Abstract During the past 600 million years of Earth history, four of five major extinction events were synchronous with volcanism in large igneous provinces. Despite improved temporal frameworks for these events, the mechanisms causing extinctions remain unclear. Volcanic emissions of greenhouse gases, SO 2 , and halocarbons are generally considered as major factors in the biotic crises, resulting in global warming, acid deposition, and ozone layer depletion. Here, we show that pulsed elevated concentrations of mercury in marine and terrestrial sediments across the Triassic-Jurassic boundary in southern Scandinavia and northern Germany correlate with intense volcanic activity in the Central Atlantic Magmatic Province. The increased levels of mercury—the most genotoxic element on Earth—also correlate with high occurrences of abnormal fern spores, indicating severe environmental stress and genetic disturbance in the parent plants. We conclude that this offers compelling evidence that emissions of toxic volcanogenic substances contributed to the end-Triassic biotic crisis.

INTRODUCTION The end-Triassic mass extinction at 201.51 million years (Ma) (1, 2) is considered to be one of the most severe biotic crises during the Phanerozoic, with substantial impact on both marine and terrestrial ecosystems (3). This extinction is generally explained by global warming due to massive input of CO 2 and/or methane to the atmosphere from volcanic activity in the Central Atlantic Magmatic Province (CAMP) (4, 5), the most extensive large igneous province (LIP) on Earth (6). High-precision radioisotope ages of CAMP volcanic rocks show that magmatic activity commenced c. 100,000 years before the end-Triassic event (7) and continued in pulses for 700,000 years (Fig. 1A) (8). As shown by major perturbations in δ13C records across the Triassic-Jurassic boundary (TJB), prolonged and voluminous volcanism released vast quantities of the greenhouse gas CO 2 , as well as SO 2 , and other potentially toxic compounds to the atmosphere (4–6, 9). The presence of altered volcanic glass spherules, euhedral pyroxene, and amphibole pseudomorphs (10) and increased levels of iridium in marine sediments (11) are indicative of the far reach of CAMP activity, but ash beds from CAMP are thus far lacking outside the CAMP area. In preindustrial sedimentary records, temporal distribution of mercury (Hg) is considered a suitable proxy for fallout from volcanic activity (12–13). Mercury is emitted primarily as gaseous Hg not only via explosive volcanism but also via degassing from nonexplosive volcanism (14). Distribution of gaseous Hg (and other substances) from CAMP would have been governed by atmospheric circulation and high-altitude wind patterns (15). The long residence time in the atmosphere of gaseous elemental Hg (Hg0), from 6 months to 2 years, would promote global or at least hemispheric distribution of this element (15). Elevated Hg concentrations in sedimentary rocks (i.e., Hg anomaly) in marine TJB successions of Nevada (16), Canada, Greenland, England, Austria, Morocco, and Peru (17) have been linked to CAMP eruptions, suggesting widespread reach of volcanic Hg from the CAMP. Recently, the use of Hg in sedimentary successions as a proxy for LIP volcanic activity has been questioned (18, 19), as Hg can also be distributed to sedimentary basins by other sources. However, the possibly global and contemporaneous increase in Hg in both terrestrial and marine TJB successions (16, 17, 20) suggests increased input of Hg to the global mercury cycle at that time. Thus, the distribution of volcanic Hg in the TJB sedimentary record could potentially provide a means to probe the relationship between CAMP volcanic pulses and biotic responses at various sites. Fig. 1 TJB timeline and correlation of the Stenlille-1 record with Kuhjoch, Austria, and New York Canyon, Nevada. (A) U/Pb ages for CAMP intrusives (white circles), CAMP basalts (brown circles), and ash beds from Nevada and Peru (yellow circles), and ammonoid events (1, 7, 8, 32, 34). Note that U/Pb ages 4, 7, 11, and 14 are all from the North Mountain Basalt. 1, Kakoulima intrusion (7); 2, Tarabuco sill (7); 3, Messejana dike (7); 4, North Mountain Basalt (8); 5, Amelal sill (8); 6, Amazonas sill (low Ti) (7); 7, North Mountain Basalt (7, 8); 8, Palisades sill (8), feeder of the Orange Mountain Basalt; 9, York Haven intrusive (8); 10, Rapidan intrusive (8); 11, North Mountain Basalt (7); 12, Fouta Djalon sill (7); 13, Hodh sill (7); 14, North Mountain Basalt (1, 2); 15, Amazonas sill (high Ti) (7); 16, Shelburne dike (7); 17, Rossville intrusive (8); 18, Preakness Basalt (8); 19, Foum Zguid (7); 20, Ash bed LM4-86, Peru (1, 2); 21, Ash bed LM4-90, Peru (1, 2); 22, Ash bed NYC-N10, Nevada (1); 23, Ash bed LM4-100/101, Peru (1, 2); 24, Amazonas Basin sill, Brazil (33); 25, Solimões Basin sill, Brazil (33). (B) Ammonite zones and extinction interval (32). (C to E) Bulk organic C-isotope (as ‰ of Vienna Pee Dee belemnite) (9, 32) and Hg/TOC (in ppb/%) records for (C) Stenlille-1, (D) Kuhjoch, Austria (17, 34), and (E) New York Canyon, Nevada (16). For an expanded version of this figure showing correlations of Hg/TOC-records and Hg -records of all studied localities, see fig. S2. Here, we focus on investigating the possible correlation of Hg loading with evidence of stress responses of terrestrial plants in the fossil record, specifically in the palynological record. We know today that, apart from greenhouse and other gases, volcanic activity can emit a range of known primary phytotoxic pollutants, including Hg and other heavy metals, fluoride, O 3 , SO 2 , and polycyclic aromatic hydrocarbons (PAHs) (21). Phytotoxic substances can induce stress responses and cause morphologically visible abnormalities not only in the parent plants (e.g., stunted growth, lesions, necrosis, and shortening of roots) but also in the reproductive cells, i.e., spores and pollen (22). Studies of both extant and fossil plants suggest that normal sporogenesis results in 95 to 97% viable spores and 3 to 5% aberrant, nonviable spores (23–26). Therefore, aberrant spore quantities above 5% are generally regarded as indications of environmental stress. Because of the durability of their sporopollenin walls, abnormal pollen and spores can be used as bioindicators of environmental stress in preindustrial sediments—an especially useful proxy for phytotoxicity in the fossil record. However, it is necessary to differentiate between nonmutagenic and mutagenic aberrant spores or pollen, where the former can be induced through various environmental stresses (e.g., drought, frost, and water logging) disrupting the spore or pollen maturation process, commonly resulting in premature shedding of immature spores or pollen that may or may not be retained and dispersed in tetrads. Mutagenic changes in the mother plant, on the other hand, lead to an increase in the number of spores or pollen that are aberrant and nonviable. A few studies have noted increased abundances of aberrant spores and pollen during other extinction events linked to LIPs and have mainly attributed these to mutagenic effects of a thinned ozone layer (24, 27–28). Recent work demonstrates that elevated ultraviolet-B (UV-B) radiation increases malformations in pine pollen and that the resulting teratology (i.e., patterns of abnormal development) exhibits the same traits as those registered in gymnospermous bisaccate pollen during the end-Permian event (29), the most severe mass extinction of the last 540 Ma (3). Others have focused on the abundance of all abnormal spores and pollen across the Permian-Triassic boundary, suggesting that volcanic pollution from the Siberian Traps was responsible for the mutagenesis (30). Here, we quantify various types of abnormalities in the reproductive cells of ferns, i.e., teratology of fossil fern spores, and use this as a proxy for ecological stress and possible mutagenesis in land plants across the TJB. We examined the teratology of two morphogroups of smooth-walled (laevigate), trilete fern spores with fairly thick exine, which we refer to as LTT-spores (laevigate, triangular, trilete spores) (Fig. 2, A to F) and LCT-spores (laevigate, circular, trilete spores) (fig. S1), in the Danish and North German basins. Several other spore and pollen taxa also exhibit abnormalities during the TJB interval (31); however, LTT- and LCT-spores are ideal to use as proxies for environmental-induced teratology as they are simple trilete spores with rather thick and unsculptured walls (exines). The exine thickness limits folding and, thus, enables distinction between malformed specimens and spores that are merely poorly preserved or folded. Similarly, the lack of complex ornamentation makes it easier to assess morphological abnormalities. Normal LTT-spores are triangular in outline, with a trilete mark with or without labra (Fig. 2, A to F), while normal spores of the LCT morphogroup are circular, commonly without, or with only thin labra (fig. S1, A to D). The two morphogroups exhibit similar aberrant forms that are ranked in categories as mild to severe teratology [severity categories (C) to (J) in Table 1], suggesting disturbance during different developmental stages (Table 1). Fig. 2 Selected photos of LTT-spores teratology, arranged after teratology category defined in Table 1 In black frames: (A to F) representatives of normal spores. In white frames, mild teratology: (G and H) dwarfs, (I to K) unexpanded forms. In yellow frames, mild to moderate teratology: (L and M) uneven trilete mark, (N) uneven trilete mark and aberrant exine cracks, (O to Q) aberrant exine cracks or folds, (R to U) thickened labra or with growths, and (V) dwarf with thickened labra. In orange frames, moderate teratology: (W) quadrilete specimen, (X) monolete specimens with thickened labra, (Y and Z) mono- or multilete specimens, (AA) monolete specimen with deformed labra and possibly deformed outline, and (BB and CC) specimens with deformed outline. In light red frames, moderate to severe teratology: (DD) specimen with weakly deformed trilete mark and deformed outline, (EE) weakly deformed proximal area on a quadrilete specimen, (FF) weakly deformed proximal area with weakly discernable laesura and deformed outline, and (GG) conjoined twins. In dark red frames, severe teratology: (HH and II) severe proximal deformation. Scale bar, 20 μm. For sample number and England Finder coordinates, see table S1. Table 1 Teratology: Characterization, severity, and possible cause. View this table: To correlate the teratology record with the CAMP volcanism, we compare the teratology to Hg loading in stratigraphically well-constrained (32) marine successions in cored wells from the Danish Basin (Stenlille-1 and Stenlille-4) and the North German Basin (Rødby-1), that span the TJB. We also present teratology and Hg data from outcrop and core samples from the predominantly terrestrial Rhaetian (latest Triassic) Norra Albert/Albert-1 succession in the Danish Basin to test contemporaneous Hg accumulation in the Rhaetian mires and freshwater systems.

SUPPLEMENTARY MATERIALS Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/5/10/eaaw4018/DC1 Supplementary Text Fig. S1. Selected photographs of LTT-spores teratology, arranged after teratology categories defined in Table 1. Fig. S2. Expanded correlation from Fig. 1. Fig. S3. Plots showing the stratigraphic occurrence and abundance of each teratological form of LTT-spores. Fig. S4. Correlation between the localities studied herein. Fig. S5. Correlation of organic C-isotopes (4), charcoal data (56), PAH (52), and mercury data (17) from Astartekløft, Greenland. Table S1. Sample and slide numbers and England Finder coordinates for the LTT-spores illustrated in Fig. 2. Table S2. Stenlille-1: Counts of total and aberrant LTT-spores. Table S3. Stenlille-4: Counts of total and aberrant LTT-spores. Table S4. Rødby-1: Counts of total and aberrant LTT-spores. Table S5. Norra Albert/Albert-1: Counts of total and aberrant LTT-spores. Table S6. Stenlille-1: Counts of total and aberrant LCT-spores. Table S7. Stenlille-4: Counts of total and aberrant LCT-spores. Table S8. Rødby-1: Counts of total and aberrant LCT-spores. Table S9. Mercury and TOC values for the investigated localities. Table S10. Sample and slide numbers and England Finder coordinates for the LCT-spores illustrated in fig. S1. References (61–76)

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Acknowledgments: J. Halskov, Geological Survey of Denmark and Greenland (GEUS) helped with some of the illustrations. C.E.L. and C.T. also acknowledges support from the Danish National Research Foundation Niels Bohr Professorship for this research. Funding: This work was supported by the Geocenter Denmark grant 2013-6 (to S.L.) and benefitted from the grant ALW-OP.623 of the Dutch Science Foundation (NWO) (to B.v.d.S.). Author contributions: The project was designed by S.L. with input from H.S. and B.v.d.S. Palynological analyses were primarily carried out by S.L. with contributions from B.v.d.S., C.H., and K.D. The sedimentology was carried out by G.K.P. Mercury and TOC analyses were performed by H.S. and C.E.L., with input from C.T. The manuscript was developed by S.L., and all authors contributed to editing the final manuscript. Competing interests: The authors declare that they have no competing interests. Data and materials availability: All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Additional data related to this paper may be requested from the authors. All palynological slides are housed at the Geological Survey of Denmark and Greenland. Tables S1 and S10 list sample and slide numbers and England Finder coordinates for the photographed specimens. For quantitative teratological data, see tables S3 to S8. Mercury and TOC data are listed in table S9.