Huangzhishan, South China; platform ramp facies at Liangfengya and Meishan, South China; shelf basin facies of alternating mudstone and carbonate at Shangsi, South China; restricted platform facies in the Neotethys at Guryul Ravine, Kashmir,

Fossil analyses

The possible mass extinction horizon can be determined by analyzing changes in the skeletal components of various fossil groups in thin sections (Kaiho et al., 2006; Chen et al., 2015). In this study, we used a modified point-counting method to quantify the occurrence of skeletal fragments of major fossil groups in different horizons under a microscope. Quantitative fossil fragment data for various clades were obtained by examining detailed thin sections, focusing on the microfacies and

Fossils

In Meishan, fossil components of crinoids, fusulinids, corals, bryozoans, ostracods, gastropods, foraminifers, and brachiopods abruptly disappeared at the top of Bed 24e (Kaiho et al., 2006; Chen et al., 2015). The disappearance of fossil fragments in the upper part of Bed 24e is the most distinct horizon in which skeletal fragments of major fossil groups are abruptly eliminated (Fig. 2a). The sharp decline in the abundance and diversity of fossil fragments from the bottom to the top of Bed 24e

Vegetation collapse and proto-recovery

Sea-level changes are thought to impact the ratio of long-chain n-alkanes/n-alkanes. A rapid sea-level drop could have occurred near the EPE (Li et al., 1986; Yin et al., 2014; Xu et al., 2017). In that case, the ratio of long-chain n-alkanes/n-alkane would have increased. However, the ratio decreased in the vicinity of the EPE. In a non-marine section in South China, the same vegetation collapse event was found at CI level C (Biswas et al., 2020). Therefore, the coincidental events reported in

Conclusions

We estimated the following four terrestrial vegetation events:

  • 1)

    The onset of the terrestrial vegetation collapse (end-Permian vegetation collapse 1–EPVC1) occurred several tens of kyr earlier than the EPE in low-latitude Northern Hemisphere sections;

  • 2)

    End-Permian vegetation collapse 2 (EPVC2) occurred just below the end-Permian extinction (EPE);

  • 3)

    The end-Permian complete plant devastation after EPE (EPCD) occurred dozens of kyr after the EPE, near the P–Tr boundary;

  • 4)

    Proto-recovery of terrestrial

Author contributions

K.K. planed this study. K.K., L.T., G.M.B., and Y.L. sampled rocks. M.A., R.K.B., and Z.-Q.C. conducted thin section fossil analyses. Organic geochemical analyses have been conducted by M.A., R.K.B., Y.L., R.S. and K.K. Sample treatment for conodont by Y.L. K.K and M.A. wrote the paper. M.A., K.K., and R.K.B. created figures. All authors discussed on this paper.

Declaration of Competing Interest

None.

Acknowledgments

We thank Jinnan Tong and Haijun Song for providing access to a part of the sections studied, Satoshi Takahashi, and Masahiro Oba for helping with the sampling, Satoshi Yamakita for field work and identification of conodonds, Hideko Takayanagi for measuring carbonate carbon isotope ratios, Megumu Fujibayashi for measuring organic carbon content and organic carbon isotopes, and Noritoshi Suzuki and Taro Hino for providing conodont zones. We also thank two anonymous referees provided insightful

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