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Gondwana Research 25 (2014) 1308–1337

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Gondwana Research

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GR Focus Review Impacts of global warming on Permo- terrestrial ecosystems

Michael J. Benton a,⁎, Andrew J. Newell b a School of Sciences, University of Bristol, Bristol, BS8 1RJ, UK b British Geological Survey, Maclean Building, Wallingford OX10 8BB, UK article info abstract

Article history: Geologists and palaeontologists have expressed mixed views about the effects of the end- mass Received 26 June 2012 on continental habitats and on terrestrial . Current work suggests that the effects on land Received in revised form 20 November 2012 were substantial, with massive erosion following the stripping of vegetation, associated with long-term Accepted 12 December 2012 aridification and short-term bursts of warming and . Wildfires at the Permo-Triassic boundary Available online 31 December 2012 contributed to the removal of forests and the prolonged absence of forests from the Earth's surface for up to 10 Myr. These physical crises on land impinged on the oceans, suggesting tight interlocking of terrestrial Keywords: Mass extinction and marine crises. Levels of extinction on land may well have been as high as in the sea, and this is certainly Permian the case for . The mass extinction seems to have been less profound for and , but it is Triassic hard at present to disentangle issues of data quality from reductions in abundance and diversity. Several Continental killing agents have been proposed, and of these tetrapods may have succumbed primarily to acid rain, Terrestrial mass wasting, and aridification. Plants may have been more affected by the sudden effects of heating and wildfires, and the crisis for insects has yet to be explored. © 2012 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.

Contents

1. Introduction ...... 1309 2. The end-Permian mass extinction and loss of life on land ...... 1309 3. The first 10 million of the Triassic ...... 1310 4. Reconstructing ancient climates ...... 1311 4.1. Sedimentological evidence for ancient climates ...... 1311 4.2. Palaeogeography and climate in the Permo-Triassic ...... 1312 4.3. Numerical climate models ...... 1312 5. Sedimentology of the terrestrial Permo-Triassic boundary interval ...... 1313 5.1. Location and setting of key sections ...... 1313 5.2. General character of PTB terrestrial sections ...... 1313 6. Impact of PTr global warming on geomorphic processes ...... 1315 6.1. Weathering ...... 1315 6.2. Erosion rates in the PTB interval ...... 1316 6.3. Wildfire...... 1318 6.4. Changes in fluvial style ...... 1318 6.5. Changes to lacustrine systems ...... 1319 6.6. Desertification and aeolian activity ...... 1320 7. Evidence for atmospheric change ...... 1320 7.1. ...... 1320 7.2. Oxygen ...... 1321 7.3. Sulphur, chlorine, and fluorine ...... 1321 7.4. Destruction of the (?) ...... 1321 8. Plant through the Permo-Triassic crises ...... 1322 9. Insect evolution through the Permo-Triassic crises ...... 1323

⁎ Corresponding author. E-mail addresses: [email protected] (M.J. Benton), [email protected] (A.J. Newell).

1342-937X/$ – see front matter © 2012 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.gr.2012.12.010 M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 1309

10. evolution through the Permo-Triassic crises ...... 1324 10.1. Changing opinions ...... 1324 10.2. Scaling the vertebrate ...... 1324 10.3. Triassic recovery of ...... 1325 10.4. Regional studies on vertebrate extinction and recovery ...... 1325 10.5. Vertebrate through the EPME crisis ...... 1327 11. Killing agents ...... 1327 11.1. Introductory remarks: advocacy or science? ...... 1327 11.2. as the EPME killer ...... 1328 11.3. Hypercapnia and ocean acidification as the EPME killers ...... 1329 11.4. Global warming as the EPME killer ...... 1329 11.5. Aridity as the EPME killer ...... 1330 11.6. Acid rain and mass wasting as the EPME killers ...... 1331 11.7. Wildfires as the EPME killer ...... 1332 12. Death on land during the EPME ...... 1332 Acknowledgments ...... 1333 References ...... 1333

1. Introduction potential killing consequences of such long-term and short-term changes. Most work on the end-Permian mass extinction (EPME) has fo- cused on marine rather than terrestrial organisms. Killing agents in the oceans have generally been linked to increased CO2 concentra- 2. The end-Permian mass extinction and loss of life on land tions and global anoxia, associated with euxinia (anoxic and sulphidic conditions), hypercapnia (CO2 poisoning), and ocean acidification, al- The model for causation of the EPME has become focused on the though the relative importance of each aspect of this cocktail is debat- consequences of the Siberian Trap volcanic eruptions. The most widely ed (Wignall and Twitchett, 1996; Kump et al., 2005; Knoll et al., 2007; accepted model today (Wignall, 2001; Benton, 2003; Benton and Riccardi et al., 2007; Algeo et al., 2011). For life on land, many killing Twitchett, 2003; Erwin, 2006; Knoll et al., 2007; Algeo et al., 2011; mechanisms have been proposed, but dominant among these have S.-z. Shen et al., 2011; Payne and Clapham, 2012; Retallack, 2012) iden- been long-term and short-term changes in atmospheres and oceans, tifies consequences of the eruption of the Siberian flood basalts including global warming and reduction in the oxygen content of (Reichow et al., 2009) which over a peak eruptive period of around the atmosphere. Global warming could clearly have had an important 600 kyr generated large volumes of sulphate aerosols and carbon diox- role in killing land and plants, and the severity of the effects ide (Fig. 1). Methane was probably a major contributor towards a would depend on the amount and speed of the temperature rise, but runaway through its release from destabilised isotopi- perhaps more importantly on related mass wasting and aridity. For cally light hydrate reservoirs (Berner, 2002) and the thermal metamor- oxygen reduction, only animals would obviously be affected, and sce- phism of Siberian coal measures and organic-rich shales (Retallack et al., narios for selective extinction through hypoxia have been proposed 2006; Grasby et al., 2011). for tetrapods at least (e.g. Huey and Ward, 2005). Decreases in the δ18O ratio of shallow marine biogenic carbonate Much of the evidence for a long-term rise in mean temperature and suggest that seawater temperature during the may fall in mean oxygen content of the atmosphere through the Permian have risen by 6–10 °C (Kearsey et al., 2009). Joachimski et al. Period, have come from global models, notably the Geocarbsulf model (2012) suggest low-latitude surface water warming of 8 °C based of Berner (2006, 2009). Further, the sharp increase in temperature on oxygen isotope records in south China, and these values are con- and the drop in oxygen across the Permo-Triassic boundary (PTB) firmed by palaeosol studies (Retallack, 2012). Temperatures at the have been based on evidence from stable isotopes, palaeosols, leaf sto- are estimated at 32–35° in the earliest Triassic (Joachimski mata, and charcoal distribution (Glasspool and Scott, 2010; Retallack, et al., 2012), and up to 40° at the Smithian–Spathian boundary ( 2012). There are still many questions about the of the long- et al., 2012). term and short-term warming and oxygen reduction processes, and EPME killing models (Fig. 1) are based on the massive volumes of the evidence for both. CO2 that were suddenly pumped into the atmosphere, and led to The killing models for land plants and animals are also open to dis- global warming and the short-term production of acid rain. The acid cussion. First is the difficulty of establishing just how severe were the rain killed plants on land, and this led to massive erosion as regolith effects of the EPME crisis on key terrestrial organisms such as plants, was released, which is indicated by a shift from fine-grained sedi- insects, and vertebrates. Some have stated that there was no extinc- ments deposited in lakes and meandering rivers to conglomeratic tion in each of these major groups, others have indicated a major cri- braided fluvial facies, in Russia, South Africa, Europe, and some sis, and yet others point to more subtle effects of limits on origination other locations (Newell et al., 1999; Ward et al., 2000; Arche and and changes in dominant ecosystems. Second, having determined López-Gómez, 2005). The massive erosion was associated with wild- what may have happened to life, the explanations have sometimes fires, perhaps triggered during the unusually arid conditions (S.-z. been incomplete, and do not necessarily provide a convincing killing Shen et al., 2011; W. Shen et al., 2011). Sedimentation rates in terres- model for all the terrestrial life that disappeared at the time. trial successions increased (Retallack, 1999) and there was an abrupt, Recovery from the EPME has also been extensively discussed increased influx of terrigenous siliciclastics to the oceans (Algeo and (reviewed, Chen and Benton, 2012), with debate focusing on whether Twitchett, 2010; Algeo et al., 2011) associated with soil-derived bio- the post-PTB world suffered a series of climate crises over some markers (Wang and Visscher, 2007). Edie Taylor, in review, noted a 5 Myr or not, the causes of such crises, and their potential effects on criticism of this scenario, that the sedimentary conditions themselves the timing of the recovery of terrestrial life, whether rapid or delayed. in the earliest Triassic, namely high-energy sandstones, are not con- The purpose of this review is to consider the evidence both for the ducive to preservation of plant , and so their absence could be physical aspects of climate and atmospheric change on land, and the more apparent than real. Indeed, it would seem unlikely that all 1310 M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337

SIBERIAN TRAPS ERUPTIONS

SO 2 emissions CO 2 emissions Thermogenic methane

Increased Increased Acid continental seawater rain faster weathering 87Sr/86 Sr Global warming reaction rates

Increased Soil TERRESTRIAL Positive marine C-isotope erosion MASS EXTINCTION productivity excursion

Oceanic anoxia Negative Disturbed landscapes C-isotope siltation excursion Abundant MARINE microbial MASS EXTINCTION growth

Fig 1. Model of likely environmental consequences of the eruptions, showing the flows of consequences of global warming and acid rain. Causal links are indicated by solid arrows, and possible second-order controls on the negative carbonate C-isotope excursion at the EPME are indicated by dashed lines. Modified from Algeo et al. (2011), and based on an earlier version by Wignall (2001).

woody plants disappeared, even though there was a substantial turn- on land include a 62.9% loss of terrestrial families (Benton, 1995), over in plants worldwide at the PTB (see Section 8). rather higher than the figures for marine families, at 49% (Sepkoski, The timing of the crisis is relatively well established. High-resolution 1984, 1996; Benton, 1995). The 62.9% figure could reflect a truly U–Pb dating at Meishan and other PTB sections in south China show higher rate of extinction on land, based as it is on data compilations that the extinction peak occurred just before 252.28 Ma, had a duration by many specialists (Benton, 1993), or it could reflect the patchier of less than 200 kyr and coincided with a δ13C excursion of −5‰ that is sampling of terrestrial taxa, especially among relatively under- estimated to have lasted for around 20 kyr (S.-z. Shen et al., 2011). It studied groups such as insects. Estimates of extinction rates and pat- had been suggested that the terrestrial PTB might be slightly younger terns for plants, insects, and vertebrates are considered in more detail than the marine PTB (e.g. Yin et al., 2003; Peng and Shi, 2009), but below (Sections 8–10). this is not substantiated by recent stratigraphic work, which shows that the PTB in South China at least is coincident on land and in the 3. The first 10 million years of the Triassic sea (S.-z. Shen et al., 2011). Further, this has been the assumption for the terrestrial sequences in South Africa (Smith and Ward, 2001) Attention has generally focused on the EPME itself, but conditions and Russia (Taylor et al., 2009), based on and continued to be challenging to life for some time into the Triassic magnetostratigraphy in the Russian sections. Further work on dating (Fig. 2). Poor environmental conditions in the are indi- the PTB and the EPME crisis interval outside the South China basins is cated by unusual biosedimentary features in marine sediments, in- still required, and this is especially true of the terrestrial redbed cluding abundant microbialites, wrinkle structures, and seafloor successions. carbonate precipitates, which reflect the absence of metazoans that The magnitude of the EPME has been debated, and data from global had been devastated by the EPME, combined with episodes of low ox- and regional sources have been brought under consideration. Global da- ygen and high chemical precipitation (Algeo et al., 2011). These un- tabases cannot represent extinction and recovery at the level usual conditions are matched in the sea by the ‘coral gap’, when because it would be impossible to ensure all groups had a uniform there were no reefs built by colonial metazoans in shallow water and updated species-level , and further, sampling issues (Flügel, 2002) and on land by the ‘coal gap’ (Veevers et al., 1994; would be especially prominent at such low taxonomic level (Raup, Retallack et al., 1996, 2011; Rees, 2002; Retallack, 2012), during 1979). Generic- and family-level data bases for marine animals have which forests, and hence coal deposits, are absent. The loss of reefs suggested that species globally suffered extinction levels of 96% and trees was more than just the loss of a large number of species, (Raup, 1979)to80%(McKinney, 1995), the differences reflecting re- but rather the loss of entire complex, and rich ecosystems, that left spectively whether all species are treated as equally liable to extinction large holes in world marine and terrestrial communities until they or not. These global-scale estimates are rather close to the 90% species had rebuilt themselves from different constituent species. extinction estimated in a study of the Meishan Permo-Triassic section This evidence for continuing poor environmental conditions in the (Jin et al., 2000), and revised to about 85% species loss over the estimat- first 5 Myr of the Triassic is confirmed by four negative excursions in ed 200,000 years of the intense extinction episode, spanning Meishan carbon isotope ratios, suggesting repeated greenhouse crises (Payne beds 24e to 28 inclusive (S.-z. Shen et al., 2011). et al., 2004; Retallack et al., 2011). These carbon isotope shifts Such detailed estimates of species loss have not been attempted for (Fig. 2) are as large as that at the PTB, and so, if they are worldwide terrestrial taxa. Global-scale estimates of the severity of the extinction phenomena, they might have been associated with similarly M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 1311

Fig. 2. Environmental changes and variations from the latest Permian to . Arrows indicated on the conodont and ophiuroid range bars show increasing data into the Middle Triassic. The ‘Erosion’ column indicates hypothesised erosion of soil and bedrock from land to sea, after Algeo et al. (2011). Stratigraphic dates, carbon isotope fluctuations, Siberian Traps (STLIP) eruption, anoxia ranges, trace data, and reef, reef builder, chert and coal gap data are given in full detail in Chen and Benton (2012). Abbreviations: Ae., Aegean; Bith., Bithynian; Di., Dienerian; Gr., Griesbachian; Illy., Illyrian; Sm., Smithian; and Vol., volcanism. Modified from Chen and Benton (2012).

devastating physical environmental consequences. Apart from the through the first 5 Myr of the Triassic are confirmed, it would seem debate over their timing, magnitude, and effects on recovering life reasonable to assume that these were a key cause of the prolonged re- of the time, it is still uncertain how such repeated light-carbon excur- covery, epitomised by the 10 Myr it took for coral reefs and 15 Myr sions could have been generated so frequently. One spike could rep- for forests to re-establish themselves. resent an episode during which the global reserves of methane stored in deep ocean gas hydrates were exhausted. Either the meth- 4. Reconstructing ancient climates ane reserves could recharge faster than had been assumed, or large volumes of CO2 were repeatedly released from coal beds (Retallack 4.1. Sedimentological evidence for ancient climates et al., 2011) or from frequent volcanic eruptions (Payne and Kump, 2007). In understanding the Late Permian and Early Triassic on land, accu- The pattern and rate of recovery of life in the Triassic is debated rate reconstruction of palaeoclimates is crucial, and sedimentary rocks (Chen and Benton, 2012), whether it is possible to refer to ‘early’ re- are the key. The formation of many sedimentary rocks is directly covery, within the first 1–3 Myr after the EPME, or ‘delayed’ recovery, influenced by climate and so they are key indicators of palaeoclimatic some 7–10 Myr into the Triassic. Examples of marine taxa that began variables such as wind direction and strength, rainfall, and atmospher- to recover quickly include ammonoids (Brayard et al., 2009) and ic or oceanic temperature. An understanding of palaeoclimate proxies conodonts (Orchard, 2007; Stanley, 2009), which diversified in the and their reliability is important for understanding the cause and ef- first 2 Myr of the Early Triassic, reaching apparently stable local fect of major events such as the EPME, as input data and control in nu- diversities. Likewise, foraminifera in the South China sections show merical palaeoclimatic models (Roscher et al., 2011) and, through the that recovery began 1 Myr into the Triassic, and was not much affect- recognition of rain-shadow effects, estimating the palaeorelief of ed by Early Triassic crises (Song et al., 2011). This early phase of re- mountain belts (Fluteau et al., 2001). covery was short-lived for most groups, however, and there were Coals, evaporites, aeolian dunes, glacial deposits and fossil plants further extinctions at the end of the Smithian and Spathian (Payne are some of the most widely applied palaeoclimate indicators. Coals et al., 2004, 2011b; Galfetti et al., 2007; Orchard, 2007). Ecosystems indicate former peatlands and lush vegetation growth and are gener- had apparently recovered substantially in the sea in the middle to ally taken as proxies for an ever-wet (humid to perhumid) climate, late , 8–10 Myr after the crisis (Hallam and Wignall, 1997; although they also have a strong dependence on basin subsidence Payne et al., 2004, 2011b; Stanley, 2009; Algeo et al., 2011; Hu et al., and high regional water tables (Falcon-Lang and DiMichele, 2010). 2011; Chen and Benton, 2012). The recovery of life on land shares Evaporites are generated under specific climatic conditions of high some of these patterns (see below, Sections 8–10). mean annual temperature and low precipitation and today form The stepwise recovery of life in the Triassic (Fig. 2) could have mostly within narrow (25–40°) latitudinal belts. However, they can been delayed either by biotic drivers (complex multispecies interac- occur at lower latitudes where topography creates local rain shadows. tions; Solé et al., 2010) or physical perturbations, or a combination Like coals, their distribution is strongly controlled by structural geol- of both. Certainly, if the repeated carbon isotope spikes and sedi- ogy with isolated rift basins and continental sags forming preferential mentary evidence for unusual and poor environmental conditions sites for evaporative water bodies (Warren, 2010). Aeolian dune 1312 M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 deposits indicate arid climates, but their formation and preservation events may be represented only by non-deposition also require an abundant supply of mobile (dry and unvegetated) or erosion. For example, fluvial systems may respond to climate sand and basin subsidence. The presence or absence of permanent ice change by switching between aggradational and degradational re- is the primary feature of icehouse and greenhouse global climates. gimes as the balance between sediment supply and stream power Polar ice sheets moving across lowland basins and marine shelves shifts (Bull, 1990). Aeolian dune systems may become inactive during leave behind a distinctive suite of ice-contact facies with high preserva- wet phases so that humid climates are represented only by cryptic tion potential. However, glaciers in long-eroded mountain belts leave stabilisation surfaces (Newell, 2001). no direct evidence in the geological record and their former presence is remarkably difficult to establish from linked basin deposits such as 4.2. Palaeogeography and climate in the Permo-Triassic fluvial outwash (Smith et al., 1998). Plant fossils can be used for climate reconstruction either through an understanding of their ecology based Around the PTB, all continents were merged into the supercontinent on living relatives or through the leaf stromatal index, which varies in- , centred more or less on the equator and stretching almost from versely with the partial pressure of carbon dioxide (Retallack et al., pole to pole (Fig. 3). Pangaea was surrounded by the Panthalassa Ocean 2011). This is important because atmospheric carbon dioxide levels and a deep oceanic gulf, Tethys, which was latitudinally confined to are closely linked to global climate (Royer et al., 2004). the tropical–subtropical belt, and contained several Asian landmasses Clay minerals provide additional crucial data on palaeoclimates. (Roscher et al., 2011). The impact on climate of this peculiar plate They form by chemical weathering so that the types of clay configuration has been investigated by modelling (Kutzbach and and their relative abundance in a geological unit are often closely re- Gallimore, 1989; Kiehl and Shields, 2005). The concentration of exposed lated to climate. Kaolinite, for example, is created by intense chemical land at low and mid-latitudes, and the presence of a warm sea-way weathering in warm, humid climates where silica is leached out, leav- would have maximised summer heating in the circum-Tethyan part of ing soils enriched in alumina. However, climatic interpretations the continent and created a strong monsoonal regime (Kutzbach and should always consider additional controls, such as source rock com- Gallimore, 1989). Furthermore, extreme continentality, with hot sum- position, which may include clay-rich soils and formations deposited mers and relatively cold winters, is expected (Kutzbach and Gallimore, under a different climatic regime, sorting during transport, and later 1989). Polar regions were ice-free, and their latest Permian deposits con- diagenetic alteration (Yakimenko et al., 2000). The framework miner- tain coals, plants and soils typical of cool temperate latitudes (Retallack alogy of sandstones may also record palaeoclimate signals (Suttner et al., 2006). The polar regions were temperate, not only because of ele- and Dutta, 1986), with similar caveats on their interpretation to clays. vated CO2 levels (Royer et al., 2004), but also from the unrestricted Red beds have long been interpreted as desert deposits, but it is ocean transport of heat toward the poles and a reduced albedo arising now acknowledged that well drained conditions are probably a from the lack of permanent land ice (Kiehl and Shields, 2005). more important control on the red colouration than specific The harsh hot-house climatic conditions that characterised the palaeoclimatic conditions (Sheldon, 2005). Many red beds appear to Late Permian were probably maintained (Preto et al., 2010) or exacer- have formed under warm, humid conditions, sometimes with evi- bated during the Early Triassic with, for example, the northward and dence for strong seasonality. southward expansion of low-latitude arid belts into the vast, formerly Changes in river channel style or palaeohydraulics calculated from humid basins of European Russia and the (Chumakov and cross-bed or point bar thickness may be an indicator of climate Zharkov, 2003; Royer et al., 2004). change, although it is important to eliminate alternative external con- trols such as tectonics and autocyclic behaviour (events responsible 4.3. Numerical climate models for the accumulation of sediments that are part of the sedimentary system itself, such as the size and configuration of a river channel). The peculiar plate configuration of Pangaea around the PTB Moreover, while it is relatively straightforward to estimate channel attracted some early and pioneering work on energy balance models size, it is much more difficult to determine the duration of peak (Crowley et al., 1989) and atmospheric general circulation models flows within palaeochannels, a requirement for estimates of long- (Kutzbach and Gallimore, 1989). These models demonstrated the term discharge and precipitation within the catchment. Fluvial sys- likelihood of extreme seasonal temperature variation within the tems in semi-arid settings tend to scale toward the largest flood large continental interiors of Pangaea and the probability of arid con- event, even if these are infrequent. Thus an increase in channel size ditions on the western side of Gondwana and Laurussia. The early may not equate to increased climatic humidity (Newell et al., 1999). models were also successful in reproducing the expected high precipi- The relationship between climatic zones and broad belts of similar tation and strong monsoonal circulation of the Tethys coast. However, soils has long been appreciated, and this inspired the zonal concept of there appeared to be discrepancies in polar and high-latitude regions soils. This relationship has been extended to the geological record where the models generally predicted much colder conditions than through the use of palaeosols as proxies for precipitation, tempera- suggested by the presence of coal forests in the Antarctic (Retallack et ture, and climate seasonality (Retallack, 1999, 2012; Sheldon and al., 2007). Tabor, 2009; Retallack et al., 2011). Reliable interpretations require More recent models (Kiehl and Shields, 2005), which include cou- an appreciation of how relief, parent material, and vegetation can lo- pling of atmospheric and oceanic circulation, have had greater success cally override climate as a primary control on soil type. Carbonates at reproducing cool temperate polar regions by allowing a flow of precipitated within soil profiles have played an important role in warm water into high latitudes, which, because of the configuration of charting atmospheric δ13C changes through geological time in terres- Pangaea, was relatively unrestricted in high latitudes. Models are now trial sequences (Royer et al., 2004), and often produce results with being turned toward understanding climate change events across the remarkable similarity to the marine record (Korte and Kozur, 2010), EPME. The climate models of Roscher et al. (2011) show that an episode providing that factors such as soil drainage (Tabor et al., 2007), mi- of global cooling around the PTB was more effective at producing the crobial activity, and root respiration are taken into account. observed changes in climate belts than global warming. The time resolution offered by terrestrial deposits is an important Coupled climate–carbon cycle models by Winguth and Winguth consideration in their use as climate proxies. Climate change can (2012) have been used to explore oceanic anoxia. These authors occur over short time scales, but some terrestrial geological deposits found it hard to generate complete anoxia, but that the oxygen min- accrete very slowly and will not capture a record of each climate imum zone expanded considerably, while the deep Panthalassa change event. For example, many palaeosols appear to show the over- remained ventilated. Further, these models suggested that upwelling print of more than one climate type (Yakimenko et al., 2000). Some of toxic water was probably not a global phenomenon, and so M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 1313

Fig. 3. Permian–Triassic Pangaean palaeogeography, with the location of the main PTr terrestrial basins and boundary sections indicated, (1) West Siberian/Kuznetsk Basin, (2) Precaspian/Urals foreland basin/Russian Platform, (3) Central European Basin, (4) Iberian Basin, (5) South China, (6) Paraná Basin, eastern South America (7) Karoo, South Africa, (8) Satpura/Raniganj basins, central , (9) Bowen Basin, western , and (10) Victoria Land and the central Transantarctic Mountains, Antarctica. From Roscher et al. (2011). Late Permian climate zones are generalised from Schneebeli-Hermann (2012).

probably not a major player in the EPME. The effects of increased sections across the world; however, there is still much to do in all lo- weathering and enhanced nutrient input into the oceans was felt cations. Moreover, with the emergence of Earth Systems Science and only in the Early Triassic, according to the models, and so probably ongoing efforts to understand the possible environmental outcomes contributed to the delayed recovery of life. of modern global warming (IPCC, 2007) the information to make informed interpretations of observed changes in the stratigraphic 5. Sedimentology of the terrestrial Permo-Triassic boundary interval record of the PTB are now increasingly available. Modelling studies in particular highlight the complex interactions and feedbacks that 5.1. Location and setting of key sections can occur between the lithosphere, atmosphere, and hydrosphere during global warming events. It should of course be remembered PTB sections in terrestrial deposits are distributed across five mod- that studies investigating anthropogenic global warming do not con- ern continents, with key sections located in Russia, western Europe, sider the vast magmatic eruptions that accompanied events at the China, South Africa, Australia and the Antarctic. Relative to the PTB. The configuration of the continents was also very different in palaeogeography of the Pangaean supercontinent these terrestrial the Late Permian (see Section 4.2), and global warming started from sections occupy a range of palaeolatitudes and pre-extinction a much higher initial temperature in a world that was free from palaeoclimatic zones (Figs. 3 and 4), including the high latitude permanent ice sheets (Roscher et al., 2011). cool-temperate deposits of Australia, Antarctica, and Siberia, the sub-tropical, semi-humid to semi-arid basins of Western Europe, 5.2. General character of PTB terrestrial sections the Russian Platform and South Africa, and the ever-wet tropical coastal zone of India and south China (Table 1). The terrestrial bound- The distinctive negative δ13C excursions that occur around the PTB ary sections were deposited within a broad range of structural in marine sections have now been recognised in many non-marine settings including major foreland basins (Russia, South Africa), PTB successions around the world, including South Africa, Australia, intracratonic sags (Paraná), narrow extensional rifts (Spain), and Antarctica, and Germany (Fig. 4; Retallack et al., 2006; Korte and pull-apart basins (India). Each structural setting creates a unique Kozur, 2010). Concerns about how continental bulk carbon isotope combination of relief, sediment source, local climate, and scale. The values could readily deviate from coexisting atmospheric values range of pre-extinction terrestrial depositional systems is equally (Tabor et al., 2007; Korte and Kozur, 2010) have been largely alleviat- broad, ranging from small semi-arid alluvial fans to vast channel– ed by the use of independent dating methods on excursion events floodplain systems with peat-forming swamps (Table 1). The wide (Taylor et al., 2009). The presence of age-verified isotope excursions range of pre-extinction scenarios in terms of palaeoclimate, structural in many sections greatly increases confidence that continental facies, setting and depositional system is both interesting and useful in that with their considerable potential for stratigraphic gaps, can capture a it provides an opportunity to examine how different environments record of events at the PTB. Given the apparent completeness of the responded to the effects of PTr climate change. stratigraphic record in many terrestrial PTB sections and the magni- Over the past decade much time and effort has been expended on tude of events surrounding the EPME, it is surprising, and somewhat the EPME, with the result that detailed stratigraphical and sedimen- disappointing, that discrete ‘event beds’ are generally not identified tological descriptions are now available for many of the terrestrial (Gastaldo et al., 2009). More usually, the PTB is marked by a shift in 1314 M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337

Fig. 4. Compilation of measured sections across the Permo-Triassic boundary, from a selection of key basins across Pangaea (see Fig. 3 for locations). All of the sections have been replotted and generalised where necessary to the same vertical scale, except the Kuznetsk Basin, which is a sketch stratigraphical section covering several kilometres of strata. The left to right arrangement of the sections broadly reflects decreasing humidity of the pre-extinction Late Permian depositional environments.

depositional environment (which may be either gradational or Regardless of palaeolatitude or basin setting, most terrestrial PTB abrupt) that extends upwards to include much of the Early Triassic sections appear to record a shift towards warmer and drier conditions (see Sections 6.2 and 6.4). at the time of the EPME (Smith, 1995; Newell et al., 1999; Erwin et al., The most obvious environmental changes generally occur in high- 2002; Chumakov and Zharkov, 2003). latitude, cool temperate settings (Australia, Antarctica, Siberia) and in However, to view PTr climate change as a unidirectional shift to- the ever-wet coastal (e.g. south China, India) where peat- wards hotter and more arid conditions is probably an oversimplifica- forming swamps disappear abruptly at the end of the Permian. This tion. Much modelling work on modern global warming has concluded ‘coal gap’ extends across much of the Early and Middle Triassic that more extreme climates with intense droughts and floods are a (Veevers et al., 1994; Retallack et al., 1996). In tropical, semi-humid likely consequence of global warming (IPCC, 2007). As discussed basins such as the Karoo (Smith, 1995) or the south Urals (Newell below, a range of sedimentary evidence supports this view, including et al., 1999), brown overbank mudstones with plant remains in the changes in fluvial style (Newell et al., 1999), enlargements of drain- Late Permian are replaced by highly oxidised red mudstones in the age networks (Newell et al., 2010), variations in pedogenic carbonate Early Triassic, often reworked into coarse braided river deposits. In (Pace et al., 2009), mixed aeolian–fluvial sedimentation (Arche and the semi-arid rift basins of the Iberian Peninsula, Late Permian fluvial López-Gómez, 2005), and shifts in the maturity of sandstone compo- strata with plant remains are replaced in the Early Triassic by mixed sition (Ghosh and Sarkar, 2010). aeolian–fluvial deposits (Arche and López-Gómez, 2005). These shifts Conceptual and numerical models of PTr climate change are still at in sedimentary style were the first clues towards developing a new an early stage of development. For example, it is still uncertain model for the EPME on land, and for important drivers of extinction whether the extension of the environmental crisis in the Early Triassic in the sea arising from these perturbations on land (Newell et al., is a consequence of repeated environmental disturbances or the 1999; Algeo et al., 2011). Mass wasting of the landscape following result of complex feedbacks resulting from the initial disruption to aridification and acid rain supplied bursts of nutrient rich soil and the carbon cycle. More detailed information is required on how siliciclastic debris to shallow seas, expanding the oxygen minimum terrestrial processes such as wildfires, weathering, and erosion were zone (OMZ) and boosting surface productivity. Anoxia and euxinia affected by the EPME, so that the complex feedbacks of these processes combined to drive marine extinctions, while terrestrial extinctions on climate can be incorporated into models of increasing sophistication. presumably resulted from aridity, acid rain, loss of soils, and perhaps Our understanding of how a number of earth surface processes may short-term effects of wildfires and damage to the ozone layer. have been altered by PTr global warming is considered below. M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 1315

6. Impact of PTr global warming on geomorphic processes

2008) 6.1. Weathering Ward et al. , Pace et al. Chemical weathering is the term used to describe the transforma- and tion of minerals formed at particular pressure and temperature condi- tions within the earth into more stable secondary minerals and solute (2009) (2000) Smith (1995) Sarkar et al. (2003) Michaelsen (2002) Retallack et al. (1996) Peng and Shi (2009) Newell et al. (2010) López-Gómez (2012) Davies et al. (2010) species through interaction with dilute waters close to the earth's surface. Silicate weathering is an important control on atmospheric dry – CO2 because mineral dissolution and subsequent precipitation results in a net loss of CO2 from the Earth's surface (Berner et al., 1983). This makes estimates of weathering rates and processes in the PTr interval an important element in understanding Early Triassic climatic instability. The strontium isotope record in marine limestones is one of the most widely applied proxy indicators of continental weathering in-

uvial and aeolian sedimentation tensity (Martin and MacDougall, 1995; Huang et al., 2008). Temporal fl variations in the isotopic ratio of 87/86Sr reflect changes in the fluvial (continental) input relative to hydrothermal inputs to the ocean, controlled by the rate of seafloor spreading. Martin and MacDougall (1995) recognised a major excursion in 87/86Sr ratios at the PTB which fl 87/86

oodplains, mixed was characteristic of a greatly increased ux of riverine Sr, and climate conditions Braided rivers Sandy, braided river systems, alternating wet Sandy braided river systems Rivers with non carbonaceous palaeosols Gravelly or sandy braided rivers, highly oxidised fl Coarse-grained braided channels with wide barforms may indicate enhanced rates of chemical weathering at the PTB, possi- bly related to global warming and increased humidity. Influxes of soil-derived biomarkers at the EPME into shallow marine deposits have been similarly interpreted as indicators of enhanced weathering (Algeo et al., 2011). Further, virtually all marine sections at the PTB show a shift toward greater clay content in the immediate aftermath of the EPME, which suggests generally greater chemical weathering in- oodplains with densely fl

oodplains with calcretes, tensity in continental areas and enhanced production of pedogenic clay fl oodplain swamps with peat

fl minerals (Algeo and Twitchett, 2010).

uenced fi fl Palaeosols are weathering pro les formed during pauses in deposi- oodbasins with palustrine

fl tion within terrestrial sedimentary basins. Within a palaeosol, the rela-

oodplains with densely vegetated tive proportion of immobile elements such as aluminium to mobile fl elements such as magnesium may provide information on contempora- neous weathering rates (Sheldon and Tabor, 2009). This approach has

oodplains been used at a number of PTB locations. At the Graphite Peak section swamps, marine in fl vegetated backswamps backswamps Seasonally well-drained poorly-drained carbonate and evaporites, distributary channels mires in Antarctica, earliest Triassic palaeosols show enrichment of barium relative to strontium, which was interpreted as a result of greater leaching relative to underlying coal-measure palaeosols of the latest Permian (Sheldon, 2006). Comparable increases in chemical weathering were reported from PTB palaeosols in the Sydney Basin (Retallack et al., 2011). At the Chahe terrestrial PTB section in SW China, an increase of aluminium relative to magnesium in the so called ‘geochemical anoma- ’

humidity ly layer was interpreted as an escalation of weathering around the EPME (Yu et al., 2007). The interpretation of weathering rates from palaeosols clearly re- quires the elimination of local factors that may enhance leaching, 60°S Tropical, semihumid Fluviolacustrine with extensive peat forming 30°S Arid, rain shadow Aeolian Early Triassic strata missing Delorenzo et al. ( 60°S Cool temperate60°S Meandering channels, poorly Cool drained temperate, swampy humid Meandering river systems, 80°S Cool temperate and humid Rivers and 60°N Warm, temperate, humid Meandering rivers and 10°N Tropical, ever-wet Fluviolacustrine, heavily vegetated Fluviolacustrine 40°N Subtropical, seasonal 30°N Tropical, semihumid Fluvial and lacustrine Fluvial and aeolian – – – – – – – – – such as improved soil drainage and any changes in palaeosol geo- 0 30 chemistry that are related to changes in source material rather than weathering processes. Palaeosols only provide a record of weathering patterns in depositional basins and not in eroding source areas, which globally may account for a higher proportion of weathering products. The framework mineralogy of sandstones provides an alternative source of information on weathering intensity, which may be represen- tative of eroding source areas (Suttner and Dutta, 1986). Mature sands and sandstones that have a high ratio of quartz relative to feldspar Foreland basin/halokinetic basin/intracontinental sag volcanic province and rock fragments are often derived from highly weathered sources, on the assumption that other factors such as multiple cycles of reworking, time-dependent or tectonically-controlled changes in source rock, source area relief, and unstable-grain destruction by trans- port and burial diagenesis have been eliminated. Michaelsen (2002) ob- served that in the Bowen Basin of Australia the Early Triassic Sagittarius Sandstone showed a significant enrichment of quartz and a decrease in

Platform feldspars relative to the underlying Late Permian Rangal Coal Measures. Gondwana Basins, India Pull apart 40 BasinParaná Basin Continental sag Type 20 Palaeolatitude Pre PTB Climate Pre PTB deposystem Post PTB deposystem Reference Karoo Basin, South Africa ForelandBowen Basin, Australia Foreland 40 40 Antarctica Foreland 60 Siberia, Kuznetsk Basin Foreland 40 South Urals/Russian Iberia Rift basins 20 South China Flanks of basaltic

Table 1 Characterisation of facies and inferred environments of selected terrestrial PTB sections. He interpreted this as an indicator of increased temperature-driven 1316 M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 weathering rates in the Early Triassic. Interestingly, a reverse situation The best record of changes in terrestrial erosion is likely to be was observed in the Precaspian Basin of Kazakhstan where core from found in the marine stratigraphic record, particularly in nearshore the Saigak-2 borehole showed that potassium feldspar was very rare deltaic and estuarine settings that receive a large input of land- in Late Permian deposits but occurs in the Early Triassic (Barde et al., derived sediment. A number of studies have now recognised in- 2002). This was interpreted as a shift from relatively wet conditions in creases or changes in soil-derived biomarkers in shallow marine the Late Permian to relatively dry in the Early Triassic, reasonable sequences at the EPME, and these have been used as evidence for since there is evidence that chemical weathering is driven much more enhanced rates of weathering and erosion (Sephton et al., 2005; Xie by water availability than temperature rise (Goddéris et al., 2009). In et al., 2005, 2007). Increases in the bulk sediment accumulation rate the Raniganj Basin in India, Suttner and Dutta (1986) found no marked around the PTB have also been used as evidence for higher terrestrial change in sandstone composition and weathering regime at the PTB, sediment fluxes to marine depositional systems (Algeo and Twitchett, the lowermost 295 m of the Early Triassic Panchet Formation having 2010). similar framework mineralogy to the Late Permian Raniganj Forma- There may have been a major change in the nature of mass wasting tion. However, above 295 m, the Early Triassic Panchet Formation during the Early Triassic (Algeo and Twitchett, 2010; Algeo et al., 2011), showed an abrupt increase in sandstone maturity, which was inter- with a switch from massive soil erosion at the time of the EPME to bed- preted as a shift from warm semiarid conditions to warm humid rock erosion. The immediate biological indicators of massive terrestrial conditions. erosion at the EPME are soil-derived biomarkers (Sephton et al., 2005; Strontium isotopes, biomarkers, palaeosols, and sandstone miner- Xie et al., 2005, 2007; Wang and Visscher, 2007) and nutrient- alogy, while not in total agreement, point to increased weathering stimulated algal blooms (Kozur, 1998; Afonin et al., 2001). These phe- rates at the EPME. While increased temperature around the PTB is nomena occur just below the EPME horizon, so linking these events to commonly implicated as the primary cause of enhanced weathering, the marine extinctions (Sephton et al., 2005). However, soil biomarkers and high temperatures can speed up weathering by a factor of 3 or are not recorded later in the marine Lower Triassic successions, and this more (Drever and Zobrist, 1992), there is evidence to suggest that was interpreted by Algeo and Twitchett (2010) as evidence for a brief the availability of undersaturated soil waters is actually a more im- soil erosion crisis during the EPME episode, with later increases in the portant control on silicate mineral dissolution rate (Kump et al., influx of siliciclastics to the oceans resulting from bedrock erosion. Fur- 2000). A direct link between temperature and weathering is difficult ther work on the basin sedimentology of Early Triassic river-dominated to obtain, even in modern catchments, because of the complex link- deltas may further test this idea. Evidence of Early Triassic deltaic ages among temperature, rainfall, plant growth, elevation, and other progradation against a background of eustatic sea-level rise (Hallam factors (Drever and Zobrist, 1992; Kump et al., 2000), but the temper- and Wignall, 1999) could result from high rates of terrestrial sediment ature rise of 8–10 °C at the PTB (see above) might then itself have delivery. For example, seismic sections in Early Triassic deltaic strata doubled or trebled normal weathering rates on land. of the Northern Barents Sea show a remarkable series of large clinoform Land plant cover is a particularly neglected variable in discussions beds formed by huge prograding delta systems (Høy and Lundschien, of EPME weathering rates, given the evidence for major changes in 2011). vegetation type and the possible importance of wildfire around the There is also a range of evidence from terrestrial settings for PTB (W. Shen et al., 2011). Land plant cover has an important impact increased rates of erosion. PTB sections in Antarctica developed in on weathering rates by increasing the residence time of water in soil muddy palaeosols show thin (15 cm) beds of reworked soil frag- systems and the concentrations of acid species such as CO2 and or- ments (peds) suggesting unusually voluminous and short-lived epi- ganic acids. Removal of land plants causes an increase in soil drainage, sodes of soil erosion around the PTB (Retallack, 2005). Comparable primarily because of a decrease in evapotranspiration, an effect par- features have been observed in Australia and South Africa (Sheldon, ticularly marked in tropical environments because of the dense 2006). Many fluvial sequences which cross the PTB, for example in plant cover (Goddéris et al., 2009). Modelling studies indicate a vast the Karoo, India, and the south Urals, show a marked increase in increase in the flux of chemical weathering products when land grain size across the boundary, often towards coarse pebbly material plants are removed (e.g. by wildfire) without the need for elevated (Newell et al., 1999; Ward et al., 2000; Chakraborty and Sarkar, temperatures or increased precipitation (Goddéris et al., 2009). 2005). In the absence of evidence for tectonic uplift or changes in The complex relationships between rates of erosion and weathering source, this grain-size shift could indicate the rapid erosion of coarse is a further factor that should be taken into account. If erosion rates are debris that was formerly locked in hillslope reservoirs by vegetation low, thick soils depleted in cations are developed, and these may yield cover (Newell et al., 1999). Removal of vegetation lowers erosion little in the way of solute load (Goudie and Viles, 2012). Increase in thresholds and increases runoff rates, which both promote the trans- the erosion rate, as would occur if binding vegetation were removed port of coarse-grained bedload (Syvitski and Kettner, 2011). by wildfire, creates thin soils with greater contact between soil waters As discussed below (see Sections 6.3 and 8), the extent of Early and fresh mineral surfaces. Chemical weathering then proceeds at a Triassic land-cover change is difficult to evaluate. Beyond the disap- fast rate, limited only by the rate of mineral dissolution, and the solute pearance of the cool-adapted flora of Gondwana, it is dif- load is high. ficult to determine extinction patterns among plants, and they do not Finally the importance of lichens, fungi and bacteria in accelerat- appear to show clear-cut losses of major clades at the PTB (McElwain ing chemical weathering processes (Burford et al., 2003) provides an and Punyasena, 2007; Xiong and Wang, 2011). Wildfire may have interesting and unexplored link between evidence for enhanced played a more important role in land-cover related erosion than weathering at the PTB and the fungal spike. Their fossil records are plant loss by extinction. More detailed work is required on poor, but these taxa all include species with profound abilities to sur- how changes in plant communities may have influenced sediment vive drought (see Section 11.5). yield through changes in root density/depth and leaf canopy. Vegeta- tion change may in fact have played a minor role relative to changes 6.2. Erosion rates in the PTB interval in precipitation pattern. As postulated by Newell et al. (1999) an increase in the grade of sediment across the PTB could be related to Increased rates of erosion are widely reported consequences of intense rainfall and high-magnitude discharge events, which, even if PTr global warming. It is also important to understand the links these were of low frequency, would have moved a much higher between global warming and erosion rates because erosion makes a volume of coarse sediment. major contribution to carbon cycle feedbacks in a changing climate Considering Pangaea as a whole, it is probable that large areas of (Goudie and Viles, 2012). the land surface were predisposed to the risk of increased erosion M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 1317 following a shift toward a hotter climate at the PTB. Increases in ero- precipitation to generate runoff and move sediment (Fig. 6). In the sion and sediment yield are particularly marked where landscapes Late Permian, Pangaea was characterised by vast continental inte- shift from sub-humid to semi-arid regimes, reflecting an optimum riors and unusually wide sub-humid climate belts (Chumakov and balance between a reduction in vegetation cover and sufficient Zharkov, 2003).

(A) LATE PERMIAN Pre-crisis Silicic magmas terrestrial ecosystems

Pre-crisis marine ecosystems Soils Coal

Slow sedimentation OMZ

Siberian Suboxic volcanic centers (early stage) (B) END-PERMIAN EVENT Flood basalts CO2 emissions/global warming Methane Acid rainfall Nutrients Elevated marine productivity

Coal Terrestrial devastation Magma Expanded OMZ intrusion Eroded soil

Photic-zone Siberian euxinia Suboxic-anoxic volcanic centers (main stage) (C) EARLY TRIASSIC Flood basalts Global warming (lessening) Acid rainfall Disaster vegetation

Rapid weathering Episodic upwelling + shallow euxinia

OMZ Rapid sedimentation Siberian Suboxic-anoxic volcanic centers (late stage) (D) MIDDLE TRIASSIC Recovered Post eruption terrestrial ecosystems

Recovered marine ecosystems Coal Soils

Slow sedimentation OMZ

Siberian volcanic centers Suboxic (inactive)

Fig. 5. Interpretative reconstructions of changes in terrestrial–marine systems during the PTB crisis. Early stage Siberian Traps volcanism with minimal environmental effects during the Late Permian (A). Main stage eruptions with attendant environmental effects during the latest Permian (B). Late stage eruptions with lessening environmental effects during the first part ( Stage) of the Early Triassic (C). Post-eruption recovery of terrestrial and marine ecosystems by the Middle Triassic (D). Modified from Algeo et al. (2011). 1318 M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337

6.3. Wildfire fluvial style or grain size at the PTB have been interpreted as results of changing climate or vegetation cover. Such interpretations are actu- Wildfires were common throughout the Permian, and to the end of ally remarkably rare in pre- fluvial sequences, where tec- the at the PTB, and there was then a long gap through tonics or sea level is often favoured as the dominant control on fluvial the Early Triassic and much of the Middle Triassic that corresponded stratigraphy. Many of the documented changes show remarkable to the ‘coal gap’ (Veevers et al., 1994; Retallack et al., 1996). Abundant similarities. charcoal, black carbon and carbon spherules have been described at In the Karoo Basin, South Africa sediments below the PTB comprise the EPME from the Meishan section in south China (W. Shen et al., drab greenish grey mudrocks with a few thick laterally accreted sand- 2011) and are interpreted as evidence for extensive wildfire associated stone bodies. Above a boundary transition zone of around 20 m these with the mass extinction. Evidence for wildfires is important because strata change to reddish brown mudrocks with calcic palaeosols and they are well known catalysts for erosion and increased sediment yield numerous ribbon sandstone bodies and more continuous sheet sand- in small basins (Meyer et al., 1992), although the potential contribution stones. Smith (1995) interpreted the facies transition as a change in of climate-driven increases in wildfire activity to the sediment produc- fluvial style from meandering to low sinuosity channels with general tion in large river basins has not been well quantified. Moreover trace drying of the floodplain habitats (Fig. 7). He postulated a structural con- gas and particle emissions associated with wildfires have a major impact trol, but the alteration in river morphology was later interpreted as the on atmospheric composition and chemistry and on climate itself (S.P. result of a rapid and major die off of rooted plant life producing a Harrison et al., 2010). The record of wildfires through the Permian and marked increase in sediment yield (Ward et al., 2000). Triassic is also now used as key evidence in determining likely changes In the south Urals, the PTB is marked by a dramatic shift from in atmospheric oxygen levels (see Section 7.3). metre-thick sandstone-dominated channel fills in the Late Permian Climate change is known to have a strong influence on all aspects to major, multi-storey gravelly, braided channels in the Early Triassic of the wildfire regime from the seasonal timing of lightning ignitions, (Fig. 8; Newell et al., 1999). An apparent increase in channel size is through temperature and humidity control of fuel drying to wind- also accompanied by a large increase in the length of the drainage driven fire spread (S.P. Harrison et al., 2010). Other major climate system. In central parts of the Russian Platform, the PTB is marked change events in the geological record such as the PETM are by the abrupt progradation of sandy fluvial systems into former characterised by major increases in burning (Collinson et muddy lacustrine floodbasins which lie up to 900 km from source al., 2007). areas in the Urals (Newell et al., 2010). In the northern Bowen Basin of Australia, the PTB is expressed as an 6.4. Changes in fluvial style abrupt and sharp change in fluvial regime at the contact between the Rangal Coal Measures and the Sagittarius Sandstone (Michaelsen, Changes in the style of river channels are marked in many terres- 2002). The Late Permian fluvial style is characterised by large-scale, trial PTB sections (Figs. 4 and 7). Currently, most of these changes in sandstone-dominated, low-sinuosity trunk river channel deposits flanked by extensive crevasse-splay systems. The fluvial architecture of the Sagittarius Sandstone is characterised by sheet-like elements suggesting deposition in broad shallow channels in a deforested braid-plain setting with flashy runoff regime (Michaelsen, 2002). Sandy braided river systems also make an appearance at the PTB in the rift basins of the Iberian Ranges (Arche and López-Gómez, 2005), the pull-apart Satpura Basin in India (Chakraborty and Sarkar, 2005), and the giant intracontinental Kuznetsk Basin of Siberia (Davies et al., 2010). Only in the terrestrial PTB sections of western Guizhou and east- ern Yunnan has such a major shift in grain size across the boundary not been observed (Yu et al., 2007), although a concentration of brecciated volcanic materials occurs at the PTB in all South China sections, associated with a colour shift from the olive, grey or multicoloured sandstones and mudstones of the coal-bearing uppermost Permian to maroon and purple interbedded sandstones and mudstones of the Early Triassic (S.-z. Shen et al., 2011). These earliest Triassic sediments are frequently associated with scours, poorly sorted syngenetic breccia and calcareous siltstone nodules, all of which suggest a dramatic collapse of soil systems near the PTB in South China. The wide palaeogeographic distribution of basins, synchronicity, wide range of tectonic settings, and close temporal association with mass extinctions, vegetation turnover, and carbon isotope excursions is strong evidence that there is a link between the changes in fluvial style and climate. The similarity of the changes in fluvial style is re- markable given the many different configurations of drainage basins in terms of bedrock, elevation, vegetation cover, palaeolatitude, and other factors. Some differences, such as those observed in western Guizhou and eastern Yunnan (Yu et al., 2007; S.-z. Shen et al., 2011)

Fig. 6. Conceptual plot of sediment yield relative to precipitation and vegetation cover. would actually be expected. The largest increases in sediment yield are likely to occur when climate changes from The most common explanation for the change in fluvial style is as temperate to semi-climate, which represent the optimum combination of reduced a result of vegetation dieback, which would have increased sediment vegetation cover with sufficient precipitation and runoff to facilitate sediment erosion. delivery, created flow variability, and decreased bank stability, all fac- Many of the large Late Permian basins (e.g. Karoo, Russian Platform) appear to have tors that are known to promote a multichannel, braided river pattern. changed from relatively humid to semiarid conditions across the PTB, which would account for large global increases in sediment yield. Newell et al. (1999) also stress the probable importance of a switch Modified from Goode et al. (2012). toward low frequency, but high-magnitude flood events, which can M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 1319

Fig. 7. Changing river styles across the PTB. Summary sedimentological log of the PTB sequence compiled from the study sections in the Bethulie District, Karoo Basin, South Africa, with interpreted palaeolandscape reconstructions. Vertical scale in metres. Modified from Smith and Botha (2005).

drive increases in the grain size of the sediment load and enlargement probably reflecting the high global temperatures and rates of evapora- of drainage systems. In dryland environments, channels and drainage tion relative to water input. systems typically scale towards the largest flood event rather than the Late Permian perennial lake successions have been recognised in average (Newell et al., 1999). the rapidly subsiding Satpura Gondwana pull-apart basin of central India (Chakraborty and Sarkar, 2005), but these do not persist beyond the PTB because they were overrun by Early Triassic sandy braided 6.5. Changes to lacustrine systems river deposits. Comparable disruption to lacustrine environments has been recorded elsewhere; for example, Late Permian playa lacus- Long-lived, deep lacustrine basins are probably the terrestrial trine deposits of the Moscow Basin are also replaced by sandy braided settings with greatest potential to capture a high-resolution record river deposits around the PTB (Newell et al., 2010). The abrupt switch of climate change events. It is unfortunate then that thick sequences in environment could reflect increased sediment supply coupled with of laminated, perennial lake deposits crossing the PTB have not been an enlargement of fluvial distributary networks to cope with low found. Despite the presence of suitable tectonic settings for deep frequency but high magnitude flood events. perennial lakes (e.g. linear rift basins), most Late Permian and Early The North German Basin is one of the few locations where lacustrine Triassic lacustrine deposits are shallow, ephemeral, and evaporative, environments persist across the PTB. Hiete et al (2006) documented the 1320 M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337

Fig. 8. The dramatic shift from low-energy, meandering stream to high-energy, braided stream sediments cross the PTB in Russia. Latest Permian sediments include metre-thick sandstone-dominated channel fills with lateral accretion surfaces (A), and these change to major, multi-storey gravelly, braided channels in the Early Triassic (B).

boundary succession in great detail using core from the Wulften-1 bore- widespread development of bicarbonate-rich, oxic waters (Woods et hole just south of the Harz Mountains. In the Wulften-1 borehole, the al., 1999). Accepting similar controls on non-marine microbial carbon- PTB, as determined by palynology, is located close to the so-called ates, an increased flux of bicarbonate to lakes could have resulted Graubankbereich towards the base of the Calvörde Formation in the from enhanced weathering of silicate minerals or an increase in soil Lower Bundsandstein (Hiete et al., 2006). This is stratigraphically water fluxes following land cover change (Raymond et al., 2008). above the major basin-wide change from sabkha to playa lacustrine fa- There were major changes in the importance of evaporites be- cies that occurs in the upper part of the Zechstein. The Graubankbereich tween the Late Permian and the Early Triassic (Warren, 2006). Late is a distinctive 8–9 m thick grey mudstone, which probably represents a Permian evaporites include major deposits in the Zechstein Basin in phase of perennial lacustrine deposition that was greatly extended northwest Europe and in west Texas, which together define a broad relative to that seen elsewhere in the Calvörde Formation. The grey band of equatorial aridity extending from about 50°N to 30°S colouration and abundance of pyrite indicates synsedimentary or palaeolatitude (Chumakov and Zharkov, 2003). However, Warren syndiagenetic anoxic conditions (Hiete et al., 2006). This is comparable (2006) notes a broadening and intensification of evaporite deposits to the Moscow Basin around Vyazniki (Newell et al., 2010), where a dis- in the Early Triassic, with huge deposits associated with continental tinctive bed of dark grey, laminated lacustrine mudstone (c. 1 m thick) redbeds in southeast and western USA, western Canada, northwest occurs close to the PTB. The bed contains a rich fossil assemblage Africa, western and southeast Europe, central South America, and and is sandwiched between more typical Late Permian strongly east . Interestingly, Warren (2006) does not consider that oxidised/evaporitic playa lacustrine mudstones and a thick succes- the increase in salt volume reflects increased aridity in the Early sion of latest Permian to Early Triassic fluvial sands (Newell et al., Triassic, but is a result of increased tectonic activity and the creation 2010, 2012). of many isolated, low-latitude rift basins and intracratonic sags that These examples from Germany and Russia provide evidence that in formed suitable sites for salt accumulation. two northern hemisphere basins the PTB is marked by a temporary positive shift in the water balance of latest Permian lakes. This could 6.6. Desertification and aeolian activity result from either increased precipitation/water inflow to the lakes or because of decreased evaporation. The timing of these anomalous In the Late Permian, Pangaea was characterised by high average perennial lacustrine deposits relative to the Siberian flood basalts temperatures and vast continental interiors with unusually wide is uncertain, but it has been suggested that sulphur emissions from semiarid to subhumid climate belts (Chumakov and Zharkov, 2003). the eruptions would have created short-term climate cooling (and Large areas of the land surface were thus at risk from desertification reduced evaporation), which, given the high latitude of the eruptions, should global mean temperature rise higher. may have had most impact on the northern hemisphere (Black et al., The geological record of large Late Permian deserts is relatively 2012). However, laminated shales coincident with the PTB are also limited, with extensive areas of aeolian dune sandstones best known from the southern hemisphere Karoo Basin, which were known from the Paraná Basin of eastern South America (Preto et al., interpreted by Smith (1995) and Ward et al. (2000) as evidence for an 2010). This basin was located in the arid western sector of Pangaea episode of extensive playa lakes in an otherwise fluvially-dominated and was probably strongly influenced by a rain shadow effect. At the succession. On the other hand, Gastaldo et al. (2009) have questioned PTB there appears to have been a geographic expansion in the area of the uniqueness and environmental significance of the PTB event bed aeolian activity, with ergs developing in a number of new locations in the Karoo Basin, but their interpretation has been rejected by Ward including the rift basins of Iberia (Soria et al., 2011; López-Gómez et et al. (2012). al., 2012), the south Urals (Tverdokhlebov et al., 2003), and central Early Triassic fluviolacustrine deposits of the North German Basin Europe (Uličný, 2004) in what were formerly relatively humid environ- are also notable because they contain common oolitic and microbial ments in the Late Permian. carbonates, particularly in the Dienerian to Smithian Bemburg Forma- tion, which overlies the Calvörde Formation discussed above (Paul 7. Evidence for atmospheric change and Peryt, 2000). The Bemburg Formation is generally accepted as a non-marine deposit, but the microbial carbonates mirror the appear- 7.1. Carbon dioxide ance of this anachronistic facies in Early Triassic shallow marine settings (Wignall, 2008). In these marine deposits, it has been suggested that Variation in the carbon-isotope stratigraphy across at the EPME such microbialites may record carbonate supersaturation from the has been widely explored because it is recorded in both marine and M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 1321 terrestrial settings (Korte and Kozur, 2010; S.-z. Shen et al., 2011). al., 2012). These differences between modelled (low of 13–16%) and The pronounced negative carbon isotopic excursion at the PTB has charcoal-based (low of 18.5%) atmospheric oxygen compositions in long been known and is key evidence in many extinction scenarios. the Early and Middle Triassic are profound in their implications for A causal link between major changes in the global carbon cycle in life, and whether hypoxia had a key role as a killing agent, and they re- the oceans and the atmosphere and the synchronous eruption of the quire further exploration. Siberian flood basalts seems likely (Korte and Kozur, 2010), but the magnitude of the negative excursion requires additional inputs of iso- 7.3. Sulphur, chlorine, and fluorine topically light carbon from sources such as methane hydrate release or thermal metamorphism of coal and organic-rich shale (Wignall, Degassing of the Siberian Traps would have released a range of other 2007; Grasby et al., 2011). volatiles into the atmosphere, such as sulphur, chlorine, and fluorine. Using the stomatal leaf index, Retallack (2012) compiled estimates Measurements of these volatiles in melt inclusions from the Siberian of atmospheric CO2 through the Permian and Triassic: he noted peaks Traps show concentrations that are anomalously high relative to other in the mid-Capitanian, at the PTB, and six further peaks through the continental flood basalts (Black et al., 2012). Contact metamorphism

Early and Middle Triassic. The highest calculated level of CO2 was at of evaporites and coals during the volcanic eruptions would have the EPME horizon, a remarkable 7832±1676 ppm, which is 28 times been a second source of volatile gas release (Svensen et al., 2009). the postglacial–preindustrial CO2 levels of 280 ppm, and 20 times the Kump et al. (2005) suggested that anoxia may have become suffi- current, industrial value of 394 ppm. The broad magnitudes of these ciently severe in the oceans at the EPME that hydrogen sulphide estimates have been confirmed from carbon isotopic measurements leaked into the atmosphere, with the combined effect of reaching on palaeosol carbonates (Retallack, 2012). toxic levels, destroying the ozone shield, and raising methane levels. The elevated levels of carbon dioxide and methane in the atmo- The injection of sulphur, chlorine, and fluorine into the upper atmo- sphere drove a runaway greenhouse effect (Wignall, 2008). The EPME sphere could have had a range of other effects including direct toxic- carbon isotope shift was not an isolated event: a second major negative ity, acid rain, and temperature change. Volcanic SO2 reacts with excursion occurred shortly after the first (Xie et al., 2007), and a series water in the atmosphere to form sulphate aerosols, which increase of high-magnitude fluctuations continued throughout much of the the optical depth of the atmosphere and may result in a short (pos- Early Triassic (Payne et al., 2004; Retallack et al., 2011). It is still un- sibly a maximum of 10 years) episode of global cooling (Black et al., certain whether the carbon isotope fluctuations that followed the 2012). EPME are the result of external drivers such as further volcanism or the result of internal feedbacks from a disrupted global carbon 7.4. Destruction of the ozone layer (?) cycle. Destruction of the ozone layer has become increasingly popular as a 7.2. Oxygen postulated mechanism for EPME extinction on land, especially as an agent that killed plants (e.g. Kump et al., 2005; Collinson et al., 2006; Low atmospheric oxygen levels around the PTB are based primar- Beerling, 2007; Beerling et al., 2007), and yet evidence is currently lim- ily on the isotope mass balance model of Berner (2005), which pre- ited (Wignall, 2007). dicted a continuous drop in O2 concentration from ~30% to ~13% The evidence for destruction of the ozone layer is the appearance over a 20 Myr period from the Middle Permian to Middle Triassic. In of mutated spores and pollen at the EPME (Visscher et al., 2004), the stratigraphic record, undisputed supporting evidence for low at- interpreted as a result of increased UV-B radiation which would mospheric oxygen levels has yet to be found; conclusions based on have disrupted normal meiotic (cell division) processes. Beerling palaeosol mineralogy (Huggett and Hesselbo, 2003; Sheldon and et al. (2007), however, note a measure of uncertainty about the envi- Retallack, 2003) and the palaeobiology of (Retallack et ronmental agent that caused such . They cite work that al., 2003) have both proved to be controversial. Glasspool and Scott shows such mutations of pollen in modern soybean caused by elevat- (2010) reconstructed an oxygen curve from charcoal and wildfire ed UV-B radiation, but they note further work that shows mutated data, with a highest value of 29% in the Early Permian, matching the pollen and spores in modern gymnosperms can be induced by high Berner (2005) model value, and a low of 18.5% in the Middle Triassic, levels of sulphur dioxide in polluted areas. If this is the case, then but with uncertainty over Early Triassic values because of the coal the primary evidence for destruction of the ozone layer at the time gap. Charcoal is rare to absent after the EPME, re-appearing sporadi- of the EPME is shaky. cally in the Spathian–Anisian, and achieving pre-crisis values in the In modelling how the ozone layer might have been destroyed, Anisian (Mangerud and Rømuld, 1991; Uhl and Montenari, 2011; Kump et al. (2005) emphasised the role of massive sulphide release Abu Hamad et al., 2012). in the oceans. They argued that hydrogen sulphide reacts with oxy- The charcoal gap in the Early Triassic has been used as evidence gen in the stratosphere, oxygen levels then fall, and, because oxygen for excessively low atmospheric oxygen levels in the Triassic as a is an essential reactant in the production of ozone, the loss of strato- whole, and the Early and Middle Triassic in particular. This is based spheric oxygen leads to the destruction of the ozone layer. Lamarque on the assumption that relatively high oxygen levels are required et al. (2006), on the other hand, argued that the ozone layer could for spontaneous fires to occur (A.C. Scott, 2000), and the suggestion have been damaged by levels of methane some 5000 times of excessively low (b12%) levels of oxygen in the entire Triassic preindustrial values. In a third system, Visscher et al. (2004) argued (Berner, 2005). However, high oxygen levels are not essential for spon- that the ozone layer was destroyed by the production of large quan- taneous wildfires (Belcher and McElwain, 2008), and the absence of re- tities of organohalogens that arose from the heating of organic-rich cords of wildfires in the Induan or early (see Section 6.3)is rocks and hydrothermal fluids during the eruption of the Siberian probably more directly explained by the absence of forests and the Traps. Halogen emissions can destroy atmospheric ozone. Beerling ‘coal gap’ (Uhl and Montenari, 2011; Abu Hamad et al., 2012). All et al. (2007) estimated the effects of releases of both HCl from the the indicators of wildfires, namely fossil charcoal, inertinites, and py- volcanic eruption itself, and organohalogens such as chloromethane rogenic polycyclic aromatic hydrocarbons, increased in frequency arising from the passage of molten lava through the rich coal de- through the Triassic, from very low levels in the Early Triassic, to Perm- posits around the Siberian Traps. They found that, at high levels of in- ian levels. This could indicate a collecting bias, or that it took much of jection of those gases into the stratosphere, the ozone layer would be the Triassic for sufficient woody material to become available following penetrated at high latitudes, but not around the Equator because of the re-emergence of forests at the end of the ‘coal gap’ (Abu Hamad et its ‘self-healing’ properties. 1322 M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337

Only the last of these three models has survived scrutiny (Wignall, disappearance or extreme decline of a range of gymnospermous and 2007; Harfoot et al., 2008). The postulated volumes of hydrogen pteridophytic palynomorph groups. Earliest Triassic macrofloras and sulphide and methane required to destroy the ozone shield are far palynofloras in Antarctica were dominated by peltasperms and beyond anything possible, so leaving the third, halogen, model as lycophytes; corystosperms, conifers, and ferns become increasingly the only viable explanation. But was the ozone shield breached at common elements of assemblages through the Lower Triassic part the time of the EPME? The only evidence is from the mutated spores of the formation and dominate floras of the Upper Triassic strata. and pollen, which could have arisen from other drivers. However, es- In a numerical study of land–plant diversity through the Permo- timated volumes of halogens ejected from the Siberian Trap eruptions Triassic of South China, Xiong and Wang (2011) found that total are unusually high (Black et al., 2012), as was the explosive nature of diversity declined steadily from the early Late Permian (Wuchiapingian) the eruptions, which might have propelled those halogens into the to the early Middle Triassic (Anisian), a span from 260 to 237 Myr ago), stratosphere, so the suggestion of enhanced UV radiation as a poten- based on macroplant fossils (Fig. 9). (pollen and spores), on tial killer at the EPME has not been rejected. the other hand, showed only a small fluctuation across the PTB and this was in fact a diversity rise. The long-assumed relative stability of plants 8. Plant evolution through the Permo-Triassic crises through the PTB crisis is confirmed in this study, although rates of generic extinction were acutely high (91%) in the Induan (earliest The timing of extinction patterns among plants at the PTB has been Triassic), at a time when origination rates were also at their lowest debated, and patterns differ in the northern and southern hemispheres level (18%) for the sampled time interval. Importantly, however, (McLoughlin et al., 1997; McElwain and Punyasena, 2007; Xiong and Xiong and Wang (2011) identify that land plants in South China Wang, 2011). Certainly, the cool-adapted Glossopteris flora of Gondwa- underwent sustained high extinction rates (>60%) throughout the en- na disappeared (Retallack, 1995), but the wider debate may have been tire Late Permian to early Middle Triassic interval, a span of 23 Myr, partly obscured by the use of a distinct terminology and methodology compared to estimated durations of heightened extinction among (DiMichele et al., 2008). In particular, palaeobotanists generally de- marine faunas of some 3–11 Myr (Payne et al., 2004, 2011b; Chen scribed the evolution of floras through the Permian and Triassic in and Benton, 2012). Considered in a broader context, these times of terms of the long term replacement of so-called Paleophytic floras, enhanced extinction were part of continued fluctuations in generic dominated by broad-leaved pteridosperms, cordaites, and pecopterid turnover through the entire Permian and Triassic time span, perhaps ferns, by Mesophytic floras largely of conifers (Knoll, 1984; Knoll and related to the major changes in temperature and aridity through this Niklas, 1987; Traverse, 1988). This transition began well before the interval. Xiong and Wang (2011, p. 157) conclude that ‘More stable PTB, and lasted essentially from the end of the Early Permian to the diversity and turnover rate as well as longer extinction duration suggest Middle Triassic, and it did not seem that the PTB was a focus for that land plants near the PTB of South China may have been involved in enhanced extinction, or that plant life in any sense had to ‘recover’ agradualfloral reorganisation and evolutionary replacement rather from a crisis analogous to that which affected animals. than a mass extinction like those in the coeval marine faunas.’ These observations have always seemed at odds with the evidence The moderate to high rates of extinction of plant species and genera that acid rain and massive erosion may have affected the land surface were not reflected in the loss of major clades other than Glossopteridales, of large parts of the world at the time of the PTB (Newell et al., 1999; and this appears to be a difference from extinctions (Wing, Ward et al., 2000; Algeo and Twitchett, 2010), and that the first 2004; McElwain and Punyasena, 2007). If this is the case, longer-term 15 Myr of the Triassic are notable for the ‘coal gap’ (Retallack et al., changes among plants, and the apparent absence of a sharp, single 1996, 2011), a time during which trees were rare to absent, and event, paints a picture of broader-scale floral biome evolution and turn- coals, plentiful in the latest Permian, did not recur until well into over, with species and genera being replaced over long time spans. the Middle Triassic. Plants differ from most animals in being autotrophic primary producers, Indeed, DiMichele et al. (2008) suggest that use of the ‘Paleophytic’ limited by temperature, rainfall, and topography, but perhaps less liable and ‘Mesophytic’ concepts has been misleading, and they recommend to sudden extinction by environmental shock. It may indeed be true abandonment of the terms. They report that there is no evidence for that plants have more survival strategies than many animals, and global ‘Paleophytic’ and ‘Mesophytic’ floras. Instead, they argue that can survive certain kinds of environmental crisis by or Permo-Triassic plants are best thought of as occurring in a complex by the loss of only certain species and genera within higher taxa of biome-scale species pools that reflected climate at many spatio- (Traverse, 1988; Valentine et al., 1991). temporal scales. Therefore, they recommend that vegetational changes In a global-scale study of fossil plant families, Cascales-Miñana and in the late and early will be best understood in Cleal (2012) found that the EPME did stand out as a major extinction terms of responses of such species pools to global climate changes, at event. The extinction affected some non-seed-plant families, especially local and regional scales. This is a more complex approach, requiring those of palaeotropical wetlands (e.g. Bowmanitaceae, Lepidocarpaceae, intense study of palaeobotany and sedimentology of individual ba- Asterothecaceae), but the most severe effects were on seed-plant fami- sins, but it highlights the problem hitherto of confounding floral suc- lies, particularly conifers. This may seem a surprising result because co- cessions that reflect changes in palaeogeography, climate, and nifers are known to be well adapted to survive in stressed conditions, topographic location with temporal or evolutionary changes. Some especially shortage of water, and increased aridity was one of the terrestrial settings, such as low-lying basins, preserve floras better features of the Late Permian and the EPME (see Section 6). However, than others, such as mountains, and stratigraphic successions that many of the conifer families that died out were monogeneric. Survivors document changing florasmaysimplybesamplingchangingenvi- among the non-seed plants were mostly small in habit, such as ronmental conditions rather than evolution. As temperature and the Lycopodiaceae, Selaginellaceae, Isoetaceae, Equisetaceae, and rainfall change through time, so too may the assemblages of plants, Gleicheniaceae, all of which survive to the present day. Fewer characterised as distinct biomes or species pools by DiMichele et seed plants survived, and these include Cycadaceae, which are al. (2008, p. 161), ‘assemblages of plants tied to different kinds and also alive today, and perhaps their slow growth and reproductive ranges of environmental conditions, and strongly reflective of the strategy helped them at the time of the EPME, and through subse- naturally sharp environmental discontinuities that characterise ter- quent crises. restrial Earth.’ The replacement of stable gymnosperm-dominated Permian floras Detailed studies in Antarctica, and generalised across Gondwana by rapidly growing, early successional communities dominated by lyco- (McLoughlin et al., 1997) show that the PTB was marked by the ex- pods and ferns in the earliest Triassic of the northern hemisphere tinction of glossopterid and cordaitalean gymnosperms, and by the (Grauvogel-Stamm and Ash, 2005; Galfetti et al., 2007; Hermann et al., M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 1323

600

500

s e i c e 400 p s l i s s o 300 f a g e

M

200 Number of taxa of Number genera 100 Megafossil genera

ASS-ART KU-RO W-C WU CH I O ANS LAD CRN-NOR1 NOR2-R PERMIAN TRIASSIC

Fig. 9. Diversity of land–plant taxa across the PTB of South China. Plant vignettes are, from left to right, Glossopteris, Gigantopteris, Pleuromeia, and Araucaria, each typical of the time interval in question. Abbreviations: ANS, Anisian; ART, Artinskian; ASS, ; C, Capitanian; CH, Changhsingian; CRN, Carnian; I, Induan; KU, Kungurian; LAD, ; NOR, Norian; O, Olenekian; R, Rhaetian; RO, Roadian; W, ; and Wu, Wuchiapingian. Modified from Xiong and Wang (2011).

2011), resulted in reduced sequestration of organic matter in terrestrial 9. Insect evolution through the Permo-Triassic crises facies during the Early Triassic ‘coal gap’ (Veevers et al., 1994; Retallack et al., 1996, 2011). The changeover in floras is marked also by the well The fossil record of insects through the Permian and Triassic has not known ‘spore spike’ at or close to the PTB, which is marked by high abun- provided a clear picture of their evolution in response to possible envi- dance of the enigmatic palynomorph Reduviasporonites. This is identified ronmental stresses, nor of their response to the EPME, and many noted by some authors as a fungal spore (Eshet et al., 1995; Visscher, et al., palaeoentomologists are not convinced that there even was a crisis: 1996) and by others as an algal spore (Foster et al., 2002). Whether a Ponomarenko (2006), for example, argues rather that there was noth- ‘fungal event’ or an ‘algal event’, the spore spike reflects the massive ing other than a long-term decline. Labandeira and Sepkoski (1993) dieback of plants of the latest Permian gymnosperm-dominated ecosys- and Béthoux et al. (2005) accept that there was a mass extinction tems prior to the radiation of lycopods. event, but they note the problems of a temporally and geographically Earliest Triassic floras throughout Eurasia and the southern conti- incomplete fossil record, the lack of extensive study of many entomo- nents were dominated by dense stands of the succulent lycopod faunas, and the absence of an agreed phylogenetic system. Pleuromeia, which reached a height of 2 m at most. This would An enduring problem for understanding the response of insects to appear to be a classic ‘disaster taxon’, which emerged suddenly into the EPME is that there is a largely unsampled temporal gap, spanning the post-extinction world, and did so worldwide — cosmopolitanism the Late Permian and Early Triassic, and insect faunas can only be following the loss of endemic floras and faunas is a key feature of the compared at either end. This gap was estimated at 15 Myr by initial post-crisis recovery. Pleuromeia was unusually abundant, with Béthoux et al. (2005),butShcherbakov (2008b) pruned that to less its spores (Densoisporites) dominating palynological assemblages to than 5 Myr. The latter author noted that there are several very levels over 90% (Looy et al., 1999), so floras were spectacularly uneven, good insect faunas from the latest Permian of the Sydney and or unbalanced, and all other plant taxa were rare. Pleuromeia dominated Karoo basins, as well as five or six fossil insect sites in the Early Trias- terrestrial floras to the end of the Early Triassic, a span of 4–5Myr,and sic of Russia and Mongolia, including the Babiy Kamen' site in the was then replaced wholesale in the earliest Middle Triassic by floras Kuznetsk Basin, which has yielded representatives of more than 15 dominated by the conifer Voltzia (Looy et al., 1999; Hermann et al., insect families. 2011). Floras dominated by Dicroidium in Gondwana did not attain In their global-scale study, Labandeira and Sepkoski (1993) docu- Permian levels of diversity and provinciality until the Middle Triassic mented that 8 out of 27 orders of insects (30%) disappeared in the (Retallack, 1995; McLoughlin et al., 1997). A further spore spike oc- Late Permian to Early Triassic interval, and a further three that sur- curred in the middle Smithian (Hermann et al., 2011), preceding the vived into the Triassic at reduced diversity became extinct during end-Smithian extinction when the lycopods were replaced by woody that period. The extinction rate through the Late Permian at familial gymnosperms, indicating a switch from warm and equable climates to level was about 50%, on a par with vertebrates and with marine or- latitudinally differentiated climates (Galfetti et al., 2007; Hermann et ganisms as a whole (Sepkoski, 1984; Benton, 1995). On the other al., 2011). hand, it should be noted that insects evolve slowly when compared The ‘coal gap’, lasting through the Early and early Middle Triassic to tetrapods: for example, looking back from the present day to the corresponds then to a time of overall impoverishment of terrestrial KT boundary 65 Myr ago, nearly 100% of contemporary insect fami- floras. Plants had declined substantially in diversity through the lies still had representatives, whereas this is true for only 20% of EPME, and they diversified again in the Smithian, but did not return tetrapod families (Labandeira and Sepkoski, 1993) — such compari- to pre-extinction levels until the Late Triassic (Retallack et al., sons of course depend on the assumption of equivalence of families 2011). During the recovery phase, some long-lasting clades that of insects and tetrapods. In an overview focusing on Russian sites, survive today appeared, including many fern families, but especially Shcherbakov (2008a) notes a loss of 40% of insect families through a substantial diversification of seed plants, including conifers, seed the latest Permian to Induan interval, but he notes also that there ferns, ginkgophytes, and . were high extinction peaks in the Middle Permian (Kazanian) and 1324 M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337

Middle Triassic (Ladinian). It is hard to establish the true nature of ex- specimens in museums, and this has clarified many aspects tinction and origination of insects through this episode, and whether of basic geology and alpha taxonomy. these apparent extinction peaks are real or not. (3) The cladistic revolution has meant that every group of Permo- Detailed studies of two large clades, the Archaeorthoptera and Triassic tetrapods has been revised thoroughly and in a cladistic , reveal common trends (Béthoux et al., 2005). Several context, and this provides reasonable phylogenetic trees, which lineages became extinct at or close to the PTB, and other clades either in turn allow meaningful phylogenetic correction of diversity esti- expanded or appeared in the Middle Triassic. There were important mates, and the possibility of palaeobiogeographic and functional- radiations of Diptera (flies) and Coleoptera () in the Triassic, morphometric studies. which confirms the role of the EPME in stimulating a major turnover in insect faunas, and in setting some of the groundwork of modern 10.2. Scaling the vertebrate extinctions insect ecosystems. The Late Permian to Middle Triassic turnover in entomofaunas was So far, most attention has focused on tetrapods rather than fishes. marked also by major changes in ecology, as the late Mississippian to Pitrat (1973) found that marine fishes declined in diversity sharply Permian fauna of herbivorous (mites and apterygote and at the end of the Permian, just like other marine animals, but that pterygote insects feeding on pteridophytes and basal gymno- freshwater and eurhyaline fishes experienced their main extinctions sperms) gave way to the modern phase (Triassic to Recent) comprising earlier in the Permian. Thomson (1977, p. 401) also concluded that mites, orthopteroids, hemipteroids, and basal holometabolans feeding ‘there is little evidence among fishes for a Permo-Triassic mass ex- on pteridophytes and gymnosperms (Labandeira, 2006). The latter as- tinction’. Benton (1989b), on the other hand, identified an extinction semblage persisted of course when additional novel groups rate of 44% for all families of fishes through the Late Permian, but began feeding on angiosperms from the to Recent. It is with most of the losses occurring in the Kazanian, the stage that frustrating, in light of the crucial importance of the Late Permian to then preceded the terminal-Permian Tatarian. Such a ‘Kazanian’ Early Triassic interval in witnessing one of the four key diversifica- event would now equate to Roadian in the Middle Permian, but the tions in insect evolution, that this episode cannot be investigated dating of Permian fish-bearing units against the global standard in more detail: palaeontologists can only hope for new discoveries time scale has changed substantially since 1989, and the ‘Kazanian of rich insect-bearing fossil deposits in the latest Permian and Early event’ is likely to disappear. Meaningful regional and global-scale Triassic terrestrial deposits, perhaps in Russia, China, and South studies of fish diversity and disparity across the PTB are still Africa. required. In narrative terms, the EPME had a notable impact on tetrapod evo- 10. Vertebrate evolution through the Permo-Triassic crises lution. Complex latest Permian ecosystems dominated by herbivorous pareiasaurs and and carnivorous gorgonopsians, were re- 10.1. Changing opinions placed by new clades of (crurotarsans, dinosauromorphs) and () (Benton, 1983, 1995; Ward et al., 2000; Just as with plants and insects, many palaeontologists did not see Benton and Twitchett, 2003; Benton et al., 2004; Brusatte et al., 2008, compelling evidence for a mass extinction among vertebrates at the 2010, 2011; Sookias et al., 2012). The difficulties arise when this broad end of the Permian. For example in the standard textbook in the field, narrative is explored in closer, numerical detail. Carroll (1988) wrote: ‘The most dramatic extinction in the marine envi- In an early compilation of family-level data, Benton (1985, 1987) ronment occurred at the end of the Permian, wiping out 95% of the found an extinction rate of 49% through the Tatarian to Scythian in- non-vertebrate species and more than half the families. Surprisingly, terval. Benton (1989a) listed 21 families of amniotes that had died there was not a correspondingly large extinction of either terrestrial out during the EPME, and noted that six out of nine fami- or aquatic tetrapods.’ Carroll (1988) was echoing conclusions reached lies disappeared. Taking these data further, Maxwell (1992) identified earlier by Pitrat (1973) and Thomson (1977), and accepted by Erwin extinction rates of 67% and 78% for amphibian and families (1990) and others at the time as evidence that the end-Permian mass respectively, the highest rates throughout the entire Permian and extinction was largely a marine affair that had little effect on terrestrial Triassic. life. Based on the new ‘Early Tetrapods Database’ (ETD; Benton et al., Viewpoints have changed substantially since 1990, not only for in press), an updated record of all basal tetrapod genera from Devo- plants and insects, but importantly for vertebrates, whose record nian to (Table 2), four out of 11 families of (36%) through the Permian and Triassic has now been studied in consider- and 17 out of 32 families of amniotes (53%) became extinct at the able detail. There are still of course all the serious problems of an in- end of the Changhsingian. This represents an overall loss at family complete and highly sporadic fossil record, which must be recognised level of 49% of tetrapods through the EPME, equivalent to the figure and mitigated if possible (Benton et al., 2004, in press; Smith, 2007; noted by Benton (1985), but based on substantially revised data. It is Irmis and Whiteside, 2012). However, since 1990, three practical important to note that 11 of the 22 familial lineages (50%) that sur- improvements have occurred that enable such studies: vived through the EPME were extinct by the end of the Induan, evi- dence of a ‘dead walking’ effect (Jablonski, 2001). There was a (1) Stratigraphic reference sections have been established for the high rate of origination of new tetrapod families, especially amni- Permian and Triassic, and the new standard Permian time otes, in the Early Triassic, but a high proportion of these died out be- scale (Gradstein et al., 2004; Ogg et al., 2008) has hugely changed fore the end of the Olenekian (Table 2), and this was especially true and stabilised understanding. This is especially true for the for amphibians, which lost 10 out of 15 families (67%), compared to Permian, where the switch from the Russian continental time 7 out of 26 families of amniotes (27%), which together equate to a divisions (Ufimian, Kazanian, Tatarian) to North American and high value for all tetrapods (41%). Chinese marine systems (, Lopingian) for the The analysis can be continued at generic level, but the gains in taxo- Middle and Upper Permian, respectively, has made an enormous nomic detail are offset by losses in statistical confidence because of the difference to assumptions about correlation and relative timings likely deterioration in completeness of sampling at lower taxonomic of key tetrapod-bearing successions (e.g. Rubidge et al., 2010; levels (Sepkoski, 1984; Robeck et al., 2000). Taken at face value, the Benton, 2012). ETD data show a rise in tetrapod generic diversity from 94 to 112 (2) Palaeontologists have been able to move freely between the from the Changhsingian to Induan stages, crossing the PTB (Fig. 10, West, Russia, and China to compare sections in the field and arrow 5; Benton et al., in press). This seemingly counter-intuitive result M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 1325

Table 2 Induan stage. So, the actual generic loss across the PTB was 84 out of 94 Survival and extinction of tetrapod families through the EPME and Lower Triassic intervals. genera present in the Changhsingian stage (89% generic loss for tetra- Families represented by a single genus are marked with an asterisk (*). pods). The recovery after the EPME is shown by the origin of 102 out Basal tetrapods (‘amphibians’) Amniotes (‘’) of 112 taxa that were present in the Induan (a remarkably high origina- Families that died out during the EPME tion rate of 91%). Melosauridae ROA–CHX *Nyctiphruretidae WOR–CHX *Dvinosauridae WUC(u)–CHX Pareiasauridae WOR–CHX 10.3. Triassic recovery of vertebrates Discosauriscidae SAK(l)–CHX Captorhinidae MOS(u)–CHX Karpinskiosauridae CAP(l)–CHX *Claudiosauridae WUC(l)–CHX Burnetiidae WOR–CHX Problems of selective preservation of fossils and changes in sedi- Ictidorhinidae WOR–CHX mentary facies especially confound the data on tetrapod recovery in Pylaecephalidae WOR–CHX the Early and Middle Triassic, and it is hard to know how to correct Emydopidae WOR–CHX for such a bias (Benton et al., 2004; Irmis and Whiteside, 2012). For Oudenodontidae WOR–CHX example, the raw data for the earliest Triassic (Induan stage) show Aulacephalodontidae WUC(l)–CHX ‘ ’ Dicynodontidae WUC(l)–CHX a remarkable diversity peak for amphibians , with the origin of 50 Gorgonopsidae ROA–CHX of 58 genera (86% rise), but followed by a rate of loss that was just Moschorhinidae WUC(u)–CHX as rapid as their rise, as was noted from the familial data (Fig. 10; – Scylacosauridae WOR CHX Table 2). This diversity peak among temnospondyls and other Whaitsiidae CAP(u)–CHX *Dviniidae WUC(u)–CHX non-amniotes has long been noted (Milner, 1990; Benton et al., Procynosuchidae WUC(l)–CHX 2004; Ruta and Benton, 2008), but has yet to be fully understood. Was this a real burst of radiation following the EPME, in which the pri- Families that survived the EPME marily aquatic temnospondyls were disaster taxa that were somehow – – ? MOS(l) IND Owenettidae WUC(l) CRN(l) favoured by prevailing climatic conditions, or is this an artefact of a Amphibamidae MOS(u)–IND Procolophonidae CHX–RHT(u) Tupilakosauridae ROA–IND Weigeltisauridae WUC(l)–IND major change in sedimentation across the PTB towards higher-energy WOR–IND Paliguanidae WUC(l)–IND streams (Newell et al., 1999; Ward et al., 2000) that show excessive pres- WUC(l)–ANS(u) Tangasauridae WUC(l)–IND ervation of the detrital remains of water-living animals combined with – – Chroniosuchidae WOR CRN(u) Younginidae WUC(l) IND under-representation of other ecological categories, including terrestrial Byrtrowianidae CHX–LAD(u) Protorosauridae WUC(l)–OLE(u) Proterosuchidae CHX–ANS(u) amniotes? Myosauridae WUC(l)–IND Numerical palaeoecological studies confirm the unusual nature of Kingoriidae CAP(u)–ANS(l) these earliest Triassic terrestrial tetrapod communities. Roopnarine et Lystrosauridae WUC(u)–OLE(l) al. (2007) applied a trophic network model to Permian and Triassic – Akidognathidae WUC(l) IND communities of the Karoo Basin, South Africa, and showed that Ictidosuchidae CAP(u)–ANS(u) Scaloposauridae CAP(u)–IND while Permian communities did not appear to be especially suscepti- Galesauridae WUC(l)–ANS(l) ble to extinction, Early Triassic communities were markedly less sta- ble. The instability was reflected in the incomplete trophic webs in Families that originated and went extinct during the Early Triassic the earliest Triassic, in which large herbivores and predators were ab- Triadobatrachidae IND–OLE(u) Nanchangosauridae OLE(u)–OLE(u) Odenwaldiidae OLE(l)–OLE(u) Grippiidae OLE(u)–OLE(u) sent, and in which some taxa such as Lystrosaurus and many of the Parotosuchidae IND–OLE(u) *Merriamosauridae OLE(u)–OLE(u) temnospondyls were seemingly over-represented. It will be impor- Lapillopsidae IND–IND *Parvinatatoridae IND–IND tant to carry this study forward to explore Olenekian and Middle Tri- IND–OLE(l) Utatsusauridae IND–IND assic tetrapod communities to determine when stability was – – Benthosuchidae IND OLE(u) *Ericiolacertidae IND IND re-established. The restructuring of Induan tetrapod communities *Lyrocephaliscidae OLE(u)–OLE(u) Regisauridae IND–IND Platystegidae OLE(u)–OLE(u) is seen in the loss of browsers and predators and the increase in Derwentiidae IND–OLE(u) piscivores (Sahney and Benton, 2008).Thelossofbrowserscould Thoosuchidae OLE(l)–OLE(u) be linked to changes in vegetation, marked by the Early Triassic ‘coal gap’, linked to the major worldwide change in sedimentation Families that originated in the Early Triassic and survived into the Middle Triassic Cyclotosauridae IND–RHT(l) *Omphalosauridae OLE(u)–ABS(u) regime to high-energy erosion at the PTB (Newell et al., 1999; OLE(u)–LAD(u) Cymbospondylidae OLE(u)–CRN(u) Ward et al., 2000). Perhaps only when the full diversity of plant Brachyopidae IND–ANS(l) Mixosauridae OLE(u)–ANS(u) types, and more substantial biomass, was achieved in the Middle Tri- Plagiosauridae IND–RHT(u) Kuehneosauridae OLE(u)–NOR(u) assic could tetrapod herbivores achieve their pre-extinction diversi- – – Trematosauridae IND CRN(l) Sphenodontidae IND REC ty and abundance. Thalattosauridae IND–CRN(u) Cymatosauridae OLE(u)–ANS(l) Following a late Olenekian peak of 90 tetrapod genera, diversity Pachypleurosauridae OLE(u)–LAD(u) fell to 76 in the lower Anisian, rose again to 96 in the late Anisian, Pistosauridae OLE(u)–CRN(l) and then plummeted to 39 in the lower Ladinian (Fig. 10, arrow 6). – Rhynchosauridae IND NOR(l) In earlier works, Benton (1985, 1995) and Maxwell (1992) noted Prolacertidae IND–NOR(m) a terminal Early Triassic peak of extinction among tetrapods, but OLE(u)–NOR(m) OLE(u)–ANS(u) re-dating of redbed units in South Africa (e.g. Assem- Ctenosauriscidae OLE(l)–ANS(u) blage Zone) and elsewhere, has extended many formerly late Kannemeyeriidae OLE(u)–CRN(u) Olenekian ranges into the Middle Triassic. It is yet to be resolved, – Bauriidae IND ANS(u) however, whether any of these declines are real, and match the *Cynognathidae OLE(u)–ANS(u) *Thrinaxodontidae IND–LAD(u) turbulence in atmospheric and oceanic conditions that continued IND–ANS(u) through the Olenekian and early Anisian (Payne et al., 2004), or are artefacts of sampling.

10.4. Regional studies on vertebrate extinction and recovery of a rise in diversity across the largest mass extinction horizon of all time arises because the totals encompass major losses of genera in the These kinds of global-scale diversity studies may never yield a Changhsingian, and an even higher rate of origination in the subsequent detailed narrative of what really happened through the EPME and 1326 M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337

A of the Vyatkian, the terminal Permian Russian time unit, and the ex- tinction of nine of these corresponds to a regional family-level ex- tinction rate of 82%. Earliest Triassic terrestrial ecosystems in Russia were unusual and seemingly ecologically unbalanced. As well as the two surviving reptile families, the procolophonids and dicynodonts, the faunas were dominated by temnospondyls, as noted above. In the basal Triassic (Kopanskaya Svita; Induan), there were only medium-sized and large fish-eaters in the rivers and lakes (Tupilakosauridae, Capitosauridae, Benthosuchidae) and medium-sized insect/ tetrapod-eaters (Prolacertidae, Proterosuchidae). Dicynodonts must have been present, and indeed Lystrosaurus is known from localities in Siberia. Only one genus, Tupilakosaurus, could be identified as a ‘disaster taxon’, present for a short time immediately after the crisis. Other fam- ilies present in the Kopanskaya Svita persisted through the Early Trias- B sic. New taxa were added through the 15 Myr of the Early and Mid Triassic; further medium-sized and large fish-eaters in the fresh waters, and further medium-sized herbivores and large carnivores on land. The Middle Triassic faunas of Donguz and Bukobay times still lacked small fish-eaters and small insect-eaters, as well as large herbivores and specialist top carnivores. Middle and Late Triassic faunas from else- where in the world show the addition of further taxa that fill these ecological gaps — various amphibians as small fish-eaters, small diap- sids as insect-eaters, ever-larger dicynodonts as large herbivores, and rauisuchians as large carnivores. Statistical study of the Russian data (Benton et al., 2004) showed that the EPME did not simply remove diversity, but it also affected the dynamics of turnover within tetrapod communities. Throughout the Middle and Late Permian, origination and extinction rates followed a dramatically reversing series of peaks and troughs. The Early and Mid Triassic are characterized by the steady addition of taxa, and slow loss of existing families, but origination and extinction Fig. 10. Diversity of early tetrapods through the first half of their evolution, from the rates remained uniformly low until the Ladinian; the sudden rise at Middle (Givetian, 380 Myr ago) to Early Jurassic (, 190 Myr ago), this point might be an edge effect. Overall, the data from the South fi showing raw generic palaeodiversity data (A) and detrended ( rst differenced) data Urals indicate a slow recovery of tetrapod ecosystems, which seemed (B), against a substage-level time scale. Curves for ‘amphibians’ (= non-amniote tetrapods), amniotes, and tetrapods (= ‘amphibians’+amniotes) are shown separately. Key events to remain unbalanced even at the end of the sampling period, some are marked by arrows (see text), including the end-Permian and end-Triassic mass extinc- 15 Myr after the mass extinction. tions (arrows 5 and 8 respectively). Initial analyses of the South African PTB revealed rather different re- sults. Smith and Botha (2005) reported a 69% generic extinction rate, based on their localised collection of 225 tetrapod specimens. This fig- ure might fall to 54% if ghost ranges, implying collection failure, are the Triassic recovery, because of all the problems of sampling and a taken into account (Botha and Smith, 2006). All the extinctions took patchy fossil record already noted. More fruitful may be regional or place within a single sedimentary facies, and Smith and Ward (2001) basin-scale studies and phylogenetically based analyses of individual estimate the extinction lasted for 50,000 years. Only four genera, basins or regions that explore important questions concerning the Lystrosaurus, Tetracynodon, Moschorhinus and Ictidosuchoides,survived rate of the recovery and morphological changes within diversifying the EPME in South Africa, and yet, only 37 m above the PTB in the clades. Karoo succession, Smith and Botha (2005) reported a total of ten The rate of recovery of tetrapod ecosystems has been debated, genera, compared to 13 just below the PTB. They interpreted this to whether they became re-established rather slowly, over perhaps mean that recovery was relatively fast, really within a few hundred 10–15 Myr (Benton et al., 2004) or fast, within 1–2 Myr (Smith thousand years of the mass extinction event. The key question is wheth- and Botha, 2005). Close study of events through the Middle Permian er those ten genera represent a stable ecosystem, with balanced relative to Middle Triassic in the southern Urals in Russia confirmed the com- abundances of species (no one species dominating in an unnatural plexity of events (Benton et al., 2004). Late Permian tetrapod com- fashion) and a full diversity of ecological niches filled, from small to munities in Russia consisted of seven families of amphibians and large, and across all dietary options. 15 families of reptiles. In the rivers and lakes of each of the six A comparative study by Irmis and Whiteside (2012) has suggested a Middle and Late Permian time slices, four to seven genera of small, delayed recovery in both Russia and South Africa (Fig. 11). By assessing medium and large aquatic tetrapods (‘amphibians’)fedontheabun- community evenness, they showed that ecosystem structure was dant thick-scaled bony fishes and the less common freshwater massively perturbed by the EPME in both Russia and South Africa at sharks and lungfishes. On the wooded banks were five to 11 genera the same time that overall diversity plunged, confirming the ecological of terrestrial tetrapods (‘reptiles’), ranging in size from tiny studies of Roopnarine et al. (2007) and Sahney and Benton (2008).Im- insect-eaters to rhino-sized plant-eating pareiasaurs and the wolf- portantly in these studies, Benton et al. (2004) and Irmis and Whiteside to bear-sized, sabre-toothed gorgonopsians that preyed on them. (2012) applied a variety of methods to attempt to control for bias, Twenty of the 22 Middle and Late Permian families died out at, or be- including rarefaction to normalise for differing sample sizes. In addition, fore, the PTB, and only two, the small, mainly herbivorous Benton et al. (2004, 2011) found no correlations of the diversity data procolophonids and the larger herbivorous dicynodonts, survived with metrics of sampling such as numbers of localities, numbers of through the EPME. Of the 22 families, 11 were present at the end specimens, and mean specimen quality, but this does not rule out the M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 1327 possibility that part of the pattern reflects changing sedimentary disparity, as cynodonts filled ecospace emptied by the EPME, and regimes. Finally, in presenting data on ecosystem evenness, Irmis and then a rise in diversity considerably later. Disparity rose steadily Whiteside (2012) broadened the basis of evidence for recovery: through the Early Triassic, attained a peak in the Middle Triassic evenness values appear to recover before generic richness in both areas. and then stabilised; on the other hand, diversity rose con- tinuously and substantially through the entire 50 Myr duration of 10.5. Vertebrate clades through the EPME crisis the Triassic, and the Late Triassic origin of , as traditionally defined, was not marked by a major leap in either diversity or Further recent studies have concentrated on particular clades, disparity. each of which followed its own trajectory. In a study of temnospondyl Archosaurs show similar patterns of radiation through the Triassic, evolution through the Permian and Triassic, Ruta and Benton (2008) seemingly slow and steady, rather than explosive (Benton, 1983; found that the Induan diversity peak was robust to a variety of nu- Brusatte et al., 2008, 2010, 2011; Sookias et al., 2012). Early Triassic merical treatments to control for error (different , phylo- archosaurs were predators, perhaps never abundant or diverse, and genetically corrected diversity signal, rarefied bin-by-bin samples). the clade diversified substantially through the Middle and Late Trias- Species, genus, and family trajectories consistently revealed a rapid sic, giving rise to at least by the early part of the Late Trias- increase in temnospondyl diversity from the latest Permian to earliest sic, but perhaps earlier. In both cases, the rise of basal archosaurs, and Triassic. Ruta et al. (2011) explored patterns of evolution of parareptiles then of dinosaurs in the Carnian, was a slow affair, showing the classic through the PTB, and found, after careful data exploration, little evi- disparity-first pattern in both cases (Brusatte et al., 2008), with no dence for a sudden decline among pareiasaurs and procolophonoids, sign of a massive drive or competitive process whereby they exerted but rather a rapid alternation of originations and extinctions in a num- their superior characters over other taxa. Indeed, passive processes of ber of subclades, both before and after the PTB. body size change appear to have predominated throughout the Trias- Among larger clades that crossed the PTB, anomodonts have been sic, with archosaurs in general, and dinosaurs in particular, becoming explored in most detail. Anomodonts, including dicynodonts, were abundant and diverse through opportunistic replacement of synap- important medium-sized to large herbivores in many continental sids following extinction, both the EPME, and a later series of losses ecosystems, with 128 species in 77 faunal assemblages, spanning of major herbivore groups in the Late Triassic (Benton, 1983; the Middle Permian to Late Triassic. A diversity analysis (Fröbisch, Sookias et al., 2012). An unusual feature of the rise of the mainly car- 2008, 2009) confirms the importance of an end-Guadalupian mass nivorous basal archosaurs was that these predatory forms were gen- extinction, as well as the EPME. Both events were driven not simply erally larger than their herbivore prey, perhaps because of their by enhanced extinction rate, but also by reduced origination rate. By innate biological characters in comparison to the contemporary syn- applying a variety of techniques to assess the adequacy of sampling, apsids (Sookias et al., 2012). such as comparing raw anomodont diversity to numbers of forma- tions, localities, and specimens, Fröbisch (2008, 2009) explored the 11. Killing agents data both with and without sampling correction, and concluded that the EPME remained the key crisis in their history. 11.1. Introductory remarks: advocacy or science? Phylogenetic studies show that at least four anomodont lineages survived the EPME, including the genus Lystrosaurus, formerly thought In the post-EPME world, numerous presumed consequences of the to be uniquely Triassic in age, but they survived at low abundance, and environmental crisis might have killed life, either singly or in concert, Lystrosaurus radiated explosively in the basal Triassic, as a classic gener- namely hypoxia, hypercapnia, ocean acidification, warming, aridity, alist disaster taxon (Irmis and Whiteside, 2012), superabundant and acid rain and mass wasting, wildfires, and ozone layer destruction. representing over 90% of finds in large samples from typical communi- These potential killing agents will be considered in turn. ties (Benton, 1983), geologically short-lived, as well as cosmopolitan, Before proceeding, it is worth considering how arguments about being known from South Africa, Antarctica, India, China, and Russia. In killing agents are constructed: there is a serious methodological prob- the Middle and Late Permian, most anomodont genera had been lem in determining a proper scientific approach to testing whether a endemic, known from only a single palaeogeographic region. After postulated agent had an effect or not. Geologists can certainly seek to 1 Myr or so, Lystrosaurus disappeared, to be replaced by a wider determine the evidence for each of the proposed physical environ- range of anomodont genera later in the Early Triassic, and the clade mental changes following the eruption of the Siberian Traps, their ex- expanded dramatically in the Middle Triassic, before its long decline tent, and their geographic and temporal distribution. However, it has through the Late Triassic. In terms of morphological disparity, the so far proved difficult to devise a test of a killing agent, and this has anomodonts also show evidence for a classic ‘bottleneck’ effect, been especially acute in the decades-long discussions of the KT whereby a hugely diverse and important group in the Middle and event: the impact happened, and the details can be studied, but Upper Permian was reduced to a limited species pool by the impact what actually killed the dinosaurs and ammonites? The normal line of the EPME crisis, and rebounded slowly to recover almost its pre- of argument is to establish the coincidence of the killing agent and extinction species diversity, but the former morphological disparity the extinction, to muster evidence from modern experimental biolog- was not reacquired. In other words, the EPME wiped out so much ical studies of the effects of the proposed killing agent, and to declare of anomodont morphological disparity and adaptive/ecological the likelihood of a connection. Sometimes, auxiliary evidence can be range of forms that the recovering clade could not reacquire this sought in terms of predictions of anatomical modifications (such as wealth of form, and the re-emerging clade, important as it became larger nostrils and nasal turbinates to counter hypoxia; see below). again, represented a modest remnant of the pre-extinction morpho- Normally there is no such detectable anatomical consequence. This logical range. means that, regrettably, many published arguments are examples of The two clades that came to dominate the world after the EPME advocacy rather than science. They list pieces of evidence that cumu- were the cynodonts, including the progenitors of mammals, and latively work in favour of a particular view, but provide no means of the archosaurs, including the dinosaurs. Cynodonts were a modest refutation. group in the Late Permian, but they expanded step-by-step through The most impressive approach has been meta-analytical, as the Triassic, splitting into two major clades in the Middle Triassic, employed by Knoll et al. (1996, 2007), Clapham and Payne (2011), and further diversifying through the Late Triassic and Early Jurassic, and Kiessling and Simpson (2011),inarguingthecaseforhypercap- but latterly mainly as small flesh-eaters. A study of diversity, phylog- nia, hypoxia, and ocean acidification as the EPME killers in the eny, and discrete-character disparity shows a rapid expansion of oceans. Here, summary data of all marine taxa were divided into 1328 M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337

Millions of Years Ago (Ma) Berner et al., 2007; Knoll et al., 2007). Oxygen levels in the atmosphere 266 264 262 260 258 256 254 252 250 248 246 244 242 70 1 have varied enormously through the last 600 Myr, ranging from 13% to SOUTHERN AFRICA 31%, compared to a modern value of 21% (Berner et al., 2007). Modelled .9 60 oxygen levels (see Section 7.3) fell from an estimated 28% in the Late .8 Permian to 20% at the PTB, and 16% in the Early Triassic (Berner et al., 2007), but the latter value has been recalculated as 18.5% based on char- 50 .7

Evenness ( ) coal evidence (Glasspool and Scott, 2010). .6 40 Atmospheric oxygen levels have frequently been cited as crucially .5 important in animal evolution, for example in terms of the overall in- 30 crease in animal body size through time (e.g. Graham et al., 1995; .4 Falkowski et al., 2005; Payne et al., 2009, 2011a), and especially in

Generic Richness ( ) 20 .3 the unusually large body size of insects and vertebrates during the and Permian, which has been explained by high oxy- Evenness .2 gen levels (Graham et al., 1995; Dudley, 1998; J.F. Harrison et al., 10 Raw Richness .1 2010). Further, two of the ‘big five’ mass extinctions, those at the Rarefied Richness 0 0 end of the Triassic and the EPME, were associated with falling oxygen Trop. Cist. Dicynodon Lystrosaurus Cynognathus levels, and this has been interpreted as a contributing factor in the ex- MIDDLE PERMIAN LATE PERMIAN EARLY TRIASSIC MIDDLE TRIASSIC Capitanian Wuchiaping. Changh. Ind. Olenekian Anisian tinctions, especially of vertebrates (e.g. Kump et al., 2005; Ward, -18 8 -22 6 2006). δ C -26 4 13 In marine settings, there is extensive evidence for anoxic conditions org -30 13 δ Corg Karoo 2 -34 13 carb nearly worldwide at the PTB (Wignall and Twitchett, 1996), and this

13 δ C Corg Antarctica 0

δ -38 δ13 has been seen as a major contributor to extinction and size reduction -42 Ccarb China -2 -46 -4 Capitanian Wuchiaping. Changh. Ind. Olenekian Anisian during the EPME and Early Triassic (Wignall and Twitchett, 1996; MIDDLE PERMIAN LATE PERMIAN EARLY TRIASSIC MIDDLE TRIASSIC Knoll et al., 2007). Size reduction has been noted among marine Amanak. Malokinelskaya Kutuluk. Kop St Kz Go Pe Donguz 20 1 gastropods as a whole, within some bivalve, gastropod, and lineages, and in general burrow dimensions, and this too has been 18 .9 explained by oxygen stress (Payne, 2005; Twitchett, 2007). Marine 16 .8 extinction and selection against large size during the EPME may relate in part to the reduced oxygen levels, but could also be driven by reduced 14 .7 predation pressure and decreased primary productivity (Payne et al., Evenness ( ) 12 .6 2011a), although the last point is disputed by Algeo et al. (2012) who fi 10 .5 nd no evidence, except in South China, for worldwide reduction in marine productivity. 8 .4 It is well known that major physiological effects occur in both the b Generic Richness ( ) 6 .3 hyperoxic (>21%) and hypoxic ( 21%) ranges, and the focus here is on the latter (Harrison, 2011). For example, physiological experiments 4 .2 on flies, , and beetles have shown that hypoxia generally 2 .1 decreases body size (Frazier et al., 2001; J.F. Harrison et al., 2010; RUSSIA 0 0 Payne et al., 2011a; VandenBrooks et al., 2012) by reducing develop- 266 264 262 260 258 256 254 252 250 248 246 244 242 ment time, growth rate and fecundity. Further, oxygen concentration Millions of Years Ago (Ma) is negatively correlated with tracheal diameter in insects of the Fig. 11. Regional records of diversity and extinctionamongtetrapodsinRussiaandSouthAf- same body size (Henry and Harrison, 2004; VandenBrooks et al., rica. Raw generic richness, rarefied generic richness and evenness for non-marine tetrapods 2012), causing changes to these and other respiratory organs as part from the Permo-Triassic of southern Africa (top) and Russia (bottom) to carbon isotopic re- of an adaptive response to the need for greater respiratory efficiency cords as a proxy for the global carbon cycle (middle). Vertically adjacent to each graph are (J.F. Harrison et al., 2010). Atmospheric oxygen levels can set thermal the biostratigraphic divisions used for temporalbins(assemblagezonesforsouthernAfrica 13 limits to the body size of aquatic insects at least (Verberk and Bilton, and svitas for Russia). δ Corg data from non-marine sections at Lootsberg Pass in the Karoo 13 Basin of southern Africa and Graphite Peak in Antarctica. δ Ccarb data from marine sections 2011). in South China. Amanak., Amanakskaya; Changh., Changhsingian; Cist., Cistecephalus Assem- Hypoxia also has effects on vertebrates. Alligators exhibit reduced blage Zone; Go, Gostevskaya; Ind., Induan; Kop, Kopanskaya; Kz, Kzylsaiskaya; Kutuluk., growth rates and compensatory changes in lung volume in response to Kutulukskaya; Pe, Petropavlovskaya; St, Staritskaya; Trop., Tropidostoma Assemblage Zone; changes in atmospheric oxygen (Owerkowicz et al., 2009), and carp and Wuchiaping., Wuchiapingian. Modified from Irmis and Whiteside (2012). show similar changes in their gill structures (Sollid et al., 2003). Gener- ally, experimental studies confirm that hypoxia is associated with body size reduction in fishes, alligators, snakes, rats, and (Payne et physiological categories (physiologically well or poorly buffered, al., 2011a). need for carbonate ions to build skeleton or not), and the predicted It is worth noting on the other hand that many organisms display levels of extinction and survival of each category were sufficiently remarkable hypoxia tolerance (Schmitz and Harrison, 2004; Bickler statistically distinct to confirm the prediction that physiology was and Buck, 2007). Insects, for example, are much more capable of re- the key. Such an approach is still required for life on land at this covery from anoxia than most vertebrates, but there is also a very time; but it may fail because of the much wider disparity in physiol- wide range of tolerance to hypoxia and anoxia among terrestrial in- ogy between insects, tetrapods, and plants, and the lack of uniformi- vertebrates. Crustaceans and arachnids are less tolerant to hypoxia ty in terrestrial habitats. than insects and myriapods, and this may relate to the frequency with which these organisms face such stresses (Schmitz and 11.2. Hypoxia as the EPME killer Harrison, 2004). Among vertebrates, fishes, amphibians, and reptiles are much more hypoxia-tolerant than or mammals, which re- Hypoxia has been advanced as a key killing agency during the EPME lates to the substantial differences in metabolism and oxygen require- by several authors (Retallack et al., 2003, 2006; Huey and Ward, 2005; ment between such ectotherms and endotherms (Bickler and Buck, M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 1329

2007). Among modern ectothermic vertebrates, the degrees of toler- The highest risk group were the poorly buffered forms with a high ance vary considerably. At an extreme are some carp and turtles, need for carbonate ions, such as rugose corals, rhynchonelliform bra- which can survive without any oxygen for several weeks or months. chiopods, and crinoids. Next were the well-buffered forms that need- But such short-term miracles of survival say nothing about responses ed lower amounts of carbonate, such as gastropods, bivalves, to the long-term fall in oxygen levels through the Triassic. Here, it is nautiloids, ammonoids, ostracods, and echinoids. Finally, the forms important to be aware that many or most modern ectotherms can that required little or no carbonate were the ctenostome bryozoans, tolerate hypoxia by making long-term physiological in lingulid , holothurians, conodonts, and chondrichthyans. suppressing their metabolism, being able to tolerate metabolite accumu- The generic extinction rates of these three groups were 86%, 54%, lation, and in establishing free-radical defences during reoxygenation and 5%, respectively. These figures highlight the importance of shell (Bickler and Buck, 2007). mineralogy and the key role of ocean acidification as a major killer The effects of hypoxia on plants are hard to predict, and likely of at the EPME (Clapham and Payne, 2011; Kiessling complex (Payne et al., 2011a). Experiments show that hypoxia generally and Simpson, 2011). increases vegetative growth for C3 plants, but not for C4 plants, and it Increased atmospheric CO2 concentrations across the PTB would decreases seed growth. also have had effects in surface waters (Fraiser and Bottjer, 2007).

Such observations on the physiology of modern organisms have Passive diffusion of atmospheric CO2 into ocean-surface waters would been applied to the PTB and Early Triassic. The response of many ter- have decreased the pH and CaCO3 saturation state of seawater, causing restrial animals to PTB hypoxia was presumably extinction combined a physiological and biocalcification crisis for many marine inverte- with range contraction for the survivors. Huey and Ward (2005) note brates. These deleterious effects may have lasted for much of the Early that a reduction of the atmospheric oxygen concentration to 16% is Triassic, and so contributed to the delay in biotic recovery. equivalent to changing the atmospheric conditions at sea level to As Knoll et al. (2007) say, the terrestrial record of the EPME is in- those at an altitude of 2.7 km today: lowland animals would have faced complete, but that is not the reason that hypercapnia and acidifica- the extremes of high-altitude life; some could adapt, but many presum- tion were unlikely prime killers of life on land. First, it is not clear ably went extinct. how oceanic anoxia, acidification, or hypercapnia could be trans-

In more detail, Retallack et al. (2003, 2006) suggested that many mitted onto land. Atmospheric O2 and CO2 levels may have of the differences between Permian and Triassic anomodonts were changed, but the questions concern physiological correlates in mod- related to the rapid decline in atmospheric oxygen concentrations. ern organisms. Hypoxia and hypercapnia have severe physiological They noted that Lystrosaurus had a massive barrel-like chest, perhaps effects on modern animals, as noted earlier, but plants can generally in part to accommodate expanded lungs, perhaps a muscular dia- adapt to low atmospheric O2 and high CO2 levels. Land animals phragm to force air in and out of the lungs more speedily, and a pos- would not be affected by the physiological calcification stresses of sible four-chambered heart to improve the efficiency of blood marine animals. Hypoxia and hypercapnia could reduce adult body circulation. These claims are hard to test, and it is not clear in any size in terrestrial animals, and extremes would be fatal for many case that postulated PTB oxygen levels were low enough that they species. would have created a major problem (Engoren, 2004). In addition, it has been noted (Hillenius, 1994) that Late Permian and Triassic syn- 11.4. Global warming as the EPME killer apsids had nasal turbinates, bone laminae within the nasal cavity that substantially increase the area of nasal mucous membranes, ei- Temperature is a primary extrinsic driver of the abundance and ther to improve oxygen uptake, or as a countercurrent heat exchang- distribution of species (Gaston, 2003; Hofmann and Todgham, 2010), er to limit body temperature changes during breathing, or both. These a key reason for current concerns about the likely current and future structures emerged in the Late Permian, and they could relate to the effects of global warming on biodiversity. Biogeographic studies show long-term decline in oxygen levels. numerous examples of major range shifts among plants and animals A further two anatomical changes in anomodonts have proved that have already occurred thanks to the global temperature rise of equivocal, enlargement of the secondary palate and enlargement some 1 °C in the past century (Root et al., 2003; Parmesan, 2006; of internal nostrils, both suggested to improve oxygen uptake in Harley, 2011). Environmental temperature changes affect many plants hypoxic conditions (Retallack et al., 2003, 2006; Ward, 2006). and animals directly because they have narrow physiological tolerance Angielczyk and Walsh (2008) tested whether this was likely, and windows within which they function normally; their response is usual- found mixed results: the raw data certainly showed that Triassic ly local extinction, and migration to a geographic area that retains their anomodonts had significantly larger secondary palates and inter- favoured life conditions. nal nostrils than Permian anomodonts. However, these characters The physiological mechanisms underlying temperature-induced are partially related to body size and phylogenetic relationships, migrations remain unclear (Hofmann and Todgham, 2010). Ecotherms and so their changes provide only weak support for the hypoxia are less able than endotherms to adjust to changes in external environ- scenario. mental temperatures, and so have been most studied with these ques- tions in mind. Forecasting whether a plant or animal can survive a particular change in temperature resulting from global climate change 11.3. Hypercapnia and ocean acidification as the EPME killers depends on both physiology, the ability of an organism to buffer the change physiologically, and behaviour. Fundamental physiological rea- Knoll et al. (1996, 2007) made a strong and convincing case that sons for narrow thermal tolerances in organisms include the thermal the main killing agents in the oceans at the PTB were hypercapnia stability of proteins essential for bodily function, cellular membrane

(excess CO2) associated with acidification, hypoxia, and toxic sul- properties, genomic responses to temperature change, and respiratory phide levels. In particular they noted that marine animals suffered efficiency (Hofmann and Todgham, 2010). very different levels of extinction depending on their need for carbon- Physiological and ecological studies show that the nature and ate ions in constructing their skeletons, and how well physiologically timing of temperature change can be as important as the magnitude buffered they were, in other words, how well they could control their of the change. The timing between extreme high temperature events intracellular pH and maintain respiratory efficiency under elevated is an important determinant of survival, because organisms that have

CO2 levels. Excess CO2 in seawater causes suppression of metabolism, undergone a thermal challenge require time to recover physiologically. disrupts acid–base homeostasis, and impairs calcification through re- For example, some corals can increase their thermal tolerance by duced mineral saturation (Pörtner, 2008). 1–1.5 °C, and this is predicted to reduce their vulnerability to bleaching 1330 M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 events by some 30–50 years (Donner et al., 2007). However, certain skeletons from the Karoo in South Africa. Sedimentological evidence species and growth forms can increase their tolerance more effectively shows lowering of water tables and the onset of drought conditions at than others, and this can lead to major changes in the coral reef ecosys- the same time as the disappearance of the Glossopteris flora and the ap- tem that affects all species. pearance of the new anomodont taxon Lystrosaurus in earliest Triassic The rate of warming is also crucial, and experiments with marine sediments, These authors report several ‘bonebeds’ comprising numer- and terrestrial species show that the upper temperature tolerance ous (±10) jumbled and disarticulated sub-adult Lystrosaurus skeletons, limit decreases substantially when the rate of temperature rise is re- which they interpret as drought-induced aggregations. Animals died in duced (Chown et al., 2009; Peck et al., 2009). It might seem counter- large groups on the periphery of a shrinking waterhole, and subsequent intuitive that more rapid warming allows survival to a higher massive rainfall transported the desiccated bones into shallow depres- temperature, but there are two effects at work, the critical maximum sions along with intraformational sediment debris. It should be noted temperature at which cellular and biochemical processes fail, and the that this is telling, but circumstantial, evidence, and such possible maximum temperature to which a species can become acclimatised drought-associated accumulations of tetrapods are reported also from (Peck et al., 2009). There is a difference between short-term survival theMiddleandLatePermian(e.g.Benton et al., 2012), and are not during a rapid pulse of heating that is not sustained, and unique to the post-EPME time. Perhaps droughts were merely seasonal, acclimatisation to longer-term higher temperatures. During fast and not -round. warming, species can survive at higher temperatures before anaero- Aridity can be a physiological stressor either through elevated bic end-product accumulation overcomes resistance capacity, a pro- temperatures (see Section 11.4) or through reductions in water and cess termed hardening (Hoffmann et al., 2003). At slow rates of desiccation of terrestrial habitats. Desiccation stress dramatically warming, over months or years, and where the upper limits are affects physiology and ecology of modern plants and animals well below the critical oxygen limits, acclimatisation and (Hofmann and Todgham, 2010). Physiological responses to desiccation effects become important. Long-term thermal limits are significantly include mechanisms to retain water or to tolerate dehydration. Further, lower than medium-term survival values (Peck et al., 2009). This behaviour can be a crucial defence for animals, which can move to the suggests that many organisms might survive a very short, but shade or forage at night. acute, episode of global warming (days or weeks at most), but Some of the most desiccation-tolerant organisms are prokaryotes, would succumb if the elevated temperature was maintained for including bacteria and cyanobacteria, and the most desiccation- months or years. tolerant of all are Gram-positive bacteria (García, 2011). Desiccation tol- If temperatures persist at high levels, this can simply be lethal for erance in such simple organisms extends to complete anhydrobiosis, most plants and animals. In C3 plants, photorespiration replaces pho- the near-complete removal of water, defined as water content below −1 tosynthesis at temperatures over 35 °C and few plants can survive 0.1 g H2Og dry mass. The ability of some prokaryotes to survive above 40 °C (Berry and Bjorkman, 1980; Ellis, 2010). Some animals these conditions makes many prokaryotes extremely drought resistant show rather lower lethal temperatures, but for most temperatures for long periods in natural situations; this ability has been exploited in of 40 °C or higher can cause protein damage that can be countered the pharmaceutical and food industries which dry, store, and distribute only for short heat shocks by the production of heat-shock proteins prokaryote lines. (Somero, 1995). Desiccation tolerance in many animals may depend on simple Temperature change has important synergistic effects with other physiological and biochemical mechanisms. Insects have a distinct environmental changes. For example, in experimental studies of ma- critical temperature limit above which water loss increases rapidly, rine organisms, elevated CO2 can reduce the upper thermal limits for presumably related to the biochemistry of their cuticle. Gibbs (2002) species, and exacerbate the effects of low pH on lowering metabolic proposed a lipid-melting model that links this critical temperature to rate (Hofmann and Todgham, 2010). Likewise, low pH (= acidifica- the lipid phase state and cuticular permeability: at a certain tempera- tion) can affect the ability of organisms to survive elevated temper- ture the lipid bonds fail and resistance to water loss is compromised. atures in echinoderm larvae, coralline algae, and corals (Reynaud et Birds show a similar strategy, in which cutaneous water loss may be al., 2003). Such findings are made also in longer-term ecological primarily mediated through changes in the lipid composition of the studies: for example, Cooper et al. (2008) found that synergistic stratum corneum, the outermost layer of the skin (Muñoz-Garcia and stressors were linked to a decline in calcification in corals of the Williams, 2008). Great Barrier Reef in a 16-year field study. These synergistic effects For many species, the critical desiccation level is lower than mean that the lethal temperature for most animals is 35 °C that associated with the lipid failure temperature. Desiccation (Somero, 1995), because oxygen demand increases with tempera- resistance has a high heritability in some Drosophila species ture (Pörtner, 2001, 2008). This causes hypoxaemia and the onset (Hofmann and Todgham, 2010). For example, it has been shown of anaerobic mitochondrial metabolism that is only sustainable for that invasive North American populations of Drosophila subobscura short periods. have evolved desiccation resistance within the past 30 years, and As for the EPME, a global mean rise of 5–10 °C would clearly have the more arid populations have a higher desiccation tolerance. caused severe heat stress for many terrestrial plants and animals, but This is not the case, however, for all Drosophila species, many of it is unclear how high the species extinction levels would have been. which are apparently desiccation-intolerant, and so more vulnerable If ocean surface, and presumably also land surface, temperatures rose to climate change. to 35° or more (Joachimski et al., 2012; Sun et al., 2012), then this Very few animals are truly tolerant of desiccation. The exceptions could have proved lethal to many plants and animals. Terrestrial ver- are brine shrimp, , rotifers, and some insects. The brine tebrates at least are largely absent from equatorial latitudes during shrimp Artemia franciscana can produce larvae or embryonic cysts the Early Triassic (Shishkin and Ochev, 1993; Sun et al., 2012). If from its fertilised eggs, and these cysts can survive for 2 years in dry equatorial temperatures reached 35°, then most plants and animals conditions, without oxygen, or even at temperatures below freezing would have been unable to survive, and they would have been driven or up to 80 °C (Clegg, 2005). In this species, the outermost envelope entirely from these regions. of the cyst is essential for its remarkable tolerance to stress. Tardigrades, a phylum related to arthropods, are able to survive in extreme environ- 11.5. Aridity as the EPME killer ments, including temperatures close to absolute zero and as high as 151 °C, massive doses of radiation, and spans of up to 10 years without As evidence for the direct effects of aridity at the time of the EPME, water (Wright, 1989). Tardigrades have even survived the vacuum of Smith and Botha (2005) described drought associations of tetrapod outer space for a few days in low earth orbit. Different species of M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 1331 tardigrades show different degrees of desiccation tolerance, with some 300 species of angiosperms that can survive extreme drying lower lethal humidities for initial desiccation ranging from 78 to through special adaptations of their cell membranes and macromole- 53%. Tardigrades resist desiccation by shrinking, infolding their cuti- cules, especially the production of large amounts of desiccation- cle, and reducing transpiration, forming an inert cyst, or tun. The re- induced protective proteins. These have different roles in cellular duction in transpiration causes a slump in permeability of the protection, by conserving the structures of macromolecules and cuticle, and so water can be retained despite overall desiccation membranes, by stabilising membrane structures and proteins, by (Wright, 1989; Guidetti et al., 2011). Rotifers, a phylum of small avoiding mechanical damage from vacuole shrinkage in dehydrating (b2 mm) aquatic animals, include forms that live in temporary cells, and by minimising oxidative stress from the enhanced produc- freshwater pools or terrestrial mosses or lichens, and when these tion of reactive oxygen. These resurrection plants can survive for habitats dry up they can alter their morphology and physiology, as- months or years without water, and then regrow at full vigour suming a compact shape also called a ‘tun’ (dormant stage) and en- when watered (P. Scott, 2000). Survival for more than a few years tering a dormant state (Robles-Vargas and Snell, 2010). Rotifers can however is not possible. survive whole annual cycles or drought, and the longest reported Evidently, drought is a key problem for terrestrial life. As de- survival is 9 years. They then recover in minutes or hours when ex- scribed, a wide range of plants and animals can tolerate complete des- posed to water. iccation. Species in five phyla of animals and four divisions of plants Insects do not generally show such extremes of desiccation toler- contain desiccation-tolerant adults, juveniles, seeds, or spores, and ance, but most taxa have adaptations to avoid water loss, such as an im- some of these, as indicated, can survive for years or even decades. Im- permeable cuticle with waxy components, tracheae with spiracles that portantly, there may be physiological limits in these drought-tolerant can close, and limiting water excretion. Many of these conditions organisms, restricting the ability to small organisms (plants shorter change in dormant insects, which can combine several adaptations to than 3 m; animals shorter than 5 mm), and to animals with rigid maintain water balance, including habitat choice, reduction of body skeletons (Alpert, 2005, 2006). Many desiccation-tolerant organisms water content, decreased cuticular permeability, absorption of water share biochemical and cellular mechanisms, such as sugars that re- vapour, and tolerance of low body water levels (Danks, 2000). The place water and form glasses, proteins that stabilise macromolecules chironomid midge Polypedilum vanderplanki is the largest multicellular and membranes, and anti-oxidants that counter damage by reactive animal known to tolerate almost complete dehydration without ill ef- oxygen species (Alpert, 2006). These systems are often triggered by fect. Its larvae show extremely high thermal tolerance from −270 °C drying, and some of the genes involved may be homologous in to +106 °C and can recover soon after prolonged dehydration of up microbes, plants, and animals (Leprince and Buitink, 2010). If desicca- to 17 years. Part of the explanation seems to involve the rapid accumu- tion resulting from elevated temperatures were one of the EPME lation of the carbohydrate trehalose and yet that cerebral regulation is killers on land, the likely survivors and victims could be predicted not involved (Watanabe et al., 2002). from the observations just outlined of desiccation tolerance in mod- Plants are often thought to be more tolerant of desiccation than ern organisms. animals (Hoekstra et al., 2001). The ability to survive desiccation is common in seeds or pollen, it occurs in terrestrial microalgae, 11.6. Acid rain and mass wasting as the EPME killers fungi,andyeasts,anditiswidespreadamongbryophytes,butitis rarely present in the vegetative tissues of other plants. Seeds com- As argued above (Sections 2, 6.1, 6.2, 6.4 and 7.2), the apparent monly survive for 5 or 10 years, and there are several credible re- removal of vegetation from the land surface following acid rain at the cords of survival for more than 200 years (Daws et al., 2007). Over EPME probably significantly increased weathering processes and ter- time, the viability of such long-stored seeds reduces substantially, restrial nutrient fluxes, and these then had a major impact on marine and the main causes of eventual death relate to water loss. Desicca- environmental conditions (Algeo et al., 2011). Widespread loss of plants tion tolerance in seeds (Leprince et al., 1993) is enabled by mecha- led to massive erosion on land areas at the time of the EPME, as shown nisms that prevent lethal damage to cellular components including by the shift from fine-grained meandering to conglomeratic braided membranes, proteins and cytoplasm. There are three main protec- fluvial facies (Newell et al., 1999; Ward et al., 2000; Michaelsen, 2002; tive systems: the accumulation of non-reducing sugars, which stabi- López-Gómez et al., 2005), by transported soil clasts (pedoliths; lise membranes and proteins in dry conditions and promote the Retallack, 2005), by increased sedimentation rates in terrestrial succes- formation of a glass phase in the cytoplasm; the ability to prevent, sions (Retallack, 1999), and by an abrupt influx of terrigenous tolerate, or repair a free radical attack during desiccation; and, pro- siliciclastics to carbonate platforms nearly worldwide (Algeo and tective late embryogenesis abundant proteins that are inducible by Twitchett, 2010). Continuing episodic massive erosion events through abscissic acid. the Early Triassic may have further repeated aspects of the EPME crisis Extreme survivors of desiccation are bryophytes (mosses and (Algeo et al., 2011). liverworts); as an example, a dried herbarium specimen was reported The sudden influxes of sediment may have killed filter-feeding to have regrown after 23 years of storage in entirely dry conditions marine organisms by swamping them and reducing their feeding ac- (Proctor and Pence, 2002). This remarkable desiccation tolerance by tivity, osmoregulation, growth rate, body size, larval recruitment, and bryophytes (Proctor et al., 2007) depends on their unique physiology, development (Algeo and Twitchett, 2010). Grazers could have been which differs from that of vascular plants: they are smaller, their leafy affected also if the masses of fine-grained sediment covered their shoots equilibrate rapidly with the water potential in their surround- food sources. Algeo et al. (2011) noted that many of the immediate ings, and the shoots tend to be either fully hydrated or desiccated and survivors of the EPME in shallow seas, such as the paper pectens, metabolically inactive. The length of desiccation affects the time to re- were adapted to living on unstable, soft sediments. Continuing in- cover and the degree of that recovery; both also depend on tempera- fluxes of sediment through the first few Myr of the Triassic may ture and the intensity of desiccation. The recovery of respiration, have had a major, previously under-emphasised role in disturbing and protein synthesis takes place within minutes or marine benthic communities (Algeo et al., 2011). hours; recovery of the cell cycle, food transport and the cytoskeleton On land, acid rain removed forests and soils, both of which are may take a day or more. massive repositories of biodiversity (Lindenmeyer and Franklin, Such feats of survival are extremely rare among pteridophytes and 2002; Nielsen et al., 2011). It is impossible to estimate how impor- angiosperms, so much so that the 350 or so species that can survive tant these two broad habitats are, but they likely account for the desiccation are set apart as ‘resurrection plants’ (P. Scott, 2000; largemajorityoflifeonland,whenoneconsiderstheremarkable Proctor and Pence, 2002; Bartels and Hussain, 2011). These include dominance of species inventories by insects today (perhaps 70– 1332 M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337

80%), and especially tropical forest insects, coupled with the high maintaining biodiversity at several different scales, by altering species diversities of other terrestrial arthropods (spiders, mites) and diversity, landscape diversity and dynamics, and ecosystem function. flowering plants in those habitats (Briggs, 1995). The current very Fires act as a disturbance, preventing species of late successional high biodiversity on land compared to the sea is a phenomenon stages from excluding those of earlier stages. Individual fires can of the past 125 Myr or so, and terrestrial biodiversity in the therefore increase biodiversity by preventing any single species Permo-Triassic was surely much lower than today (Vermeij and from dominating. However, when fires are too frequent, total biodi- Grosberg, 2010), and yet the loss of forests and soils during the versity can be reduced as vulnerable species are removed. Fires may EPME would have removed the habitats of considerably more than affect biodiversity at larger scales by, for example, creating patchy 50% of land life. landscapes, as well as altering nutrient cycling, successional processes, Acid rain affects both the living plants and the soil, and effects can and stand composition. be long term. From a selection of 13 environmental variables, Dietze Large fires can be a normal part of ecosystem functioning. In and Moorcroft (2011) found that the clearest determinants of forest Australia, perhaps the most fire-affected continent, large proportions decline in the eastern and central United States were air pollutants of the northern tropical savanna landscapes are burnt (Andersen et al., (acid rain, nitrogen deposition, ozone) and stand characteristics (forest 2005). Much of the savanna biota is remarkably resilient to fire, even size, tree mean age, tree mean size). of high intensity. The relative abundances of plants and animals are These effects are widely studied in modern ecosystems affected generally unaffected by fire, except for riverbank plants and animals, by industrial acid rain. For example, in North America, forest soil and small mammals. The 2-yearly managed burning appears to be too acidification and depletion of nutrient cations have been reported frequent for these species, and small mammals have undergone signif- for several forested regions (Fenn et al., 2006). Continuing inputs icant declines. Overall, Andersen et al. (2005) conclude that ‘although of anthropogenic sulphur dioxide, together with ozone and nitrogen individually massively destructive, it is hard to make a case that fires oxides (Schulze et al., 1989), lead to leaching of base cations (Ca, Mg, have a substantial long-term effect on biodiversity. In many ecosystems, K), increased availability of soil Al, and the accumulation and trans- fire is a vital and natural part of some forest ecosystems, and humans mission of acidity from forest soils to streams. More subtle changes have used fire for thousands of years as a land management tool.’ in soil acidity affect the ion balance and, in depleted soils, the trees Moretti et al. (2002) obtained similar results in their study of winter are affected immediately. The key is the balance of Ca and Al ions forest fires in the southern Alps. They found that overall species richness in forest soils: Ca is an essential plant nutrient, contributing to was significantly higher in plots with repeated firesthaninunburnt many cellular structures and physiological processes as well as control sites. The frequency of fires increased the richness of species overall forest function. Al in soil solution can inhibit Ca uptake by that live deep within forests and at forest edges, but species of open plants and disrupt these Ca-dependent metabolic and physiological landscapes, open forests and interior forests were not influenced by processes. The ratio of Ca to Al in soil solution can be an important fire frequency. A positive effect of fire was found for most subclades of indicator of forest health, especially in acid soils, and Ca loss points insects and spiders, with negative effects only for isopods and weevils. to acidification. Further, Moretti et al. (2006) noted that terrestrial arthropods were Calcium reduction has profound effects on trees. Movement of more resilient to single fires than to repeated events, recovering labile Ca among cellular compartments acts as a signal mediating 6–14 years after a single fire, but only 17–24 years after the last of physiological responses to environmental stresses such as drought, several fires. Flying arthropods proved to be most resilient to fire, cold, heat, salinity, fungal pathogens, and oxidative and mechanical then pollen-feeders and foragers, and with ground-litter scavengers stresses (Knight, 2000). Ca deficiency may then affect the ability of least able to recover following major fires. plants to sense and respond adaptively to their environment. Further, Ca is essential to the photosystem function and carbohydrate metabo- 12. Death on land during the EPME lism of plants: shortage of Ca reduces the storage of sugars, and reduces the cold tolerance of leaves. Exposure to acid rain reduces red spruce Whereas key killing agents of marine life during the EPME were cold tolerance through a reduction in Ca availability, thereby increasing likely hypercapnia, ocean acidification, hypoxia, and high sulphide the risk of winter injury and crown deterioration (DeHayes et al., 1999). levels (Knoll et al., 2007), it is unlikely that this cocktail of killers Further, shortage of Ca impairs the function of the leaf stomata, essential acted so substantially on land life. The immediate burst of wildfires for correct water balance (Borer et al., 2005). In addition, reduced Ca would have killed plants, but whether irrevocably is less clear. The affects seed germination and seedling growth, all combining to confirm significance of hypoxia is also unclear, in that atmospheric oxygen that acid rain can cause immediate leaf loss in trees, and ultimately levels had been falling throughout the Permian, and the Triassic death. lows may not have been as low as suggested by models (Glasspool and Scott, 2010). Further, although hypoxia and hypercapnia would 11.7. Wildfires as the EPME killer have had a major impact on vertebrates, some other animal groups might have suffered less, and microbes and plants presumably not The evidence for extensive wildfires in the Late Permian, and a at all. At times, the postulated destruction of the ozone layer and burst of wildfires coincident with the EPME has been described enhanced UV-B radiation have been cited as the major cause of above (Sections 6.1 and 6.3). It is unclear, however, whether wildfire extinction on land (Beerling, 2007), but evidence for these dramatic could be considered a major contributor to the species loss experi- environmental perturbations is currently mixed (see Section 7.4). enced at the EPME. The wildfires associated with the EPME, and There were three scales of potential physical drivers of extinction other mass extinctions, such as that at the end of the Cretaceous, around the time of the EPME: long-term, short-term, and repeated. were triggered by the eruptions or impacts. However, wildfires have One long-term process was continuing aridification through the Late been common throughout geological time (A.C. Scott, 2000; Bowman Permian and Early Triassic. Short-term consequences of the initial et al., 2009), and yet most are not associated with any global extinction. major eruption of the Siberian Traps may have been flash warming, The frequency of fires in Earth history correlates with oxygen levels wildfires, acid rain and mass wasting, and breaching of the ozone (Bowman et al., 2009). layer at high latitudes. Some of these short-term processes may have Fire is a key ecosystem driver in grasslands, savannas, boreal been repeated during subsequent Early Triassic crises, but this has yet forests, and heathlands. Historical records, sedimentary successions, to be established. There is evidence for repeated phases of input of and dendrochronology show that wildfires have recurred with fre- siliciclastic debris into the sea through the Early Triassic, so suggesting quencies from years to decades. Fire is an important agent for repeated episodes of acid rain (Algeo and Twitchett, 2010). M.J. Benton, A.J. Newell / Gondwana Research 25 (2014) 1308–1337 1333

Global warming at the time of the EPME presumably increased Beerling, D.J., 2007. The Emerald Planet: How Plants Changed Earth History. Oxford University Press, Oxford (312pp.). stress on much of land life, and may have driven many plants and Beerling, D.J., Harfoot, M., Lomax, B., Pyle, J.A., 2007. The stability of the stratospheric animals from the tropical belt. However, it is currently hard to esti- ozone layer during the end-Permian eruption of the Siberian Traps. Philosophical mate the global killing effects of such high, even lethal, equatorial Transactions of the Royal Society, Series A 365, 1843–1866. Belcher, C.M., McElwain, J.C., 2008. Limits on combustion in low O2 redefine temperatures on land because many species could presumably palaeoatmospheric levels for the Mesozoic. Science 321, 1197–1200. have migrated to cooler climes. 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We are very grateful to Zhong Qiang Chen for the invitation to the Preservation of exceptional vertebrate assemblages in Middle Permian fluviolacustrine mudstones of Kotel'nich, Russia: stratigraphy, sedimentology, and . IGCP572 Symposium 3: Latest Permian Mass Extinction and IGCP572 Palaeogeography, Palaeoclimatology, Palaeoecology 319–320, 58–83. Symposium 4: Ecosystem Recovery in Triassic, jointly held with the Benton, M.J., Ruta, M., Dunhill, A.M., in press. The first half of tetrapod evolution, sampling XVII International Congress on the Carboniferous and Permian, from 3 proxies, and fossil record quality. Palaeogeography, Palaeoclimatology, Palaeoecology. http://dx.doi.org/10.1016/j.palaeo.2012.09.005 [Electronic publication ahead of to 8 July, 2011, in Perth, Australia, and for funding for M.J.B. to attend. print]. We are grateful to Thomas Algeo (University of Cincinnati), Zhong Berner, R.A., 2002. 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Proceedings of the National Academy of Sciences at the University of Bristol, U.K. He received his undergradu- of the United States of America 101, 12952–12956. ate training in Zoology at the University of Aberdeen, and Wang, C.J., Visscher, H., 2007. Abundance anomalies of aromatic biomarkers in the Permian– his PhD in Geology from the University of Newcastle-upon- Triassic boundary section at Meishan, China—evidence of end-Permian terrestrial Tyne. He had positions at the University of Oxford, and ecosystem collapse. Palaeogeography, Palaeoclimatology, Palaeoecology 252, 291–303. Queen's University of Belfast, before moving to the University Ward, P.D., 2006. Out of Thin Air: Dinosaurs, Birds, And Earth's Ancient Atmosphere. of Bristol in 1989. He has always been interested in the John Henry Press, Eashington, DC (282 pp.). Triassic, and made early contributions to the understanding Ward, P.D., Montgomery, D.R., Smith, R., 2000. Altered river morphology in South Africa of the origin of dinosaurs. More recently he has been work- related to the Permian–Triassic extinction. Science 289, 1740–1743. ing on the Permo-Triassic boundary in Russia, and the time Ward, P.D., Retallack, G.J., Smith, R.M.H., 2012. The terrestrial Permian–Triassic boundary of recovery from the end-Permian mass extinction in the event bed is a nonevent: comment. Geology 40, e256. marine successions of South China. Warren, J.K., 2006. Evaporites: Sediments, Resources and Hydrocarbons. Springer, Heidelberg (1036 pp.). Warren, J.K., 2010. Evaporites through time: tectonic, climatic and eustatic controls in marine and nonmarine deposits. Earth-Science Reviews 98, 217–268. Andrew J. Newell is a Senior Geologist at the British Watanabe, M., Kikawada, T., Minagawa, N., Yukuhiro, F., Okuda, T., 2002. Mechanism Geological Survey. Wallingford, U.K. He received his allowing an insect to survive complete dehydration and extreme temperatures. undergraduate training and his PhD in Geology at the The Journal of Experimental Biology 205, 2799–2802. Queen's University of Belfast. His PhD research was on the Wignall, P.B., 2001. Large igneous provinces and mass extinctions. Earth-Science sedimentology of the Otter Sandstone Formation of Devon, Reviews 53, 1–33. and he has gone on to specialise in clastic sedimentology, Wignall, P.B., 2007. The end-Permian mass extinction — how bad did it get? Geobiology stratigraphy, and 3D geological modelling. He has done field- 5, 303–309. work all round the world, including in the classic Permo- Wignall, P.B., 2008. The end-Permian crisis, aftermath and subsequent recovery. In: Triassic red bed successions in Russia. His particular interests Okada, H., Mawatari, S.F., Suzuki, N., Gautam, P. (Eds.), Origin and Evolution of in this field are to understand the successions of sedimentary Natural Diversity. 21st Century for Neo-Science of Natural History. Hokkaido facies in different redbed basins, their stratigraphy, and the University, Hokkaido, pp. 43–48. information they provide on ancient palaeoclimates. Wignall, P.B., Twitchett, R.J., 1996. Oceanic anoxia and the end Permian mass extinction. Science 272, 1155–1158.