Lethally Hot Temperatures During the Early Triassic Greenhouse

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Science  19 Oct 2012:
Vol. 338, Issue 6105, pp. 366-370
DOI: 10.1126/science.1224126


Global warming is widely regarded to have played a contributing role in numerous past biotic crises. Here, we show that the end-Permian mass extinction coincided with a rapid temperature rise to exceptionally high values in the Early Triassic that were inimical to life in equatorial latitudes and suppressed ecosystem recovery. This was manifested in the loss of calcareous algae, the near-absence of fish in equatorial Tethys, and the dominance of small taxa of invertebrates during the thermal maxima. High temperatures drove most Early Triassic plants and animals out of equatorial terrestrial ecosystems and probably were a major cause of the end-Smithian crisis.

Anthropogenic global warming likely is contributing to the rapid loss of biological diversity currently occurring (1). Climate warming also has been implicated in severe biotic crises in the geological past, but only as a corollary to more direct causes of death such as the spread of marine anoxia (2). Here, we show that lethally hot temperatures exerted a direct control on extinction and recovery during and in the aftermath of the end-Permian mass extinction. As well as the scale of the losses, the aftermath of this event is remarkable for several reasons, such as the prolonged delay in recovery (3), the prevalence of small taxa (4), and the absence of coal deposits throughout the Early Triassic (5). These and several facets of low-latitude fossil records shown below, including fish, marine reptile, and tetrapod distributions, can be related to extreme temperatures in excess of tolerable thermal thresholds.

Climate warming long has been implicated as one cause of the end-Permian crisis (2, 6), with carbon dioxide release from Siberian eruptions and related processes providing a potential trigger for it (7, 8). Conodont apatite oxygen isotope ratio (δ18O) is a reliable proxy for paleoseawater temperatures (9), and conodonts suffered few genus-level losses at the end of the Permian (10), allowing continuous sampling of the same genera over multimillion-year intervals (11). We used δ18Oapatite of conodonts from sections in the Nanpanjiang Basin, South China, to reconstruct Late Permian to Middle Triassic equatorial seawater temperatures (Fig. 1 and supplementary text 1). Our main record, measured on the genus Neospathodus, is a monitor of upper water column temperatures (estimated ~70 m water depth, supplementary text 2), whereas data from extremely shallow water taxa (Pachycladina or Parachirognathus spp., Platyvillosus spp.) provide sea surface temperatures (SSTs).

Fig. 1

Early Triassic paleogeography showing reported occurrences of fish and marine reptiles in the Smithian. Note rare equatorial occurrence of both groups when ichthyosaurs had evolved in northern climes. The global distribution of tetrapods (25) indicates occurrences almost exclusively in higher latitudes (>30°N and >40°S) throughout the Early Triassic, with rare exceptions in Utah (Parotosuchus sp., paleolatitude ~10°N) and Poland (paleolatitude ~20°N), both probably of middle-late Spathian age (25, 26). (Inset) Paleogeography of Pangea and Nanpanjiang Basin after (4547). Fish and ichthyosaurs occurrences, see table S2. GBG, Great Bank of Guizhou.

Our results show large, near-synchronous perturbations in both carbon isotope ratios (δ13Ccarb) and δ18Oapatite with three positive excursions observed in the Dienerian [~251.5 million years ago (Ma)], early Spathian (~250.5 Ma), and at the Spathian-Anisian (Early-Middle Triassic) transition (~247.5 Ma). The minima in δ13Ccarb and δ18Oapatite are measured in the Griesbachian (~252.1 Ma) and the Smithian-Spathian transition (~250.7 Ma) (Fig. 2). The δ18Oapatite values of the analyzed conodonts taxa accord with their habitats in different water depth: Neospathodus spp. shows ~0.7 per mil (‰) heavier values than those from shallow-water Pachycladina/Parachirognathus spp. and Platyvillosus spp. Deeper-water gondolellids show even heavier δ18Oapatite (~0.4‰) than Neospathodus spp. (supplementary text 2 and table S1). Latest Spathian–early Anisian oxygen isotope data from Bianyang and Guandao are more scattered and up to 1.3‰ heavier compared with samples from other sections. These two locations are close to the Great Bank of Guizhou (Fig. 1), and such 18O enrichment toward platform interior is interpreted to be due to evaporation as seen on the modern Bahama Bank (12). However, most of the presented data are from distal, open-water environments and therefore present a faithful paleotemperature record (supplementary texts 3 and 4).

Fig. 2

Oxygen isotopes of conodont apatite and carbon isotopes of carbonates from the Nanpanjiang Basin. Oxygen isotopes show two thermal maxima in the late Griesbachian and late Smithian. Scanning electron microscope investigation of conodont surfaces shows microreticulation and no sign of recrystallization (supplementary text 3). Absolute age constraints are given in supplementary text 9; data for Meishan and Shangsi sections compiled from (9); leaf icons represent marine and terrestrial C3 plants (14). Modern equatorial SST ranges (annual mean) from (48). The error bar stands for external reproducibility of δ18Oapatite measurements (2σ). The black trendline represents smoothed δ18Oapatite fluctuations estimated from the upper water column taxa. Note uncertainty of correlating conodont zones with absolute ages. Aeg., Aegean; Bith., Bithynian. Conodont zonations: 1, Ng. changxingensis; 2, Ng. yini; 3, Ng. meishanensis; 4, H. changxingensis; 5, H. parvus; 6, Is. staeschei; 7, Is. isarcica; 8, Ng. planata; for genera abbreviations, see table S4.VSMOW, Vienna Standard Mean Ocean Water; VPDB, Vienna Pee Dee Belemnite.

Calculation of seawater temperatures from δ18O values (supplementary text 5) reveals rapid warming across the Permian-Triassic boundary [21° to 36°C, over ~0.8 million years (My); (9)], reaching a temperature maximum within the Griesbachian (~252.1 Ma) followed by cooling in the Dienerian. A second rise to high temperatures is seen in the late Smithian (~250.7 Ma), followed by relatively stable temperatures in the Spathian, cooling at the end of this stage and stabilization in the early Middle Triassic (Fig. 2). The late Smithian Thermal Maximum (LSTM) marks the hottest interval of entire Early Triassic, when upper water column temperatures approached 38°C with SSTs possibly exceeding 40°C (Fig. 3).

Fig. 3

Early Triassic diversity of major marine groups and temperature trends showing inverse relationship: Peak diversity corresponds to cool climate conditions around the Dienerian-Smithian boundary, early Spathian, and early Anisian (named cooling events I to III), whereas low diversity in Griesbachian and Smithian correlates with peak temperatures. Diversity of marine groups from (3739, 4952); fish and marine reptile only show the general presence of taxa; no quantitative diversity data are available (supplementary text 6). Floral data (2830, 42) show the loss of equatorial conifer-dominated forests above the Permian-Triassic (PT) boundary, with the earlier reappearance of this forest type at high latitudes. Gray band represents the first-order seawater temperatures trend (upper water column, ~70-m water depth) estimated by this study; red trend line represents possible SST derived from shallow water taxa. Same stratigraphic scheme as Fig. 2.

The entire Early Triassic record shows temperatures consistently in excess of modern equatorial annual SSTs. These results suggest that equatorial temperatures may have exceeded a tolerable threshold both in the oceans and on land. For C3 plants, photorespiration predominates over photosynthesis at temperatures in excess of 35°C (13), and few plants can survive temperatures persistently above 40°C (14). Similarly, for animals, temperatures in excess of 45°C cause protein damage that are only temporarily alleviated by heat-shock protein production (15). However, for most marine animals, the critical temperature is much lower, because metabolic oxygen demand increases with temperature while dissolved oxygen decreases (16). This causes hypoxaemia and the onset of anaerobic mitochondrial metabolism that is only sustainable for short periods (17). As a consequence, marine animals cannot long survive temperatures above 35°C, particularly those with a high performance and high oxygen demand, such as cephalopods (16).

Extreme equatorial warmth should have left a distinct signature in the Early Triassic fossil records, a proposition that we examine here. The fossil fish record is exceptionally good in the Early Triassic, with many well-preserved faunas known from locations such as Madagascar, Greenland, and British Columbia (supplementary text 6). This is related to the widespread distribution of anoxic facies (18) that provide excellent preservational conditions for such fossils. However, our compilation of fish occurrences reveals that they are very rare in equatorial locales, especially during the late Griesbachian and the Smithian, despite being common at higher latitudes at these times (fig. S1 and table S2). This rarity is extraordinary because Early Triassic units, such as the dysoxic-anoxic Daye Formation of South China, are widespread (supplementary text 7) and yet do not yield a fossil fish fauna. The general absence of ichthyofauna in equatorial regions coincides with the temperature maxima reconstructed from the δ18Oapatite record, and we interpret this coincidence as recording equatorial exclusion because of inhospitably high temperatures. In contrast, invertebrates remain common in these intervals (19), especially sessile mollusks with their better adapted oxyconforming metabolism allowing them to cope with synergistic stresses of high temperature and low oxygen (17, 20). Like fish, marine reptiles also exhibit high aerobic activity and are likely to have had a relatively low oxygen-limited thermal tolerance. Examining Early Triassic marine reptile (ichthyosaur) occurrences reveals that they too are not found in equatorial waters until the middle-late Spathian (supplementary text 6), ~1 to 2 My after their first appearance in higher latitudes during the Smithian (21, 22). Other notable absences from equatorial oceans are calcareous algae, whose outage spans the entire end-Permian–early Spathian interval although they are present in higher latitudes [e.g., Spitsbergen, (23)]. Their equatorial absence (supplementary text 8) likely reflects inhibiting temperatures, whereas the abundance of calcimicrobial carbonates in shelf waters, one of the stand-out features of the Early Triassic (24), was possible because of the much higher temperature tolerance of cyanobacterial photosynthesis (16).

Critically high temperatures may also have excluded terrestrial animal life from equatorial Pangea, and with SSTs approaching 40°C the land temperatures are likely to have fluctuated to even higher levels. Our compilation of tetrapod fossil occurrences reveals them to be generally absent between 30°N and 40°S in the Early Triassic (Fig. 1), with rare exceptions (25, 26); this is a stark contrast to Middle and Late Triassic occurrences, when they occur at all latitudes (fig. S1). This equatorial “tetrapod gap” does not reflect an absence of suitable strata for their preservation. For example, the Buntsandstein of Europe is one of the best known and most intensively investigated terrestrial formations of the Early Triassic; tetrapods are exceptionally rare in the lower part (Induan) and only become common in middle and upper units (late Early Triassic to Middle Triassic) (27). The tetrapod gap of equatorial Pangea coincides with an end-Permian to Middle Triassic global “coal gap” that indicates the loss of peat swamps (5). Peat formation, a product of high plant productivity, was only reestablished in the Anisian and then only in high southern latitudes (5), although gymnosperm forests appeared earlier (in the Early Spathian), but again only in northern and southern higher latitudes (28, 29). In equatorial Pangea, the establishment of conifer-dominated forests was not until the end of the Spathian (30), and the first coals at these latitudes did not appear until the Carnian ~15 My after their end-Permian disappearance (5). These signals suggest equatorial temperatures exceeded the thermal tolerance for many marine vertebrates at least during two thermal maxima, whereas terrestrial equatorial temperatures were sufficiently severe to suppress plant and animal abundance during most of the Early Triassic.

Thermal tolerance is likely to decrease for organisms with larger body sizes (31). Nonlethal effects of temperature increase include smaller adult size, which, in conjunction with increased juvenile mortality at higher temperatures (32, 33), will produce a fossil record dominated by small individuals. This is a well-known phenomenon in the Early Triassic marine fossil record and has been termed the Lilliput effect (4). We suggest that this effect is a response to high temperatures and that it should be most clearly seen in equatorial assemblages, especially during the Griesbachian and Smithian thermal maxima. This prediction is confirmed by data from equatorial marine fossils where small body and trace fossil assemblages are confined to these intervals (34, 35). Low oxygen levels also are known to cause small size in marine invertebrates (36), but, although marine dysoxia was a global phenomenon in the Early Triassic (18), the restriction of the Lilliput effect to equatorial latitudes indicates that this was primarily a temperature-controlled phenomenon.

The relation between global warming and extinction can be examined in the Early Triassic. The rapid temperature rise across the Permian-Triassic boundary coincides with mass extinction, although absolute temperatures at the time of crisis were only modest [< 30°C (9)]. Together with temperature rise, synergistic factors, such as spread of anoxia, may also play important roles in marine extinction (2, 18). However, the subsequent loss of many Permian holdover taxa later in the Griesbachian (conodonts, radiolarian, and brachiopods) may reflect lethal temperatures followed by temporary recovery and radiation in the cooler Dienerian (Fig. 3). The clearest temperature-extinction link is with the LSTM and the end-Smithian event that saw major losses among many marine groups, including bivalves, conodonts, and ammonoids (3739). Contemporaneous losses among tetrapods on land (25) suggest that this was a crisis that affected a broad diversity of ecosystems.

The ultimate driving factor behind the end-Permian warming long has been attributed to greenhouse gas emissions, either from volcanogenic (8) or thermogenic sources (40). Both are expected to leave a negative excursion in the δ13C record, and this is the case for both the end Permian–Griesbachian and Smithian intervals (Fig. 2), although it has yet to be demonstrated that a second pulse of Siberian volcanism occurred in the Smithian. However, to maintain high temperatures for the ~5 My of the Early Triassic requires strong, persistent greenhouse conditions. High temperatures also could greatly enhance the activity of decomposers (e.g., fungi and bacteria), resulting in the release of large amounts of terrestrial light carbon into the atmosphere (41) and consequently forming oligotrophic, humus-poor soils as observed in modern Amazon rainforests and in Early Triassic soils of Australia and Antarctica (42). Together with global suspension of peat formation, elevated decomposition rates may have led to a significant reduction in organic carbon burial on land further contributing to higher atmospheric CO2 levels (43).

High and oscillating temperatures in the Early Triassic likely controlled the pace and nature of recovery in the aftermath of the end-Permian mass extinction as shown by an inverse relationship between the temperature and biodiversity changes, the temporary loss of both marine and terrestrial vertebrates, and the reduced size of the remaining invertebrates. SSTs derived from δ18O data offer no evidence that a climate thermostat may ameliorate tropical warming by redistributing warmth to the poles (44). Rather, extreme global warming may progressively force taxa to vacate the tropics and move to higher latitudes or become extinct. Marine organisms exhibiting low oxygen-dependent thermal tolerance, such as vertebrates, are the first to leave.

Supplementary Materials

Materials and Methods

Supplementary Text

Fig. S1

Tables S1 to S4

References (53150)

References and Notes

  1. Information on materials and methods is available on Science Online.
  2. Acknowledgments: D. Lutz, F. Nenning, B. Yang, and X. Liu are acknowledged for lab and field assistance. This study was supported by Chinese 973 Program (2011CB808800) and the Natural Science Foundation of China (41172024 and 40830212). Y.S. acknowledges China University of Geosciences and China Scholarship Council for split-site Ph.D. at Wuhan, Leeds, and Erlangen.
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