Substantial Vegetation Response to Early Jurassic Global Warming with Impacts on Oceanic Anoxia
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ARTICLES https://doi.org/10.1038/s41561-019-0349-z Substantial vegetation response to Early Jurassic global warming with impacts on oceanic anoxia Sam M. Slater 1*, Richard J. Twitchett2, Silvia Danise3 and Vivi Vajda 1 Rapid global warming and oceanic oxygen deficiency during the Early Jurassic Toarcian Oceanic Anoxic Event at around 183 Ma is associated with a major turnover of marine biota linked to volcanic activity. The impact of the event on land-based eco- systems and the processes that led to oceanic anoxia remain poorly understood. Here we present analyses of spore–pollen assemblages from Pliensbachian–Toarcian rock samples that record marked changes on land during the Toarcian Oceanic Anoxic Event. Vegetation shifted from a high-diversity mixture of conifers, seed ferns, wet-adapted ferns and lycophytes to a low-diversity assemblage dominated by cheirolepid conifers, cycads and Cerebropollenites-producers, which were able to sur- vive in warm, drought-like conditions. Despite the rapid recovery of floras after Toarcian global warming, the overall community composition remained notably different after the event. In shelf seas, eutrophication continued throughout the Toarcian event. This is reflected in the overwhelming dominance of algae, which contributed to reduced oxygen conditions and to a marked decline in dinoflagellates. The substantial initial vegetation response across the Pliensbachian/Toarcian boundary compared with the relatively minor marine response highlights that the impacts of the early stages of volcanogenic global warming were more severe for continental ecosystems than marine ecosystems. he Early Jurassic Toarcian Oceanic Anoxic Event (T-OAE; Land ecosystem impacts ~183 million years ago, Ma) is characterized by a period of The Pliensbachian (pre-T-OAE) vegetation, based on the palynol- rapid global warming (in the region of ~6.5 °C)1, marine ogy of the studied section, was dominated by conifers/seed ferns T 2–5 6–9 mass extinction and oceanic oxygen deficiency , reflected in (represented by bisaccate pollen) alongside abundant wet-adapted the widespread deposition of organic-rich black shales10. The event ferns and lycophytes (club mosses) (Fig. 2). The first marked is also associated with a major negative carbon isotope excursion change in the spore–pollen assemblages (see Supplementary (CIE)11 lasting about 300,000–500,000 yr (refs. 12,13), signifying a Fig. 2 for selected taxa) is recorded across the Pliensbachian/ massive release of isotopically light carbon into the atmosphere. Toarcian boundary, as shown by the non-metric multidimensional Proposed causal mechanisms include elevated CO2 flux driven by scaling ordination (nMDS; Fig. 3), where Pliensbachian samples emplacement of the Karoo–Ferrar large igneous province (LIP) plot at a distance from Toarcian ones indicating a notably different in the Southern Hemisphere, and the release of thermogenic and/ taxonomic composition. Overall richness and diversity dropped at or biogenic methane1,14–21. Efforts to understand the biological the onset of the Toarcian (Fig. 2). Bisaccate pollen, produced by consequences of this event have hitherto primarily focused on conifers and seed ferns, reduced markedly in abundance, mirrored marine ecosystems, and responses include the temporary and/or by an increase in Classopollis and Chasmatosporites, produced by complete disappearance of marine plankton groups (such as dino- cheirolepid conifers and cycads27, respectively (both of which are flagellates)22,23, and widespread extinction among higher trophic warm/dry environmental indicators28). Palynological data from the groups of marine invertebrates2–5,24–26. Few studies have addressed Polish Basin also record a reduction in bisaccate pollen through the effects of the Toarcian event on land-based ecosystems; here the T-OAE interval, suggesting that this may be a widespread sig- we examine the rich fossil archives of spores and pollen (derived nal29. The pre-CIE proliferation of warm-adapted plants and the from land plants) in association with marine plankton to assess the decline of wet-adapted ferns and lycophytes through the Yorkshire impact on terrestrial environments and test links between continen- section suggest that the climate had already substantially warmed tal and marine ecosystem changes. before the CIE (Fig. 4). One of the most complete and well-preserved Pliensbachian– During the CIE, spore–pollen richness and diversity decreased Toarcian sequences is found in Yorkshire, UK11 (Fig. 1, considerably (Fig. 2), signifying substantial losses amongst the ter- Supplementary Fig. 1). The succession was deposited in a marine restrial vegetation and the presence of highly depauperate floral shelf setting, allowing us to directly link the terrestrial vegetation, communities. Throughout this episode, bisaccate pollen-producers represented by abundant wind- and water-transported spores and underwent a second decline in abundance and were replaced by pollen, and marine plankton signals in the same samples. We ana- cheirolepid conifers (Fig. 2). In the latter half of the CIE, we recorded lysed 54 samples taken from an 85 m section spanning the T-OAE. a sudden and prominent abundance peak in Cerebropollenites mac- The dataset comprises 40,014 spore, pollen and marine plank- roverrucosus (Fig. 2, Supplementary Fig. 2), probably produced by an ton occurrences, and 28,141 palynofacies particles (see Methods extinct relative of the extant conifers hemlock (Tsuga)30 or Japanese for details of the palynofacies analysis; raw data are provided in umbrella-pine (Sciadopitys)31. High abundances of Cerebropollenites Supplementary Data 1 and 2). Changes in fossil assemblages are have been recorded from early Toarcian successions of Greenland32, summarized in Fig. 2. suggesting that this was a widespread floral response. Interestingly, 1Department of Palaeobiology, Swedish Museum of Natural History, Stockholm, Sweden. 2Department of Earth Sciences, The Natural History Museum, London, UK. 3Dipartimento di Scienze della Terra, Università degli Studi di Firenze, Florence, Italy. *e-mail: [email protected] NATURE GEOSCIENCE | www.nature.com/naturegeoscience ARTICLES NATURE GEOSCIENCE a N 58° N SaltwickBay Study area Kettleness 54° N Staithes Whitby Port Mulgrave 54°30′ N Runswick Bay 1 km 4° W 0° 0°40′ W b Europe Asia North America Tethys South Africa Ocean America Pangaea Australia Antarctica 500 km Fig. 1 | Location of the study area and palaeogeographic maps of the early Toarcian. a, Sample localities from the North Yorkshire coast, UK. b, Palaeogeographic maps of the early Toarcian; the red star marks the study area. Grey areas represent land; blue areas represent seas. Credit: Maps adapted from ref. 24, Geological Society of America; ref. 25, PLOS (a); ref. 43, SpringerNature Ltd (b, global); ref. 60, Elsevier (b, European and global). C. thiergartii, an ancestral or sister species to C. macroverrucosus, event. Samples from the post-CIE part of the Mulgrave Shale is a marker species for the Triassic/Jurassic boundary, where it Member strongly overlap with samples from the CIE interval. This first appears at the CIE peak and maximum atmospheric CO2 lev- indicates that vegetation during the CIE was more similar to post- els in the aftermath of that mass extinction33. The proliferation of CIE floras than pre-CIE floras. When samples are labelled according Cerebropollenites during multiple past hyperthermal events suggests to their lithologies (Supplementary Fig. 3), laminated mudstones that the source plants were adapted to hot, arid climates and/or dis- display some clustering relative to other samples; however, there is turbed settings that would have occurred during these episodes of relatively weak grouping of lithologies in the nMDS plot, suggesting ecological turnover. that temporal shifts in assemblages are not dominantly controlled Following the CIE, floral richness and diversity rebounded rap- by lithology but represent actual changes in parent vegetation. idly (Fig. 2), and Cerebropollenites-producers returned to pre-event abundances, signifying a short-lived (estimated at <250,000 years Marine ecosystem impacts based on the duration of the CIE12,13) but substantial floral response Our sample set, derived from a marine shelf setting, also provides (Figs. 2, 4). Terrestrial vegetation returned to its pre-event richness insights into marine ecosystem changes. Abundances of dinoflagel- and diversity but not to its pre-CIE composition, indicating a turn- late cysts and spiny acritarchs declined markedly at the onset of the over in floral communities. Cupressaceae and Cheirolepidaceae CIE, and were replaced by a substantial increase in sphaeromorphs apparently filled the niches previously occupied by bisaccate (Fig. 2, Supplementary Fig. 2). These sphaeromorphs, which co- pollen-producers before the Toarcian event. Perinopollenites- occur with abundant amorphous organic matter (AOM), are com- producers, which are indicators of wet environments34, gradually parable to the prasinophyte algae Halosphaeropsis liassica, a marker increased in abundance following the CIE, whereas arid-adapted taxon for the T-OAE35. The prasinophyte Tasmanites also increased cycads declined, signifying a return to a more temperate climate in abundance at the onset of the CIE, reflecting an overhaul of the following the event. ‘normal’ marine ecosystem. These shifts in abundance are accom- In the nMDS plot (Fig. 3), samples group according to their panied by a major increase in AOM (Fig.