The fungal and acritarch events as time markers for the latest Permian mass extinction: An update

The fungal and acritarch events as time markers for the latest Permian mass extinction: An update

Accepted Manuscript The fungal and acritarch events as time markers for the latest Permian mass extinction: An update Michael R. Rampino, Yoram Eshet ...

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Accepted Manuscript The fungal and acritarch events as time markers for the latest Permian mass extinction: An update Michael R. Rampino, Yoram Eshet PII:

S1674-9871(17)30122-6

DOI:

10.1016/j.gsf.2017.06.005

Reference:

GSF 580

To appear in:

Geoscience Frontiers

Received Date: 24 April 2017 Revised Date:

23 June 2017

Accepted Date: 29 June 2017

Please cite this article as: Rampino, M.R., Eshet, Y., The fungal and acritarch events as time markers for the latest Permian mass extinction: An update, Geoscience Frontiers (2017), doi: 10.1016/ j.gsf.2017.06.005. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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The fungal and acritarch events as time markers for the latest Permian mass extinction: An update Michael R. Rampinoa,b,*, Yoram Eshetc a

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Departments of Biology and Environmental Studies, New York University, New York NY 10003, USA

b

NASA, Goddard Institute for Space Studies, New York, NY 10025, USA

c

Open University of Israel, 1 University Road, Raanana 4353701, Israel

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*Corresponding Author: [email protected]

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ABSTRACT

The latest Permian extinction (252 Myr ago) was the most severe in the geologic record. On land, widespread Late Permian gymnosperm/seed-fern dominated forests appear to have suffered rapid and almost complete destruction, as evidenced by increased soil erosion and changes in fluvial style in deforested areas, signs of

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wildfires, replacement of trees by lower plants, and almost complete loss of peatforming and fire-susceptible vegetation. Permian–Triassic boundary strata at many sites show two widespread palynological events in the wake of the forest destruction: The fungal event, evidenced by a thin zone with >95% fungal cells

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(Reduviasporonites) and woody debris, found in terrestrial and marine sediments, and the acritarch event, marked by the sudden flood of unusual phytoplankton in the marine realm. These two events represent the global temporary explosive spread of

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stress-tolerant and opportunistic organisms on land and in the sea just after the latest Permian disaster. They represent unique events, and thus they can provide a time marker in correlating latest Permian marine and terrestrial sequences.

Keywords: Permian-Triassic boundary; fungal event; acritarch event

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1. Introduction The latest Permian period (~252 Myr) saw the largest mass extinction recorded in Earth's history, affecting marine and non-marine invertebrates, vertebrates

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(Erwin, 2006), and more than 95% of Late Permian arborescent gymnosperm plant species, including the widespread Glossopteris flora of Gondwanaland (e.g., Retallack, 1995; Visscher et al., 1996; Looy et al., 1999; Tewari et al., 2015). The extinction event was apparently abrupt, and seems to have been synchronous in the

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oceans and on land (Twitchett et al., 2001; Sephton et al., 2002, 2009). Recovery of the post-extinction Triassic ecosystems was slow. Stable, complex ecosystems in the sea and on land most likely did not develop until the Middle Triassic (as illustrated by

(Chen and Benton, 2012).

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the lack of coal deposits and coral reefs in the Early Triassic), as much as 4 Myr later

The apparently rapid extinction of terrestrial plants seems to record a disaster that was marked by the disappearance of forests in many areas. Not only were trees apparently killed outright, the dominant tree species became extinct, which means that

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conditions were such that there were probably few refugia for survivors of the disaster. Evidence of abundant charcoal, black carbon and polycyclic aromatic hydrocarbons (PAHs) coincident with the latest Permian extinctions suggests that wildfires were widespread at that time, which may partially account for the forest

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destruction (Grice et al., 2007; Shen et al., 2011). The lack of evidence for wildfires during the subsequent Early Triassic (the so-called “charcoal gap”) may have been a

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function of a paucity of forest trees to fuel such fires (Abu Hamad et al., 2012). Furthermore, the occurrence of destructive acid rain is indicated by recent work suggesting that forest soils suffered severe acidification (with pH < 4) at the same time (Sephton et al., 2015). In many places in the world, the devastation of forests of the latest Permian was followed by a brief interval when fungi became widespread, probably taking advantage of the large amounts of dead and decaying biomass. Visscher et al. (1996) reported this occurrence worldwide, and several additional sites have been reported since (e.g., marine and terrestrial sections in South China) (Fig. 1). The event was most likely rapid, as gradual change would not produce, at any one time, the amount 2

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ACCEPTED MANUSCRIPT of woody material required for such a widespread outbreak of fungi, and there is no mixture of fungal cells with gymnosperm pollen. The recovery of terrestrial vegetation involved a period when lower plants such as ferns and lycopsids (club mosses, spike mosses and quillworts) replaced the forest trees. Arborescent gymnosperms became abundant again only after some time, and with new species. In

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the oceans, primary productivity seems to have been depressed (Rampino and Caldeira, 2005), and opportunistic marine organisms suddenly increased in numbers. In this paper, we discuss the nature of two major events associated with the latest Permian: the fungal event (FE) and the acritarch event (AE), and interpret them

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as reflecting an abrupt latest Permian widespread environmental disaster. These events, found in a number of P-T boundary sections worldwide can provide a timeline for

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correlating marine and terrestrial sections. 2. The fungal event

The fungal event (FE) (or fungal spike) is a term used to describe a thin layer, found widespread in non-marine and marine sediments, at the time of the latest Permian extinction. The zone contains a high abundance of fungal remains

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(commonly > 95%) in the form of single cells or chains of cells, which are interpreted to represent the hyphae and sexual reproductive spores of ascomycete fungi (Fig. 2). In many localities, the FE layer is devoid of any other palynomorphs, but contains much land-derived woody debris (e.g., Foster, 1979; Eshet et al., 1995; Visscher et

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al., 1996; Looy, 2000; Foster et al., 2002; Steiner et al., 2003; Sephton et al., 2005; Sandler et al., 2006; Wang and Visscher, 2007; Metcalfe et al., 2009). The fungal

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remains are referred to Reduviasporonites (Wilson, 1962). Elsik (1999) argued that Reduviasporonites is the senior synonym of Tympanicysta (Balme, 1979) and Chordecystia (Foster, 1979) – names used in earlier studies. Reduviasporonites ranges at least from the Capitanian to the Early Triassic, but usually in low abundance. According to Elsik (1999), Reduviasporonites has morphologic characteristics similar to the modern fungus Rhyzoctonia, which can be pathogenic under conditions of ecological stress. Based on a relatively low δ13C signature in Reduviasporonites, and the dominance of n-alkene/n-alkane doublets in the pyrolysis products of its cell walls, Foster et al. (2002) expressed reservations concerning the fungal nature of the 3

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ACCEPTED MANUSCRIPT microfloral remains in the FE zone. Ouyang and Utting (1990) had earlier suggested that they might be of algal origin. Afonin et al. (2001) related Reduviasporonites to fresh-water green algae, and explained their abundance at the Permian–Triassic boundary as representing the spread of large ponds and river systems that they supposed to have existed at the time. Recently, Spina et al. (2015) also supported an

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algal affiliation for Reduviasporonites. Hochuli (2016) proposed that the fungal cells were recent contamination, but why this should take place only in samples near the PT boundary is not explained.

Other studies, however, have provided convincing evidence for the fungal

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nature of Reduviasporonites (Visscher et al., 2011). Sephton et al. (1999, 2009) found that carbon and nitrogen isotopes, as well as carbon/nitrogen ratios in

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Reduviasporonites are consistent with a fungal origin. A fungal source was also supported by the geochemical analysis of aromatic hydrocarbons in the latest Permian in the Peace River (Western Canada), Meishan (South China) and Kap Stosch (East Greenland) sections (Nabbefeld et al., 2010).

Sawada et al. (2012) reported that the aromatic compounds in the latest

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Permian layer in the GSSP Meishan, China section could most likely be attributed to fungi and lichens. Also in the GSSP section, Grice et al. (2009) identified a spike of perylene that is most likely derived from perylenequinone pigments of wooddegrading fungi. Matson et al. (2005) reported alkyl napthalene and oxygen-

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containing aromatic compounds (e.g., xanthones) that may be generated by lower plants and fungi, from a marl bed at the latest Permian extinction level in Italy. Furthermore, the identification of Reduviasporonites as fungus is actually illustrated

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by Cirilli et al. (1998), who show (their Plate IV, 1) Reduviasporonites cells infesting woody debris in the uppermost Permian in Italy.

Fungi are known to be among the first colonizers after forest destruction

(Carpenter et al., 1987; Claridge et al., 2009). So-called “fire fungi” commonly spread on downed trees after forest fires and other destructive events. For example, soon after the forest devastation in the 1980 Mt St. Helens eruption, networks of fungal mycorhizae were seen spreading among the fallen logs (Foxworthy and Hill, 1980). Similar widespread growth of fungus on downed trees was observed on the island of Montserrat, after a volcanic eruption in 1995 destroyed part of the island’s tropical 4

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ACCEPTED MANUSCRIPT rainforest (pers. comm. to M.R.). Furthermore, studies have also shown that modern terrestrial fungi proliferate in dying forests that are affected severely by acid precipitation (e.g., Hudson, 1968; Abrahamsen et al., 1993; Dix and Webster, 1994; Wang et al., 2012). The fungal event was first reported from marine sediments of the oolitic

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Tessero Horizon, which represents the transition from Permian to Triassic deposits in the Southern Alps in Italy (Visscher and Brugman, 1986, more recently supported by Spina et al., 2015), and later from several Permian–Triassic boundary sections in southern Israel (Eshet, 1990; Eshet et al., 1995). Today, the FE is reported globally

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(Fig. 1) (e.g., Eshet et al., 1995; Vischer et al., 1996; Steiner et al., 2003; Peng and Shi, 2009; Bercovici et al., 2015, and sources therein), mainly from shallow-marine

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sequences where fungal cells were transported from land, but also from non-marine sections, such as in South Africa (Steiner et al., 2003), and China (Yin et al., 2007a,b; Cao et al., 2008; Peng and Shi, 2009; Bercovici et al., 2015; Cui et al., 2015; Bercovici and Vajda, 2016), so these are definitely not marine fungi.

In both the marine and the non-marine realms, the FE coincides closely with

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the latest Permian mass extinction (e.g., Kozur, 1998; Twitchett et al., 2001; Peng and Shi, 2009; Schneebeli-Hermann et al., 2013, 2015), and with a negative excursion of δ13C in carbonates and organic material that occurs in the latest Permian (e.g., Sephton et al., 2009; Korte and Kozur, 2010; Schneebeli-Hermann et al., 2013). The

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FE is recognized as a potential marker for the end of the Permian in both marine and non-marine sediments (Looy, 2000; Looy et al., 2001; Steiner et al., 2003; Bercovici

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et al., 2015). Although the FE may be absent in some places, the thin interval of sediment

representing

the

event

(with

an

overwhelming

abundance

of

Reduviasporonites) could easily have been missed in some studies of the P-T boundary, due to widely spaced sampling intervals (e.g., Pittau 2001; Michaelsen 2002; Hochuli et al., 2010a, b; Jha et al., 2012; Zhang et al., 2015). For example, in the Meishan, China GSSP section, with accumulation rates calculated to be as low as 0.4 cm per kyr (Burgess et al., 2014), the brief fungal event would be an easily missed zone only 1.2 to 2 cm thick.

3. The acritarch event

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ACCEPTED MANUSCRIPT Acritarchs are organic-walled microfossils that are interpreted as unicellular marine algae, but are an artificial and rather heterogeneous group (Riegel, 2008). According to Katz et al. (2004) and Shen et al. (2013), the Paleozoic and Early Triassic acritarchs are the remains of primary producers that pre-dated more modern forms, such as dinoflagellates and diatoms. Riegel (2008) has shown that acritarch

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diversity has gone through great changes with time in response to variations in seawater chemistry, nutrient availability and atmospheric composition. This includes the so-called “Phytoplankton Blackout” from the Carboniferous through the Triassic periods, when acritarchs either disappeared or became rare (Riegel, 2008). Some

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major crises in the oceans, as have occurred at the Triassic–Jurassic boundary (van de Schootbrugge et al., 2007), and at the K-Pg boundary (Vajda and McLoughlin, 2004,

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2007), are marked by blooms of acritarchs.

Abundant acritarchs, mainly belonging to the broad form-genera of Veryhachium, Micrhystridium, Dictyotidium and Leiosphaeridia (Fig. 3), forming the acritarch event (AE) (or acritarch spike), are reported widely from Permian–Triassic marine sections, becoming especially abundant in the aftermath of the marine extinction event, and commonly just after the appearance of the FE in marine

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sediments (Visscher and Brugman, 1988; Brinkhuis and Visscher, 1994; Eshet et al., 1995; Retallack, 1995; Vajda and McLoughlin, 2007; Lei et al., 2013; Luo et al., 2013). The AE is also marked in several widespread sections by a biomarker (C33 n-

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alkylcyclohexane) that may be specific for acritarchs (Grice et al., 2005). These acritarchs probably represent stress-tolerant phytoplankton (Lei et al., 2013; Luo et al., 2013), which were apparently among the first pioneering primary

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producing planktonic organisms to temporarily bloom in the oceans in the wake of the devastated marine ecosystems at the end of the Permian (e.g. Downey, 1972; Grice et al., 2005; Lei et al., 2013; Schneebeli-Hermann, 2013; Shen et al., 2013). In support of this, Vecoli and Le Herisse (2004) noted a proliferation of Veryhachium and Micrhystridium species during a Late Ordovician drop in general acritarch diversity, and conclude that those species represent ecologically more tolerant forms of phytoplankton.

4. Palynological changes across Permian–Triassic boundary 6

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ACCEPTED MANUSCRIPT We suggest that the profusion of fungi, represented by the FE, which are found in both terrestrial and marine sediments, can be most useful in creating a reliable land-sea correlation, as well as a chronological and spatial reconstruction of the ecological events before, during and after the latest Permian extinction. Studies that investigated ecosystem recovery after the latest Permian crisis

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(e.g. Retallack, 1995; Looy et al., 1999, 2001; Vajda and McLoughlin, 2007; Yin et al., 2007; Hochuli et al., 2010; Peng and Shi, 2009; Bercovici et al., 2015) report that after the forest ecosystems disappeared, non-arboreal lycopsids began to spread over the land. Schneebeli-Hermann et al. (2013) reported a decrease in pteridosperms (seed

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ferns) and gymnosperms (conifers), and an increase in lycopsids (e.g., club mosses) after the extinction event. The main floral turnover from forests to low-lying

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vegetation may have taken less than 10,000 years (Hochuli et al., 2010). In their detailed study of Permian–Triassic boundary sections in Israel, Eshet et al. (1995) constructed a model of four discrete palynological stages that occurred consistently in latest Permian marine sections: (1) diverse Late Permian forest flora of mainly gymnosperms, seed-ferns and rare lycopsids, (2) the fungal event: where

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fungal remains and recycled woody debris make up ~95% of the material in marine and non-marine palynological assemblages, (3) the acritarch event: where acritarchs dominate in shallow marine environments, with small amounts of lycopsids and gymnosperms introduced from the land, and (4) a dramatic decrease in acritarch

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abundance, followed by a gradual increase in diversity of gymnosperm pollen, until full recovery of forests is achieved by the Middle Triassic, about 4 million years after the extinction event. Vajda and McLoughlin (2004, 2007) showed great similarities

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between the palynological records of the end-Cretaceous and latest Permian mass extinction events, with similar FE and AE marking the times of both crises.

5. Discussion

Saprophytic fungi are among the major groups of decomposers, particularly efficient in the rapid degradation of woody tissues under aerobic conditions (Dix and Webster, 1994). Furthermore, fungi are known to adapt and respond quickly to environmental stress and disturbances. Sawada (2012) termed them "disaster biota", suggesting that they are the pioneering colonizers of terrestrial ecosystems after forest

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ACCEPTED MANUSCRIPT destruction by agents such as fire, volcanic eruptions, and acid rain (e.g., Hudson, 1968; Abrahamsen et al., 1993; Dix and Webster, 1994; Likens et al., 1996; Likens, 2013). The consistent evidence for a widespread distribution of fungi in the latest Permian suggests that there must have been a large volume of decomposing arborous

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organic matter available that could serve as a substrate for the growth of heterotrophic decomposers. The most probable source of such organic matter was the destruction of Late Permian forests. The increased soil erosion that came from a loss of forest trees would have aided transport of the fungal cells and woody debris to the sea. The FE

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was apparently short-lived. In the marine Tesero section in Italy, where sedimentation rates of ~10 cm/kyr have been suggested (based on estimates from the Gartnerkofel

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core from the adjacent Carnic Alps, where the thicknesses of latest Permian and earliest Triassic sedimentary units are about the same; see Rampino et al., 2002), the ~50 cm FE zone would comprise about 5000 years. The marginal marine P-T boundary in Israel shows the FE restricted to less than 50 cm of sediment, or less than 6500 years, based on estimates of sedimentation rates (Sandler et al., 2006). In the Karroo Basin, in a non-marine section, the FE is about 100 cm in thickness (Fig. 4).

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At estimated sedimentation rates of about 35 cm/kyr for the Balfour Formation (Steiner et al., 2003), the event would have lasted roughly 3000 years, probably ended by the depletion of available decaying woody organic matter, and the recovery of

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lower plants.

In the oceans, the combined effect of severe global warming in tropical surface ocean waters (Joachimski et al., 2012; Sun et al., 2012), oceanic anoxia (Korte

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and Kozur, 2010; Payne and Clapham, 2012; Dustira et al., 2013) and sea-surface acidification, could have contributed to the marine latest Permian extinction, eliminating most primary producers in the sea (Payne and Clapham, 2012; Retallack et al., 2011; Retallack, 2013). This could have created a ‘Strangelove Ocean’ situation, with a severe reduction in marine productivity and/or in carbon cycling in the ocean (Rampino and Caldeira, 2005). A Strangelove Ocean is suggested by the worldwide negative excursion of δ13C seen in marine and terrestrial sections (Korte and Kozur, 2010). The lack of competition from other phytoplankton could have resulted in blooms of stress tolerant taxa such as acritarchs.

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ACCEPTED MANUSCRIPT Despite extensive research, the causes of the latest Permian extinctions that led to the fungal and acritarch events remain enigmatic. Many researchers propose that huge emissions of CO2, SO2 and halogens from the Siberian Traps eruptions acted as the trigger for a chain of events that culminated with the latest Permian ecosystem collapse on land and in the oceans, which appear to have been synchronous (e.g.,

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Kozur, 1998; Twitchett et al., 2001; Sephton et al., 2002, 2009; Benton and Twitchett, 2003). These emissions could have resulted in short-term global cooling from sulfate aerosols (Kozur, 1998), a longer-term extreme global warming (from CO2 and CH4) (Benton and Twitchett, 2003; Sun et al., 2012), surface-ocean anoxia/euxinia (and

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release of toxic H2S) (Isozaki, 1997), and acidification of the land and the upper surface of the ocean (from CO2 and SO2) (Sephton et al., 2015). Destruction of the ozone layer (from volcanic HCl) (Payne and Clapham, 2012; Black et al., 2013),

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could have contributed to observed mutagenesis seen in some latest Permian palynomorphs (Vischer et al., 2004; Foster and Afonin, 2005). Environmental conditions may have been so severe as to delay the return of gymnosperm-dominated forests by recovery from refugia, and by the evolution of new species, until the MidTriassic. The widespread nature and uniqueness of the fungal event, its close

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relationship with the latest Permian mass extinction and carbon-isotope excursions, and its occurrence in marine and non-marine sediments worldwide should make it an

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ACCEPTED MANUSCRIPT Figure Captions Figure 1. Location of Permian–Triassic marine and non-marine boundary sections containing evidence for the fungal event (for references, see Visscher et al., 1996, and text). Locations are approximate. Some locations have multiple sections showing the Fungal event: 1. Karoo Basin, South Africa; 2. Mombasa Basin,

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Kenya; 3. Morondava Basin, Madagascar; 4. Salt Range, Pakistan; 5. Ranjani Basin, India; 6. Bonaparte Gulf Basin, Australia; 7. Sydney Basin, Australia; 8. Bowen Basin, Australia; 9. Banda Sea; 10. Saudi Arabia; 11. Negev, Israel (several sites); 12. Tunisia; 13. Southern Alps, Italy (several sites); 14. Dinarides,

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Bosnia; 15. Kazakhstan; 16. British Isles; 17. North Sea; 18. Zechstein Basin, Germany and Poland; 19. Moscow Basin, Russia; 20. South China (several sites);

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21. East Greenland; 22. Sverdrup Basin; 23. Northern Alaska; 24. Barents Sea; 25. Svalbard; 26. Pechora Basin, Russia; 27. Tunguska Basin, Siberia; 28. Bukk Mts., Hungary; 29. South Anatolia, Turkey; 30. Peace River Basin, Canada. Figure 2. Fungal cells (Reduviasporonites) from the fungal event zone, with typical increase in woody debris (from the Negev, Israel, Zohar 8 borehole

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Figure 3. Sample of acritarchs (Veryhachium) from the acritarch event zone

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Figure 4. Carlton Heights, South Africa non-marine section of the Permian– Triassic boundary showing the extinction of Late Permian palynomorphs, the burst of fungal remains and woody debris, and first appearances of typical Early Triassic palynomorphs. The fungal event here is one meter thick (Steiner et al., 2003).

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The fungal and acritarch events as time markers for the latest Permian mass extinction: An update Michael R. Rampinoa,b,*, Yoram Eshetc a

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Departments of Biology and Environmental Studies, New York University, New York NY 10003, USA b NASA, Goddard Institute for Space Studies, New York, NY 10025, USA c Open University of Israel, 1 University Road, Raanana 4353701, Israel *Corresponding Author: [email protected] (Rampino)

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1. The latest Permian mass extinction is marked by a fungal event in marine and non-marine sections 2. The latest Permian mass extinction is marked by an acritarch event in marine sediments. 3. The fungal event and the arcritarch events represent disaster ecologies that were dominant in the wake of the severe mass extinction on land and in the sea. 4. Reduviasporonites represents wood-degrading fungus, and does not have an algal origin.