Bolide impact triggered the Late Triassic extinction event in equatorial Panthalassa

Extinctions within major pelagic groups (e.g., radiolarians and conodonts) occurred in a stepwise fashion during the last 15 Myr of the Triassic. Although a marked decline in the diversity of pelagic faunas began at the end of the middle Norian, the cause of the middle Norian extinction is uncertain. Here we show a possible link between the end-middle Norian radiolarian extinction and a bolide impact. Two palaeoenvironmental events occurred during the initial phase of the radiolarian extinction interval: (1) a post-impact shutdown of primary and biogenic silica production within a time span of 104–105 yr, and (2) a sustained reduction in the sinking flux of radiolarian silica for ~0.3 Myr after the impact. The catastrophic collapse of the pelagic ecosystem at this time was probably the dominant factor responsible for the end-middle Norian conodont extinction.

large chondritic impactor with a diameter of 3.3-7.8 km (refs 8 and 9). An impactor of this size would produce a crater of ~56-101 km in diameter 8 , assuming an impactor entry velocity of 20 km s −1 , an entry angle of 45° and a crystalline target (density = 2750 kg m −3 ). The size range of such a crater is consistent with the size of the Manicouagan crater (diameter, ~90 km) 15 . Outside of Japan, a Norian impact ejecta deposit with shocked quartz and spherules has been found in an Upper Triassic nonmarine sequence in southwestern Great Britain, which has yielded a diagenetic age (from authigenic K-feldspar) of 214 ± 2.5 Ma (ref. 16). Although the recalculated age of 216.7 Ma for the British ejecta deposit using the method of Renne and coworkers 17,18 is slightly outside the range of the Manoucouagan impact event age, a strong mineral correspondence between samples from Manicouagan and the ejecta deposit provides convincing evidence that the Manicouagan impact was the source of the Great Britain ejecta deposit 19 .

Results
Extinction and origination patterns. We analysed a large dataset of Upper Triassic radiolarian occurrences in the Inuyama area 7,[20][21][22] , to assess the magnitude of the extinction event caused by the middle Norian impact, and to compare this event with extinction events at other stage boundaries. An analysis of the stratigraphic ranges of radiolarian species in Japan indicates a dramatic increase in extinction and origination rates across the impact horizon (Fig. 2). Radiolarians show similar (and relatively low) extinction and origination rates throughout much of the late Carnian-middle Norian. Across the ejecta horizon, a dramatic increase in extinction rate is observed in the 1-Myr interval following the impact event. Such a high extinction rate of radiolarians has not been recognized within the Norian interval 23 , and surprisingly, the magnitude of the extinction event is substantially higher than that of the radiolarian extinction at the TJB 21 . Radiolarian species diversity data show a steady decrease in diversity throughout the late Carnian to middle Norian. A sharp increase in diversity is observed across the ejecta horizon, and the diversity reaches a maximum value of 40 species (without singletons) during the late Norian. The diversity then declines rapidly throughout the Rhaetian, reaching a low point in the Hettangian (19 species). These results suggest that the middle Norian impact triggered the extinction and contemporaneous evolutionary radiation of the radiolarian fauna in the equatorial Panthalassa Ocean.
Biostratigraphy and chemostratigraphy. An analysis of patterns of radiolarian extinction (Fig. 2) reveals a high extinction rate in the 1 Myr interval after the impact event. To determine whether the extinctions were coincident with the impact event, we conducted a detailed bed-by-bed biostratigraphic analysis of the ~2 Myr interval across the ejecta horizon (Fig. 3). Our biostratigraphic analysis of the study section clearly shows that the impact event initiated the radiolarian extinction and the evolutionary radiation of new taxa. The present data show no catastrophic pattern 24 of radiolarian extinctions at the impact event horizon. However, gradual extinctions of radiolarians are observed within ~1 m above the ejecta horizon, in the end-middle Norian (Fig. 3). A biostratigraphic analysis shows that 14 middle Norian taxa gradually disappeared during this interval, including all Capnodoce and most Capnuchosphaera species. An initial phase of diversification (phase D1) started in the upper sublayer of the claystone and in the overlying chert bed. A second major wave of diversification (phase D2) is observed ~33 cm above the ejecta horizon. Given an average sedimentation rate of 1.1 mm kyr −1 in the middle Norian chert succession ( Supplementary Fig. S2), this second diversification occurred within ~0.3 Myr after the impact event.
To evaluate changes in primary productivity, we examined stratigraphic variations in organic carbon isotopic values (δ 13 C org ) from the study section at Sakahogi (Supplementary Table S1). The data show that δ 13 C org values are relatively constant below the ejecta claystone (average δ 13 C org , − 25.22‰), but that a negative δ 13 C org excursion is present in the upper claystone sublayer (Fig. 3). The δ 13 C org values increase rapidly upwards, and then recover to pre-impact levels at the first chert bed overlying the claystone layer (− 25.13‰). Above the claystone interval, δ 13 C org values vary from − 27.09‰ to − 24.57‰ (average δ 13 C org , − 25.44‰).

Discussion
A preliminary biostratigraphic study of the section at Sakahogi shows that most of the middle Norian radiolarian taxa are present in the 30 cm interval above the ejecta layer, and apparently survived well into the late Norian 7 (Supplementary Fig. S4). However, our new biostratigraphic data collected from above the previously sampled horizon indicate that extinctions of middle Norian species occurred in a stepwise fashion in the ~1 m interval above the ejecta horizon. Furthermore, our high-resolution palaeontological and geochemical data reveal that two palaeoenvironmental events occurred during the initial phase of the radiolarian extinction interval (Fig. 3). The first event (E1) consisted of the post-impact shutdown of primary productivity and a remarkable decline in the amount of biogenic silica preserved before the first phase of diversification (D1). The second event (E2) consisted of a large and sustained reduction in the sinking flux of radiolarian silica and the proliferation of siliceous sponges, occurring before the second phase of diversification (D2) and lasting for ~0.3 Myr after the impact. During the initial E1 event, the post-impact reduction in primary productivity occurred during deposition of the clay layer, as suggested by the negative δ 13 C org excursion observed in the claystone. Concentrations of TOC with low δ 13 C org values could be interpreted to represent a change in the proportion of organic matter derived from land plants versus oceans 25,26 . However, low and relatively stable C/N ratios (mean, 1.8; standard deviation, 0.6) throughout the study section indicate that contributions of land-derived organic matter are minor to absent. The rapid decrease in the biogenic silica content in the claystone (Supplementary Table S3) further indicates that the productivity of silica-secreting radiolarians was sharply reduced, and that marine primary productivity declined during the initial E1 event. Laboratory studies show that radiolarians prey on phytoplankton, such as dinoflagellates, haptophytes, and thecate nonmotile algae 27,28 ; however, we know little about the ecological factors that influence radiolarian productivity. A decline in radiolarian production in the near-surface zone may imply major changes at the base of the marine food chain, such as a substantial reduction in primary productivity or a shift toward primary producers not favored by pre-impact taxa.
The negative δ 13 C org excursion and the rapid decrease in biogenic SiO 2 content observed in the upper part of the claystone occurs within a 3.2-cm-thick section, suggesting a very short time scale for the E1 event. We used previously published 187 Os/ 188 Os ratio results 9 to estimate the duration of low-productivity conditions after the impact. Previous studies have revealed that 187 Os/ 188 Os ratios declined abruptly, from 0.477 to 0.126, in the lower sublayer of the claystone. This excursion can be interpreted as a result of the mixing of ambient seawater Os (characterized by relatively high 187 Os/ 188 Os ratios) with meteoritic Os (characterized by low 187 Os/ 188 Os ratios); the meteoric Os was vaporized at the time of the impact and was subsequently dissolved into seawater. The 187 Os/ 188 Os ratio, which is lowest in the lower sublayer, gradually increases towards the upper sublayer, and reaches pre-impact levels in chert samples overlying the claystone layer. No discrete extraterrestrial particles were observed in the upper sublayer claystone, which indicates that the 187 Os/ 188 Os ratio of this sublayer records the Os isotope composition of ancient seawater 9 . Therefore, the recovery of 187 Os/ 188 Os values in the upper sublayer claystone after the impact event may reflect post-impact removal of excess dissolved meteoritic Os from seawater, which occurred over a period of 10 4 -10 5 yr, as Os residence times range from 10 to 60 kyr (refs 29 and 30). Although the marine residence time of Os in the Late Triassic is not precisely known, deposition of the upper sublayer clay may have occurred over the period 10 4 -10 5 yr after the impact event. This interval is hypothesized to represent the duration required for the restoration of productivity by primary and silica-secreting organisms after the middle Norian impact. However, simulations using an ocean-atmosphere/carbon-cycle model 31 , which suggest a global collapse of primary productivity (in the Strangelove Ocean) resulting in the delivery and cycling of carbon in the oceans and on land, cannot explain such short-term (10 4 -10 5 yr) shifts in δ 13 C org values across the ejecta layer. The global implications of the magnitude and short duration of the negative δ 13 C org excursion reported here remain to be verified at other middle-late Norian boundary intervals worldwide.
Following the resurgence in primary productivity after the E1 event, the biogenic silica content had recovered to pre-impact values by the first chert bed overlying the claystone layer. However, our analysis reveals that major biotic components of the bedded chert changed temporarily from radiolarians to siliceous sponges, for ~0.3 Myr after the impact. Assuming a constant sedimentation rate in the middle-upper Norian chert succession of 1.1-1.6 mm kyr −1 , and a constant dissolution rate of biogenic silica during that time, the mass accumulation rates (MAR) of radiolarian silica in the pre-impact chert beds is estimated at ~0.1 g cm −2 kyr −1 , which is the same as the biogenic silica flux near the equator in the modern Pacific Ocean (0.1-0.3 g cm −2 kyr −1 ) 32 . After the impact event, the MAR decreased to 0.02 ± 0.01 g cm −2 kyr −1 in the upper sublayer claystone, and then remained low during the deposition of sponge spicule-rich cherts. On the other hand, the MAR of the siliceous sponge silica increased markedly across the claystone layer of the ejecta deposit, from ~0.01 to ~0.08 g cm −2 kyr −1 , and subsequently decreased to ~0.01 g cm −2 kyr −1 after the E2 event. Our data and previous data 9 on terrigenous elements (e.g., Ti, Al, and K) indicate that the flux of terrestrial components (aeolian dust) derived from continental crust 22,33 did not change substantially through the study interval; thus, the significant and sustained reduction in the flux of radiolarian silica appears to have coincided with an increasing volume of siliceous sponge spicules. During the Mesozoic, the concentration gradient caused by the export of silica from surface to deep waters by sinking of marine plankton may not have been as intense as in modern diatom-dominated oceans 34 , and such concentration gradients in any case would have been briefly interrupted by fluctuations in radiolarian productivity. Even lacking a direct record of Triassic silica concentrations, it is likely that a reduction in radiolarian productivity in the Panthalassa Ocean during the E2 event, which probably increased the amount of dissolved silicic acid in seawater, favored the proliferation of siliceous sponges after the impact event. Laboratory experiments on silicon uptake by siliceous sponges reveal that an increased concentration of silicic acid in water has a striking positive effect on both the size and robustness of siliceous sponge spicules 35 . Our hypothesis that dissolved silicic acid increased in seawater at the time of the E2 event is supported by the observation that longer and more robust skeletons of siliceous sponge spicules were dominant only in the spicules of the spicule-rich chert ( Supplementary Fig. S10).
Decreases in the sinking flux of radiolarian silica during the E1 and E2 events may reflect a decline in radiolarian production in middle Norian taxa, including in Capnodoce and Capnuchosphaera species. These middle Norian radiolarians are very rare above the E1 interval, whereas a small spumellarian species is abundant within the E2 interval; this spumellarian species is reported as Spumellaria gen. et sp. indet. A, and its occurrence can be used to identify the stratigraphic position of the ejecta layer in other Triassic chert sections within the Jurassic accretionary complexes in Japan 9 . These taxa can be considered as short-lived opportunistic species, as they disappeared at the end of the radiolarian faunal turnover interval. The present biostratigraphic analysis also reveals that radiation of late Norian taxa was contemporaneous with a temporal bloom in the numbers of opportunistic spumellarian species in the E2 interval. The timing of these radiation events suggests that the decrease in radiolarian biomass in the middle Norian taxa enhanced the bloom of opportunistic radiolarian species and the evolutionary radiation of late Norian taxa in the E1 and E2 intervals. Hence, the gradual extinction of middle Norian radiolarian taxa during the ~1 Myr period could be explained by ecological pressures imposed by late Norian taxa, provided that the late Norian taxa were more rapidly growing and more efficient phytoplankton feeders than the middle Norian taxa. These unusual radiation patterns are similar to those observed in the Panthalassic TJB sections in Japan and Canada 21,22 . As with the TJB event, changes in seawater acidity, temperature, and/or a reduced nutrient levels in ocean surface waters are possible drivers for the decline in the production of middle Norian radiolarian taxa. The primary cause of this decline is difficult to identify, but the relatively long period of the E2 interval (~0.3 Myr after the impact) largely excludes the possibility that the decline was triggered by instantaneous environmental stresses (e.g., extended darkness, global cooling, or acid rain 24,36 ) that would have been caused by a bolide impact.
Did the middle-late Norian extinction event occur uniformly on a global scale, or does it represent a regional phenomenon in the Panthalassa Ocean? The record of radiolarian faunal change across the middle-upper Norian boundary has been established at the species level in several regions 37,38 , showing that widespread and apparently sudden extinctions affected the Subfamily Capnodocinae and Family Capnuchosphaeridae at the boundary 23 . As a first approximation, it is probably reasonable to assume that a geographically widespread faunal change across the middle-upper Norian boundary was related to an impact event that triggered the radiolarian extinction in the equatorial Panthalassan Ocean. Existing radiolarian records are not sufficiently precise to constrain these relationships with biostratigraphic resolutions comparable to those presented here for the middle-upper Norian. Further biostratigraphic analyses of middle-upper Norian boundary sections will be required to validate this hypothesis.
We propose that the impact event was probably the major factor responsible for the conodont and Pacific (North American) ammonoid extinctions that occurred in the middle-upper Norian boundary [39][40][41] . The base of the Epigondolella bidentata conodont zone and the base of the Gnomohalorites cordilleranus ammonoid zone in western North America 39,40 define the position of the middle-upper Norian boundary that is most closely aligned with the traditional base of the Sevatian 41 , and which can be correlated with the radiolarian extinction interval in the study section in Japan. Although ammonoids are absent in the studied section, the biostratigraphic record of conodonts suggests that a few Parvigondolella species survived across the ejecta layer, but that an important middle Norian Epigondolella species became extinct just below the impact horizon ( Supplementary Fig. S11). The present data also show the first appearance of late Norian Epigondolella species in the E1 and E2 intervals. Conspicuous morphological changes occur in this genus across the ejecta layer; Epigondolella species below the ejecta layer are characterized by a wide platform, whereas those above the ejecta layer possess a longer and more narrow platform. The catastrophic collapse of the pelagic ecosystem during the E1 and E2 events was probably the major factor responsible for the conodont turnover that occurred at the end of the middle Norian.
This study has revealed that late middle Norian open-ocean ecosystems experienced profound disruptions after a large impact event (chondritic impactor of 3.3-7.8 km in diameter), and that the event was possibly related to the 90-km-diameter Manicouagan crater in Canada. Although many marine sections over the past 540 Myr have been examined, no catastrophic collapse in marine ecosystems caused by an extraterrestrial impact has yet been described, with the outstanding exception of the Cretaceous-Paleogene boundary (KPB) crisis 24 and the middle Norian event reported here. Given that no large volcanic events occurred in the Norian 3 , the fossil record of the middle-upper Norian is key to evaluating the general importance of impacts as causes of biotic and environmental changes in pelagic ecosystems.

Biostratigraphy.
To extract radiolarians for biostratigraphic analyses, 53 chert samples were soaked in a dilute HF solution (5%) for 24 h, and were then passed through a 32-μ m mesh sieve. This treatment was repeated 2-5 times to obtain sufficient residue for analysis. After drying the residue, radiolarians were handpicked under a binocular microscope and were observed using a scanning electron microscope. Conodonts were handpicked from the same residues used for the radiolarian biostratigraphy.
Carbon isotope and major element analyses. Samples for whole-rock geochemical analysis were collected from 45 chert and claystone beds across the ejecta layer. Veins and strongly recrystallized/weathered parts of the samples were avoided to minimize the effects of diagenetic and metamorphic overprinting on the sediment geochemistry. Samples were crushed and fragments were carefully hand-picked to avoid contamination by altered and weathered materials. These hand-picked fragments were then pulverized in an agate mortar for carbon isotope analysis. All glassware used in the analyses was baked for 3 h at 450 °C, and all tools were cleaned with methanol between uses to avoid organic carbon contamination. Approximately 0.8 g of each sample was treated with an excess of 6 M hydrochloric acid for 48 h at 60 °C. Samples were then rinsed five times with ultrapure water (> 18 MΩ) and dried. Carbon isotope ratios and carbon and nitrogen contents were measured using an elemental analyser (FlashEA 1112) coupled to a Thermo-Finnigan Delta Plus Advantage isotope ratio mass spectrometer at the Centre for Advanced Marine Core Research, Kochi University, Japan. Isotopic measurements were repeated two times for 19 samples across the claystone (ejecta) layer to check the reproducibility of the results. The carbon isotope ratios were calculated using standard Alanine; the precision of the organic carbon ratio (δ 13 C org ) determinations was ± 0.5‰. The analyses showed good reproducibility of values, with 3% or less fluctuation (average, 2%; N = 18). All isotopic results are reported in conventional delta (δ ) notation, defined as per mill (‰) deviations from the Vienna Peedee Belemnite (VPDB) standard value.
Major element (Si, Ti, Al, Fe, Mn, Mg, Ca, Na, K, and P) contents of the bulk-sediment samples from the cherts and claystones in the Sakahogi section were measured using a Rigaku ZSX Primus II X-ray fluorescence (XRF) spectrometer at the University of Tokyo. After drying the powdered samples at 110 °C for ~12 h, loss on ignition (LOI) was calculated from the weight loss during ignition at 950 °C for over 6 h. Fused glass beads for XRF analysis were made from a mixture of 0.4 g of ignited sample powder and 4 g of lithium tetraborate (Li 2 B 4 O 7 ) flux at ~1190 °C for 7 min in a Pt crucible. The analytical results were generally within 3% (relative percent difference) of accepted values of reference material JB-2, issued by the Geological Survey of Japan 42 .
Diversity measurements. Regional species-level diversities of radiolarians throughout the Carnian to Hettangian were measured in 10 chert sequences in the Inuyama area, Japan. The data comprise 2196 occurrences of 156 radiolarian species from 361 stratigraphic levels in the study sections; the collection intensity was uniform and without sampling gaps (Supplementary Fig. S2). Species ranges were analysed using metrics established by Foote 43 , including: total diversity, total diversity minus singletons, estimated mean standing diversity, per-taxon rate, and the Van Valen rate. Extinction (E) and origination (O) rates reported here were calculated for 1-Myr intervals using Foote's per-taxon rate: Productivity reconstruction. The Triassic bedded cherts in the Inuyama area comprise biogenic silica (radiolarian tests and siliceous sponge spicules) and terrestrial components derived from the continental crust (aeolian dust) 22,33 . Biogenic silica (BSi) was calculated as follows: where PAAS is a shale standard based on the composition of post-Archean average Australian shales 44 . In this calculation, the amount of terrigenous Si that is mainly supplied by aeolian dusts is subtracted from the total concentration of Si in the bedded cherts. To assess the relative contributions of the radiolarian and sponge silica to the BSi, we determined the volumetric composition of radiolarians and siliceous sponges three times by standard 300-grain points counts (grain-solid method) for 118 thin sections. The percentages of radiolarian and sponge silica (Si rad and Si sponge , respectively) were then calculated as follows: where V rad and V sponge are the volumetric compositions of the radiolarians and siliceous sponges based on thin section analysis, respectively. Then, the mass accumulation rate (g cm −2 kyr −1 ) of radiolarian and sponge silica (MAR rad and MAR sponge , respectively) was calculated as follows: where ρ is the bulk density of chert (2.46 g cm −3 ) or claystone (1.69 g cm −3 ) and a is the sedimentation rate for chert (0.11-0.16 cm kyr −1 ) or claystone (0.09 cm kyr −1 ). The sedimentation rate of the claystone layer was calculated from the measured thickness (3.2 cm), and the time interval of its deposition was estimated using a mean oceanic residence time of Os (~3.5 kyr) 29 , as discussed above.