Eccentricity and obliquity paced carbon cycling in the Early Triassic and implications for post-extinction ecosystem recovery

Abstract

The timing of marine ecosystem recovery following the End Permian Mass Extinction (EPME) remains poorly constrained given the lack of radiometric ages. Here we develop a high-resolution carbonate carbon isotope (δ¹³ C_carb ) record for 3.20 million years of the Olenekian in South China that defines the astronomical time-scale for the critical interval of major evolutionary and oceanic events in the Spathian. δ¹³ C_carb documents eccentricity modulation of carbon cycling through the period and a strong obliquity signal. A shift in phasing between short and long eccentricity modulation, and amplification of obliquity, is nearly coincident with a 2% decrease in seawater δ¹³ C_DIC, the last of a longer-term stepped decrease through the Spathian. The mid-Spathian shift in seawater δ¹³ C_DIC to typical thermocline values is interpreted to record a major oceanic reorganization with global climate amelioration. Coincidence of the phasing shift with the first occurrence of marine reptiles (248.81 Ma), suggests that their invasion into the sea and the onset of a complex ecosystem were facilitated by restoration of deep ocean ventilation linked mechanistically to a change in the response of the oceanic carbon reservoir to astronomical forcing. Together these records place the first constraints on the duration of the post-extinction recovery to 3.35 myr.

Eccentricity and obliquity paced carbon cycling in the Early Triassic and implications for post-extinction ecosystem recovery

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Wanlu Fu, Da-yong Jiang, Isabel P. Montaez, Stephen R. Meyers, Ryosuke Motani & AndreaTintori

The timing of marine ecosystem recovery following the End Permian Mass Extinction (EPME) remains poorly constrained given the lack of radiometric ages. Here we develop a high-resolution carbonate carbon isotope (Ccarb

the astronomical time-scale for the critical interval of major evolutionary and oceanic events in the Spathian. Ccarb documents eccentricity modulation of carbon cycling through the period and a strong

CDIC, the last of a longer-term stepped decrease through the Spathian. The mid-Spathian shift in seawater CDIC to typical thermocline values is interpreted to record a major oceanic reorganization with global climate amelioration. Coincidence invasion into the sea and the onset of a complex ecosystem were facilitated by restoration of deep ocean ventilation linked mechanistically to a change in the response of the oceanic carbon reservoir

Previous studies have shown that post-extinction recovery from the EPME was delayed14 until Middle Triassic due to anomalous oceanic conditions during the Early Triassic, elevated CO2 and surface temperatures57, widespread anoxia813 and high primary productivity14,15. However, discovery of an Early Triassic (Griesbachian to Early Smithian) rapid recovery of benthic faunas including bivalves, gastropods, brachiopods, and ostracods in Oman and the South China Block argues against persistent widespread anoxia16,17 and challenge the delayed-recovery hypothesis. Rather, a later period of widespread benthic anoxia and hot tropical temperatures at the Smithian-Spathian boundary created a new biocrisis with slowed rate of recovery6,7, making the pattern of post-extinction recovery more complex. Notably, most prior studies of the biotic recovery have focused on invertebrate benthic marine faunas24,16,17. Mesozoic marine reptiles, such as ichthyopterygians and sauropterygians, rst occurred in the Early Triassic as a part of the transition from the Paleozoic Fauna to the Modern Fauna, and dominated the Mesozoic seas18,19. Our collection of more than 80 well-preserved and multi-clade mid-Spathian marine reptile specimens from the Majiashan Section, Chaohu, South China documents that predatory marine tetrapods diversied in the Early Triassic and were well adapted to life in the sea, indicating a habitable marine environment in the mid-Spathian at Chaohu, which is earlier then previously suggested. The diverse predators, including sh and marine reptiles, and abundant invertebrates such as bivalves, ammonoids and arthropods, form the Chaohu Fauna, represent a nearly complete ecosystem. The rst appearance of abundant and multi-clade Mesozoic marine reptiles in Chaohu provides the rst glimpse of recovering biotic structure reaching a high

Laboratory of Orogenic Belt and Crustal Evolution, Ministry of Education; Department of Geology and Geological Department of Earth and Department Dipartimento di Scienze

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trophic level. The lack of geochronologic data, however, has precluded constraining the age of the Chaohu Fauna and thus the timing of post-extinction recovery remains poorly known.

Deep-sea 13Ccarb records of mid-Cretaceous to Cenozoic age reveal a persistent long-eccentricity (405-kyr) cyclicity, which records astronomical pacing of carbon cycling among Earths surface reservoirs2024. Astronomical cyclicity is also recognized following the EPME2527, when potentially the largest carbon cycle perturbation of the Phanerozoic was followed by a series of disturbances throughout the Early Triassic interval of protracted marine ecosystem recovery2,28. Astronomical cycles in carbon cycling, however, have not yet been recognized leaving ambiguous the timing of the post-extinction recovery and the role of astronomical pacing of climate and carbon cycling through a signicant portion of the biotic recovery phase. Furthermore, constraining the drivers of major carbon cycle perturbation is fundamental to understanding climate and biosphere dynamics throughout Earth history29,30.

The nature of the mechanistic link between post-extinction carbon cycle perturbations and the Early Triassic biotic recovery has been the focus of much research invoking wholesale changes in ocean oxygenation and water column stratication13,15. Major oceanic restructuring is inferred to have occurred in response to global warming, likely driven by episodic release of exogenic carbon from Siberian Trap volcanism6,31. Conversely, the role of internal mechanisms and feedbacks in the Earths climate system, including cycling through the surface carbon reservoirs, has not been investigated in the context of the recovery of life aer the largest extinction since the evolution of metazoans. In this study, we develop a new high-resolution C isotopic record of seawater dissolved inorganic carbon (13CDIC) for the end-Smithian through Spathian, utilize it to construct an astrononmical time scale, and in turn, apply it to infer major changes in ocean structure mechanistically linked to the timing of ecosystem recovery.

Results

A high-resolution 13Ccarb record is constructed spanning the end-Smithian through Spathian (~250.55 to 247.32 Ma, Olenekian, Early Triassic)32,33, from an intermediate- to deep-water 200 to 500 m) slope succession in Majiashan, Chaohu, South China (Fig.1). Observed uctuations in 13Ccarb are interpreted to record secular changes in seawater 13CDIC, an inference that is supported by the lack of correlation between 13Ccarb and lithofacies changes, 18Ocarb, 13Corg or wt.% CaCO3 (see Supplementary Figs S4 and S5). The veracity of the new 13Ccarb record is corroborated by similarity in long-term 13Ccarb trends between the Majiashan section and other global time-equivalent 13Ccarb records from South China and elsewhere2,34,35. The Majiashan 13Ccarb time-series (Fig.1) reveals 3 scales of variation: (i) an abrupt 4% positive shi across the Smithian-Spathian boundary (S-S boundary) observed in previous records31, (ii) a subsequent 106-yr-scale stepwise decrease from peak values of +2% to +4% in the early Spathian to minimum values of 0% to 3% in the middle-late Spathian; and (iii) low-amplitude (0.51%), shorter-term (105-kyr scale) oscillations superimposed on the middle-late Spathian portion of the longer-term trend (see Supplementary Fig. S6).

To evaluate potential astronomical cycles preserved in the record and their uncertainties, evolutive average spectral mist (e-ASM) analysis36 was performed on the 13Ccarb record following data preparation (see R_analysis le) by statistically comparing the observed oscillations with theoretical periods from the astronomical models La0437 and La10d38 (see Supplementary Fig. S8, Supplementary Table S2). The results show continuous short-term eccentricity, obliquity and precession over a range of sedimentation rates (see Supplementary Fig. S8, Supplementary Table S3). Using the ASM-calibrated astronomical cycles, frequency domain minimal tuning was applied to generate a oating ATS (see Supplementary Fig. S10). Following frequency-domain minimal tuning using the average eccentricity period of 115.30kyr (E2/2+ E3/2 from Supplementary Table S2; see Supplementary Fig. S10), the Majiashan 13Ccarb record exhibits power spectra peaks at periods of 457.20kyr, 127.00kyr, 46.79kyr, 29.31 kyr, 22.07 kyr and 19.03 kyr (Fig.2B, see Supplementary Fig. S11, Supplementary Table S5). A strong and continuous obliquity signal in the Evolutive Power Spectral Analysis (EPSA) of the tuned data (Fig.2C, Supplementary Fig. S12), as well as a relatively persistent precession signal (Fig.2C), provide independent conrmation of the short eccentricity minimal tuning implemented here.

The astrochronologic testing results provide a good basis for developing a nominal anchored astronomical time scale (ATS) and for dating the age of the rst occurrence of Mesozoic marine reptiles, which invaded the marine environment and represent the start of the establishment of the new marine ecosystem dominated by the air-breathing tetrapods28. Given the lack of high-resolution radioisotopic geochronology and biostratigraphy to anchor the ATS, we rely upon an assumption based on late Mesozoic and early Cenozoic carbon cycling studies, i.e. 13Ccarb minima correspond to eccentricity maxima2024,3943. Thus, the reversed eccentricity curve of La10d was tied at 247.95 Ma to a depth of 162.62m (Fig.2E,F). Using this approach, the S-S boundary34 in the Chaohu area, marked by an abrupt 4% positive shi in 13Ccarb at the top of fossil-rich black shale (pink line in Figs1 and 2DF), is constrained to 250.21Ma, which compares well with the radioisotopic date of 250.550.51Ma32 for the earliest Spathian. The duration of the 1.36-m thick black shale (18.46m to 19.82m, see Supplementary Fig. S2A) below the S-S boundary was estimated to be 19.21 kyr using an astronomically calibrated average sedimentation rate of ~7.08cm/kyr (see Supplementary Table S4). Although the exact stratigraphic level of the Spathian-Anisian boundary is unknown in the Chaohu area, it can be inferred at the Majiashan section to be at ~171.70 3.72m above the S-S boundary using an end-Spathian age of 247.320.08Ma33. In this case, the astronomically tuned time series constrains the duration of the Spathian interval to 2.89 0.08 My, which falls within the uncertainty of the U-Pb estimated duration of 3.230.60 My32,33,44.

According to our excavation at the Majiashan section, the lowest stratigraphic level of occurrence of marine reptiles in the Chaohu Fauna occurs in the Middle Member of the Nanlinghu Formation, ~117.00 m above the base of the Helongshan Formation (Fig.1), and is constrained to ~248.81 Ma (Fig.2). Abundant ichthyosauromorphs occur in the interval 135.83m to 149.26m above the base of the Helongshan Formation with a duration of ~279.79kyr (Fig.1), including Chaohusaurus, which was fully adapted to the marine aqueous habitat and yet

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Figure 1. Stratigraphy and 13Ccarb data values on column for Majiashan section (see Supplementary Table S1) with vertebrate fossil distribution. The pink horizontal line shows the stratigraphic level of the end-Smithian biocrisis, coincident with a rapid increase in 13Ccarb; the green horizontal line shows therst occurrence of Triassic marine reptiles. Helong. Fm.: Helongshan Formation; D. Fm.: Dongmaanshan Formation. The large silhouettes to the le of the lithology are marine reptiles; the small silhouettes to the le of the lithology (and one medium silhouette) are sh.

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Figure 2. Spectra analysis results of the Majiashan 13Ccarb data following astronomical tuning and anchoring. (A) 115.30-kyr-tuned time series (see Supplementary Table S4). (B) Multi-taper method spectral analysis (MTM) results, using three tapers and a time-bandwidth product of 2p. The calibrated periods of signicant peaks are shown in kyr; these peaks achieve the 90% condence level for both the MTM harmonic F-test and the AR1 red noise model (bold) or the AR1 noise model only (italics) (see Supplementary Fig. S11, Supplementary Table S5). (C) Evolutive power spectral analysis (EPSA) results, using a moving windowof 1000kyr, 3 tapers and a time-bandwidth product of 2p (see Supplementary Fig. S12). A linear trend was removed from each window prior to the EPSA. Letters E1-P mark the eccentricity, obliquity and precession cycles separately (see Supplementary Table S2). (D) Phases that are dened by the minima of the ltered 405-kyr components (in E). Horizontal dashed lines are phase boundaries. (E) Filtered 13Ccarb time series for

Majiashan section. Red and blue curves indicate short and long eccentricity cycles dened using bandpass lters of 0.00150.0028 cycles/m and 0.0060.011 cycles/m, respectively. Black dotted lines show the instantaneous amplitude envelope of the 13Ccarb short eccentricity signal. (F) Theoretical eccentricity from La10d from 249.0

Ma-247.0Ma. Red and blue curves indicate short and long eccentricity cycles. Note that La10d eccentricity curves are reversed to illustrate relationship between 13Ccarb maxima and eccentricity minima in Phase 6 marked by blue shading (see Supplementary Table S4). Radioisotopic dates from ref. 32,33. Correlation of latest Spathian interval constrained by radioisotopic ages shown by grey shading. The large silhouettes to the right of Panel F are marine reptiles; the small silhouettes to the right of Panel F (and one medium silhouette) are sh.

maintained a birth posture typical of terrestrial reptiles, and Cartorhynchus with possible amphibious habits and suction-feeding behavior45. The most primitive Eosauropterygia46, which shows similarity to Middle Triassic Eosauropterygia, occurs ~156.12 m above the base of the Helongshan Formation (Fig.1) and is constrained to ~248.10Ma (Fig.2). Ichthyosaurs were also found in the upper Spathian (Fig.2).

Discussion

Persistent eccentricity and obliquity cyclicity in the EHA of the tuned 13Ccarb data (see Supplementary Fig. S12) indicates astronomically-paced redistribution of carbon between surcial C reservoirs. Seven phases of 13Ccarb

are identied from the minima of the ltered 405-kyr components (long-term eccentricity) (Fig.2D). The good alignment between the amplitude envelope of the ltered 100-kyr components and the 405-kyr components in Phases 5 through 7 shows the robustness of the tuning results (Fig.2E). The overall weaker short eccentricity and variable phase relationship observed in Phases 1 through 4 suggests a fundamental change in the response of seawater 13C to astronomical forcing in the mid-Spathian, coincident with the onset of increased short-term

13CDIC volatility and a 2% decrease in 13CDIC, the last of a stepped long-term decrease following the S-S boundary

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positive excursion. The amplication of obliquity (Fig.2C) begins between the two abrupt 13C shis that dene the longer-term decrease in the Spathian.

The response of the ocean carbon reservoir to astronomical forcing is largely dependent on the oceanic structure, which in turn responds to climate change23. Astronomically paced changes in ocean ventilation (oxygenation) lead to periodic releases of 12C-enriched carbon to the surface ocean. For greenhouse times, such as the Early Triassic47, the greater water column stratication of greenhouse oceans makes the ocean C budget more sensitive to orbital variations20,23,24. Together the shi in eccentricity phasing and obliquity amplication likely record a major restructuring of oceanic circulation (cf. refs 24 and 25) linked to climate amelioration during the Spathian13,31. A strongly stratied water column would have supported an expanded oxygen minimum zone and build up of a large dissolved organic carbon (DOC) reservoir in the deep ocean (cf., ref. 48). Turnover from such an oceanic state to a better and deeper ventilated ocean with major restructuring would have released large amounts of this 12C-enriched carbon pool to surcial C reservoirs and accelerated the rate of carbon cycling thus amplifying the response of seawater 13CDIC to eccentricity and obliquity forcing/pacing20,21. In this context, we interpret the overall higher 13Ccarb values (+2 to +4%) of the rst 800kyr (Phase 23) of the Spathian as recording strong water column stratication, high productivity, enhanced organic matter burial and likely build up of the deep ocean DOC reservoir promoted by the expanded oxygen minimum zone13. The subsequent change in the nature of eccentricity and obliquity cyclicity, along with the nal abrupt shi to values that uctuate around a stable mean (~2%) characteristic of pre-perturbation thermocline 13CDIC values in the Majiashan slope environment31, constrains the timing of termination of O2-limited oceanic conditions to the mid-Spathian. The observation of obliquity amplication within phase 4, and continuing into phases 5 through 6, is consistent with the development of a high-latitude, oxygenated, intermediate to deep-water source perhaps in response to cooling and/or eustatic change (cf. ref. 4951) that would have led to enhanced ventilation of the deep ocean. The near loss of long-term eccentricity 13Ccarb cyclicity in Phase 7, and weakening of obliquity, could capture the return to a fully stable well-oxygenated ocean sustained by vigorous circulation (cf. ref. 24).

The ATS indicates that the stratigraphically lowest marine reptile fossil in the Chaohu Fauna, and around the world52, occurs in the later portion of Phase 4 and has an age of ~248.81Ma. This is the oldest known Mesozoic marine reptile found to date despite concerted but unsuccessful search eorts to nd older fossils. Thus, the timing of reptilian invasion into the oceans was likely not much earlier than 248.81Ma. This estimate constrains the post-extinction ecosystem recovery period to ~3.35Myr aer the PTB (at ~252.16Ma, as recognized in ref. 32). The main reptile fossil beds that yield Cartorhynchus, a basal and potentially amphibious ichthyosauriform45, as well as abundant multi-clade marine reptile fossils, occur within Phases 5 and 6 (Fig.2DF). The Chaohu Fauna is the oldest marine fauna with tetrapod as top predators and a high marine ecosystem complexity, as far as we know.

Previous studies of Early Triassic benthic faunas and vertebrate fossil localities with limited marine ecosystem complexity53,54 supported the hypothesis of a delayed biotic recovery2,4. The appearance of marine reptiles45,46 and the Triassic middle sh fauna (TMFF)55 in Chaohu in the middle Spathian marks the initiation of the establishment of a new Meso-Cenozoic marine ecosystem and thus indicates a high degree of biotic recovery following the end-Permian Mass Extinction at this time52. The temporal relationship between the occurrence of the oldest marine reptile fossil and obliquity amplication (Phase 4) and the appearance of multi-clade marine reptiles during the subsequent change in the nature of the eccentricity modulation (Phases 56), temporally linked to the nal phase of a two-step decrease in seawater 13CDIC, indicates a mechanistic link between the appearance and diversication of the marine reptiles and the major change in ocean structure and carbon cycling. We attribute the biotic recovery and initiation of a new marine ecosystem to the nal breakdown of ocean stratication and the onset of a high-latitude deep-water source, which would have enhanced ventilation of the deep ocean. Together these changes in ocean structure would have stimulated surface ocean primary productivity promoting the diversication of the marine reptiles. They further suggest that reptiles may have rst invaded Panthalassa in the middle Spathian in response to this reorganization.

Marine reptiles introduced a new pattern of shallow marine nutrient circulation in the Early Triassic that may have played a critical role in the post-extinction build-up of the marine ecosystem, by feeding at various depths and defecating near the sea surface52. The post-extinction recovery of the forest ecosystem in the middle Spathian is contemporaneous with that of the marine ecosystem56,57 as would be anticipated if changes in ocean circulation were driven by climate amelioration. Ultimately, stabilization of oceanic conditions in the Early Triassic, which involved a change in the response of carbon cycling to astronomical forcing, likely accelerated the building of the new Meso-Cenozoic marine ecosystem.

In summary, the rst occurrence of the Mesozoic marine reptiles is approximately coincident with a shi in astronomically-paced marine carbon cycling, and a ~2% shi in seawater DIC, which indicates that the South China seas remained inhabitable to large air-breathing marine predators following the end-Permian Mass Extinction until a major rearrangement of oceanic circulation. This change led to intensied ventilation and restored well-oxygenated conditions, which is mechanistically linked to astronomically driven changes in C cycling between Earths surface reservoirs. The distribution of diversied marine reptiles along the coasts of the Panthalassan Sea in the late Spathian54 was likely fueled by the climate amelioration, changing ocean structure, and increased surface ocean primary productivity in the middle Spathian. The same factors may have encouraged reptiles to invade the sea. Ultimately, stabilization of oceanic conditions in the Early Triassic may have involved climate-life interactions in which a change in the astronomical pacing of climate and carbon cycling among the Earths surface carbon reservoirs accelerated the building of the new Meso-Cenozoic marine ecosystem.

Methods

Carbonate samples were collected and analyzed at a spacing of ~510 kyr from the Majiashan section, Chaohu spanning the late Smithian to Spathian in the Isotope Lab of Nanjing Institute of Geology and Paleontology,

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Chinese Academy of Sciences with an analytical precision of <0.03%. 18Ocarb, 13Ccarb 13Corg with an analytical

precision of <0.1% and wt.% CaCO3 of microdrilled samples were generated in the Stan Margolis Stable Isotope Lab, UC Davis. The 13Ccarb data were prepared and analyzed in the R soware package Astrochon (Meyers, 2014; R Core Team, 2015).

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Acknowledgements

The study was enabled by grants from the Project 40920124002 and 41372016 from the National Natural Science Foundation of China to D.-Y.J., Project 123102 from State Key Laboratory of Palaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, CAS) to D.-Y.J., Project 20120001110072 from the Research Fund for the Doctoral Program of Higher Education to D.-Y.J., National Geographic grant ( Grant number 8669-09) to R.M. and an exchange scholar grant from the China Scholarship Council (CSC) to W.-L.F. The participation of I.P.M was supported by National Science Foundation award EAR-1024737. S.R.M acknowledges support from U.S. National Science Foundation award EAR-1151438, which funded his participation in this project, and also supported the 2014 IsoAstro Geochronology Workshop that W.-L.F. attended.

Author Contributions

D.-Y.J., R.M. and A.T. conceived the study and supervised the sample collections. W.-L.F. participated in the sample collections, ran all geochemical and times-series analyses, drew all figures, and wrote the initial manuscript. D.-Y.J. supervised the relevant sample analysis and data collection, and revised the manuscript; I.P.M. supervised the geochemical analyses at UC Davis and the interpretations; S.R.M. supervised the cyclostratigraphic analysis and age model development. All authors (W.-L.F., D.-Y.J., I.P.M., S.R.M., R.M. and A.T.) contributed to the interpretation of the results and the writing of the nal manuscript.

Additional Information

Supplementary information accompanies this paper at http://www.nature.com/srep

Competing nancial interests: The authors declare no competing nancial interests.

How to cite this article: Fu, W. et al. Eccentricity and obliquity paced carbon cycling in the Early Triassic and implications for post-extinction ecosystem recovery. Sci. Rep. 6, 27793; doi: 10.1038/srep27793 (2016).

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