Cuticle surfaces of fossil plants as a potential proxy for volcanic SO2 emissions: observations from the Triassic–Jurassic transition of East Greenland
Flood basalt volcanism has been implicated in several episodes of mass extinctions and environmental degradation in the geological past, including at the Triassic–Jurassic (Tr–J) transition, through global warming caused by massive outgassing of carbon dioxide. However, the patterns of biodiversity loss observed are complicated and sometimes difficult to reconcile with the effects of global warming alone. Recently, attention has turned to additional volcanic products as potential aggravating factors, in particular sulphur dioxide (SO2). SO2 acts both directly as a noxious environmental pollutant and indirectly through forming aerosols in the atmosphere, which may cause transient global dimming and cooling. Here, we present a range of morphological changes to fossil plant leaf cuticle surfaces of hundreds of Ginkgoales and Bennettitales specimens across the Tr–J boundary of East Greenland. Our results indicate that morphological structures of distorted cuticles near the Tr–J boundary are consistent with modern cuticle SO2-caused damage and supported by recent leaf-shape SO2 proxy results, thus identifying cuticle surface morphology as a potentially powerful proxy for SO2. Recording the timing and duration of SO2 emissions in the past may help distinguish between the driving agents responsible for mass extinction events and thus improve our understanding of the Earth System.
KeywordsFossil plant cuticle Sulphur dioxide End-Triassic mass extinction Camp Ginkgoales Bennettitales SO2 proxy Flood basalt volcanism Triassic–Jurassic boundary
The Triassic–Jurassic (Tr–J) boundary ca. 201.6 Ma (Blackburn et al. 2013) is marked by a transition of severe environmental degradation, as well as extensive marine and terrestrial mass extinctions, referred to collectively as the end-Triassic mass extinction (ETE), one of the “big five” Phanerozoic mass extinctions (Sepkoski 2002; McElwain et al. 2007; Benton 2008; Richoz et al. 2012; Steinthorsdottir et al. 2012; Petterfy et al. 2016). The emplacement of the Central Atlantic Magmatic Province (CAMP) is increasingly recognised as the main driver of the Tr–J events, through massive outgassing of CO2, recorded by stomatal densities and isotopes (McElwain et al. 1999; Hesselbo et al. 2002; Whiteside et al. 2010; Bacon et al. 2011; Schaller et al. 2011; Steinthorsdottir et al. 2011b), perhaps additionally accompanied by methane release (Pàlfy et al. 2001; Beerling and Berner 2002; McElwain et al. 2007). The consequent global warming drove degradation and disruption of ecosystems as well as large-scale biodiversity loss on land and in the oceans (Rampino 2010; Steinthorsdottir et al. 2012; Lindström 2016; van de Schootbrugge and Wignall 2016), but CAMP duration and timeline of eruption events are still debated (McHone 2002; Marzoli et al. 2004; Nomade et al. 2007; Williford et al. 2007; Ruhl et al. 2009; Schoene et al. 2010; Marzoli et al. 2011; Blackburn et al. 2013).
It is known that in addition to CO2, extrusive volcanism releases significant amounts of other gasses, including considerable amounts of sulphur dioxide (SO2) (Thordarson et al. 2001; Thordarson and Self 2003; Richoz et al. 2012). SO2 is directly damaging to vegetation in both gaseous form and in particular when combining with water and precipitating as acid fog and rain (H2SO4) (Haines et al. 1985; Cape 1993; Kim et al. 1997; Jagels et al. 2002). SO2-induced damage can include decreased leaf production/leaf area (Pande and Mansfield 1985; Bacon et al. 2013), changes to leaf function (Darrall 1986; Dhir et al. 2001; Shepherd and Wynne Griffiths 2006), as well as scarring of plant leaf cuticle and/or stomatal damage (Shepherd and Wynne Griffiths 2006; Bytnerowicz et al. 2007; Bartiromo et al. 2012; Elliott-Kingston et al. 2014). Additionally, SO2 forms tiny particles in the atmosphere, so-called aerosols, which may not only temporarily mask the effects of global warming, but also lead to devastating effects on ecosystems, mainly through causing transient global dimming and/or cooling (Thordarson and Self 2003; Storelvmo et al. 2016). During the emplacement of CAMP, recurring volcanic eruptions may have led to repeated episodes of atmospheric pollution and dimming, compounding the destabilisation of ecosystems. The negative effects of SO2 have been invoked as part of the explanation for environmental upheaval recorded across the Tr–J boundary, including the ETE events. This includes circumstantial evidence such as the severe terrestrial vegetation shifts and floral biodiversity losses, the increased abundance of spores and microbes, and a sometimes observed decoupling between marine and terrestrial biotic recovery (McElwain et al. 2007; van de Schootbrugge et al. 2009; Lindström et al. 2012, 2015; Mander et al. 2013; Bond and Wignall 2014; Lindström 2016; Petterfy et al. 2016). SO2 is thus considered to be a potentially important factor in contributing to the ETE as well as other flood basalt-induced mass extinctions in the past. It would therefore be greatly beneficial to develop reliable proxies to reconstruct SO2 emissions across mass extinction boundaries and at other times of significant environmental upheaval in the geological record. Such proxies would aid in separating the effects of SO2 and CO2 to further our understanding of climate sensitivity and thus allow improved predictions of the effects of future climate change by comparing to past global warming and mass extinction events (Bytnerowicz et al. 2007; Storelvmo et al. 2016).
In an effort to address the need for SO2 proxies, two studies have recently explored the possibility of detecting SO2 in the past, one through studying fossil leaf shape across the Tr–J boundary (Bacon et al. 2013) and another through investigating the effects of SO2 on the cuticle structure of modern “nearest living equivalents” (modern plants that are analogous to their fossil equivalents in terms of taxonomy, morphology and/or ecology) of Mesozoic plants (Elliott-Kingston et al. 2014). Bacon et al. (2013) identified a physiognomic marker in plant leaves exposed to SO2 in controlled-environment experiments and found the same physiognomic response of increased leaf roundness in fossil leaves of multiple taxa preserved across the Tr–J boundary in East Greenland. The authors identified a stepped response of different species over time – that is, some plant fossils expressed an increase in roundness before others. Taxa became rounder than previously in the beds leading up to the Tr–J transition, when SO2 emissions due to CAMP volcanic activity are considered increasingly likely. These same taxa then decreased significantly in abundance locally, before either recovering with less round leaves after the Tr–J transition, or becoming locally extinct. Importantly, the order of response mirrored that predicted by nearest living equivalent taxa of Mesozoic plants exposed to simulated palaeo-atmospheric treatments (see fig. 5, Bacon et al. 2013). Elliott-Kingston et al. (2014) subsequently also exposed several different nearest living equivalent taxa to high levels of SO2 in controlled environment experiments and identified a range of cuticle damage features that are linked to exposure to SO2 in extant plants. These damage features included changes in surface waxes, blistering, collapsed epidermal cells and stomatal complex distortion, giving the impression of ‘disorganised’ and ‘distorted’ cuticle surfaces.
Plant cuticles are very resistant polymeric structures with high preservation potential, and are already in wide use as proxies, e.g. for atmospheric CO2 concentrations (pCO2) via their stomatal densities (Woodward 1987; Beerling et al. 1998; McElwain 1998; Barclay et al. 2010; Steinthorsdottir et al. 2014; Steinthorsdottir and Vajda 2015,, Steinthorsdottir et al. 2016a, Steinthorsdottir et al. 2016b). The high preservation potential of plant cuticles as fragments in sediments, often when macrofossils are not available (Steinthorsdottir et al. 2011a,b), make them an attractive target for attempting to develop an SO2 proxy. While analysing hundreds of leaves and leaf fragments for use in pCO2 reconstruction, it was observed clearly that cuticle surfaces from certain sedimentary plant beds, particularly those close to and at the Tr–J boundary, appeared significantly more ‘messy’, with disorganised cell arrangement and increased surface textures – features referred to collectively as ‘distorted’ cuticles. Although this was observed with interest at the time, there was no clear indication of what may have caused the distortion. We note that the original study was not designed in order to develop an SO2 proxy and that future studies with the specific aim of investigating SO2 proxies will enable the proper quantification of the potential proxy outlined below. The development of such a proxy requires statistical scoring of morphological features interpreted to be caused by SO2 pollution and further analyses of cuticular morphology, including studying cross sections, measuring thickness and ultrastructure, and analysis with transmission electron microscopy (TEM) of the substomatal cavity, far beyond the scope of the current report.
The aim of this study is to preliminarily explore whether cuticle surface morphology has the potential to serve as a new palaeo-SO2 proxy. We tested the hypotheses that (1) distorted cuticles will display similar morphology to cuticles exposed to SO2 in the experiments of Elliott-Kingston et al. (2014); and (2) distorted cuticles will dominantly occur in the sedimentary beds where Bacon et al. (2013) identified increased leaf roundness.
Over all, the fossil flora at Astartekløft shows an 85% turnover rather than extinction of taxa at the Tr–J boundary, where minor components of the Triassic flora become dominant components of the Jurassic flora and vice versa (Harris 1937; McElwain et al. 2007). In-depth studies of vegetational and biogeochemical changes at Astartekløft show that diversity loss began to take place before the deposition of bed 3 and persisted until after the deposition of bed 6 (McElwain et al. 2009; Steinthorsdottir et al. 2011b; Mander et al. 2013), reflecting the complex pattern of CAMP-driven global change. Correlation and comparison with additional Tr–J transition sequences worldwide suggest that peak extinction in Astartekløft’s bed 5 (where the actual Tr–J boundary is located) probably reflects a biological tipping point brought about by the long-term cumulative effect of CAMP emplacement (e.g. Bonis and Kürschner 2012; Lindström et al. 2012; Mander et al. 2013).
Bennettitales and Ginkgoales, the two taxa studied here, are both among the most commonly preserved plant fossils and are uniquely present together in most of the beds. Bennettitales are far more abundant pre- Tr–J boundary, with abundance declining significantly across the Tr–J boundary and the group going locally extinct before bed 8 is deposited. Ginkgoales are rarer components of the flora before the Tr–J boundary, except in bed 2, but become ecologically dominant after the transition (McElwain et al. 2007, 2009). Some key differences in the composition of the macroflora and cuticle database include the strong presence of various conifers in the macroflora, including e.g. the broadleaf conifers Podozamites and Elatocladus, which are abundant in several beds throughout the section, but absent or near-absent as dispersed cuticles. This discrepancy between the macrofossil and cuticle records is likely due to the conifers in question having thin leaf cuticle, which does not preserve well (Harris 1932). Contrastingly, Ginkgoales are not present in bed 5 as macrofloral remains but cuticle fragments from Ginkgoales taxa are clearly identified in this bed. This raises the possibility that proxies for SO2 that focus exclusively on either plant macrofossils or dispersed cuticle will not alone provide a clear signal of the presence or strength of SO2 in the fossil record.
Material and methods
The database analysed here consists of more than 1200 cuticle images of 95 Ginkgoales (Ginkgoites, Baiera and Sphenobaiera) and 82 Bennettitales (Anomozamites and Pterophyllum), both from entire leaf specimens and dispersed cuticles extracted from bulk samples across the Tr–J boundary. The fossil plants have been classified to genus-level based on macrofossils, whereas the cuticle morphology is very similar between the genera within Ginkgoales and Bennettitales respectively, preventing classification below order-level for the dispersed cuticles; therefore all cuticles are lumped together in these two taxonomic groups. Each studied cuticle specimen was photographed 5–10 times, with images distributed evenly across the cuticle surface, at ×200 magnification using a mounted Leica camera (Leica DM 2500 with epifluorescence module Leica eqb-100) and Auto-Montage Pro (©Synoptics, version 5.03.0061). For a complete list of the specimen database, including specimen numbers, details of sample processing and data previously collected, see Steinthorsdottir et al. (2011b). The image database was analysed visually and the various structures observed scored for frequency and co-appearance between the two studied plant groups. The database is hosted by the UCD Plant Palaeoecology and Palaeobiology Group, University College Dublin, Ireland.
Morphology of cuticle surfaces interpreted as SO2 fumigation response
The morphological range and type of distortion observed on the fossil plant cuticle surfaces will be of a similar type to that observed in SO2 fumigation experiments on extant plants.
Distorted cuticles will be dominantly identified in the same beds as the roundest leaves (beds 4–6) and will be rare or absent in the other beds, where less evidence for SO2 has been identified.
Schematic overview of cuticle features believed to be potential SO2 proxies. Cuticle surface features are scored separately for both plant groups in each stratigraphic plant bed through the Tr–J transition at Astartekløft, East Greenland. Legend: • = Cuticle present, undistorted; # = disorganised epidermal cell arrangement, surface etching; ≈ = cuticle folding, ridging, bulging; − = Cuticle/ plant group absent. Bold denotes strong presence of the reported features. Interpreted strength of SO2 pollution: Open image in new window = minimal or absent; Open image in new window = moderate; Open image in new window = severe. Macrofossil abundance from (McElwain et al. 2007; table 3)
Fidelity of the cuticle database
The extensive cuticle database studied here comprises a large selection of epidermal surface images of almost 200 fossil Ginkgoales and Bennettitales specimens across the Tr–J boundary, and thus illustrates in detail the range of morphologies found in each group within each bed. However, the cuticle specimens were originally selected based on best preservation (for optimal pCO2 reconstruction, see Steinthorsdottir et al. 2011b) and it was therefore not possible to construct a rigorous statistical analysis, rendering the results presented here somewhat qualitative. Due to the database design, the likelihood of observing distorted cuticles is less in some beds than if indiscriminate observation of randomly chosen specimens had been the original selection goal. This nonetheless strengthens the findings because, despite the original criteria of best-preserved cuticles, distorted cuticles are still a common presence in the database and identified in increasing abundance at the Tr–J boundary, best illustrated by all cuticles in beds 5 and 6 being distorted. Evidence of a small proportion of additional distorted cuticles may thus have been overlooked in some beds, particularly beds 1, 1.5, 7 and 8, but this in turn highlights the overwhelming proportion of distorted cuticles in the other beds. We therefore consider the fidelity of the database regarding mapping the occurrence of distorted cuticles across the Tr–J boundary to be high.
Comparison of Tr–J transition fossil cuticles to modern cuticles from simulated palaeoenvironment experiments
It was hypothesised that cuticle distortion observed in the fossil cuticle database would be similar to that observed in SO2 fumigation experiments, and the analysis of the fossil cuticles from Astartekløft clearly revealed numerous morphological distortion characteristics analogous to those identified on modern plant cuticles by Elliott-Kingston et al. (2014). In a study on the impact of continuous sulphur dioxide (SO2) exposure for 6 months at 0.2 ppm on modern plant leaf surfaces, Ginkgo biloba interveinal leaf tissue and stomatal subsidiary cells collapsed under continuous SO2 fumigation whereas stomatal papillae remained intact (Elliott-Kingston et al. 2014). Similar morphological changes are evident in the fossils in this study from bed 2 (Fig. 3e). Elliott-Kingston et al. (2014) also showed elevated areas of damaged leaf tissue as a result of SO2 exposure. In some cases this took the form of epidermal cells with overlying cuticle raised up into circular ‘bulges’; in others, areas of epidermal cells had collapsed below leaf surface level, which may have resulted from the bulges subsequently collapsing. In addition, the authors showed leaf areas with cuticle (without the underlying epidermal cells) raised up into ‘bubbles’ that subsequently burst. This epidermal and cuticle distortion stretched the cells, resulting in the enlarged tissue folding and forming ridges when it burst or collapsed. Folding and ridging are prominent features of the fossil cuticles (Fig. 3e–f; Fig. 5e–f; Fig. 9c–e) and although raised bulges and blistering are not directly observable on fossil cuticles, possibly due to epidermal cell degradation, and cell and cuticle compression during fossilisation, the ‘disorganised’ epidermal cell arrangement sometimes noted may be the observable product of SO2 fumigation.
Nguyen Tu et al. (1998) showed that a Cenomanian (c.100–94 Ma) fossil Ginkgoales, Eretmophyllum andegavense, still contained wax compounds, thus waxes may still be observable as part of the surface structure on fossil cuticles. Elliott-Kingston et al. (2014) also showed cuticular wax degradation in all species that produced new leaves under SO2 fumigation. In many species, surface waxes appeared thicker due to excessive wax production or degradation of individual wax structures that subsequently combined into a less structured mass (Bartiromo et al. 2012; Elliott-Kingston et al. 2014). The fossil cuticles appear to show production of extra cuticular wax in some cases (e.g. Fig. 3e; Fig. 5f; Fig. 9e). Taken together, exposure of modern plant leaves to SO2 fumigation resulted in a less organised cuticle surface, with clearly visible alterations in wax structure, which is comparable to many of the fossil cuticles.
Comparison of fossil cuticle distortion to macro-leaf physiognomy across the Tr–J boundary
It was hypothesised that fossil cuticle distortion, potentially caused by elevated atmospheric SO2, would be observed in the same beds as the roundest fossil leaves described by Bacon et al. (2013). In addition, increased leaf roundness was observed in several taxa – selected to be nearest living equivalents for abundant taxa at Astartekløft – that were exposed to simulated palaeoatmospheric conditions designed to mimic the Tr–J transition atmospheric conditions in controlled environment experiments (Bacon et al. 2013). Increased leaf roundness was observed when the plants were exposed to SO2 and a similar increase in leaf roundness was observed in fossil taxa in beds that correspond to the time of most likely CAMP activity and thus highest atmospheric SO2 levels across the Tr–J boundary. The physiognomic responses of fossil Ginkgoales and Bennettitales to atmospheric SO2 (see Fig. 4; Bacon et al. 2013) and the relative abundance of each plant group through the section (McElwain et al. 2007) can be briefly summarised as follows. Ginkgoales are rare in most Rhaetian sediments at Astartekløft, but Bacon et al. (2013) interpreted increased leaf roundness already by bed 2 as a response to SO2. Thereafter, Ginkgoales become extremely rare, almost to the point of local extinction, until the Hettangian bed 7, after which they become the dominant vegetation component at Astartekløft. Bennettitales leaves are abundant in Rhaetian sediments but show no physiognomic response until bed 4, (Bacon et al. 2013) when they become much rounder than leaves in previous beds. Bennettitales then decline sharply in abundance through to bed 7, after which they are entirely absent from the sediments.
A unique benefit of the cuticle analysis, compared to the leaf physiognomy analysis, is that cuticles of both plant groups are present in multiple beds across the Tr–J boundary, whereas e.g. Ginkgoales macrofossils are absent in beds 1.5, 3, 4, and 5. Contrastingly, Podozamites macrofossils are present in all beds except bed 7, whereas no Podozamites cuticle is found. The cuticle of Podozamites has been classified as particularly thin (Harris 1935) and no examples were recovered when bulk material was macerated to extract cuticles. However, this group is well-represented in the leaf macrofossil record and shows a significant increase in leaf roundness in bed 5, where some of the most distorted cuticles for other taxa are identified. Thus, the two approaches together show the most powerful evidence for the presence and effects of SO2 across the Tr–J boundary. The cuticle analysis agrees with the leaf physiognomy analysis, thereby increasing confidence in both methods. Furthermore, the cuticle analysis method adds an additional independent line of evidence of plant responses across the Tr–J boundary, suggesting that SO2 remained an active environmental pressure across the entire transition (beds 2/3 to 6; Fig. 11), when macrofossils of Ginkgoales and Bennettitales are absent. Importantly, the cuticle SO2 proxy provides the possibility of recognising times when plants were most exposed to SO2 and/or which plants were most stressed by SO2, by recording SO2-induced distortion in cuticle fragments when macrofossils may not be available.
Cause of cuticle morphological changes: Volcanic gasses or taphonomy?
Fossil vegetation records the environmental degradation typically accompanying mass extinction events e.g. by changes in community composition, abundance and diversity (McElwain et al. 2007, 2009). Plants do not, however, respond to mass extinctions in the severe manner fauna generally does, with comparatively few genera going extinct (McElwain and Punyasena 2007; Vajda and Bercovici, 2014). This makes it possible to track the responses of plant groups across mass extinction events because members of the same genus are likely to be found before, during and after the events. This resilience makes plants more useful tools than terrestrial fauna for mapping changes in the palaeo-environment and ecosystems. There is very little change in taphonomic conditions in the first six beds (beds 1–5), with well-preserved cuticles and macrofossils found in all of the beds. These beds are isotaphonomic in terms of deposition environment, whereas beds 6–8 were deposited in slightly different environment. Upchurch et al. (2007) surmised that cuticle distortion can be a function of either poor preservation and/or processing. Preservation is unlikely to account for the distortion observed here, due to the taphonomic factors already discussed that provide nearly homogenous preservation potential across the beds. Cuticle distortion is also considered unlikely to have occurred during processing, due to the observation of identical distortion on both intact non-processed and macerated cuticles from the same beds. Additionally, the preservation, in some cases, of both sides of the leaf cuticle envelope in processed cuticle fragments discounts the possibility that thin cuticle sheets were merely creased or otherwise distorted during processing.
The only major conditions that are predicted to change are those related to atmospheric composition, particularly (i) pCO2, and (ii) SO2 due to volcanic gas emissions, as well as an accompanying fire activity spike in bed 5 (Belcher et al. 2010). Concentrations of CO2 rise across the Tr–J boundary (Steinthorsdottir et al. 2011b) to peak in bed 6. It is unlikely that this atmospheric composition change would negatively affect preservation potential across the boundary, because higher pCO2 is predicted to increase leaf preservation potential (Bacon et al. 2016). The fire spike in bed 5 (Belcher et al. 2010) is recorded by a major increase in fossilised charcoal, but there is no noticeable decline in the quality of preservation of fossil plant material (leaf or cuticle), with more individual leaf fossils excavated from this bed than any other for the same volume of rock (McElwain et al. 2007). The only observable changes in fossil preservation are those related to SO2 activity. Leaf roundness peaks in bed 5 for the Bennettitales genera, Anomozamites and Pterophyllum (they are absent as macrofossils in bed 6), as well as for two conifer genera, Elatocladus and Podozamites (Bacon et al. 2013), and all cuticles extracted from beds 5 and 6 are distorted. Given that no other significant changes are observed, particularly in the isotaphonomic beds 1–5, the observed alterations to mean leaf shape and cuticle morphology are highly likely to be driven by exposure to SO2 and not by taphonomic changes.
Potential influence of SO2 on the palaeo-pCO2 proxy
The geologically sudden elevation of pCO2 and the concomitant temperature increases are considered the primary drivers of many mass extinction events. Proxies to investigate both have been available for decades, making the assessment of changing atmospheric pCO2 and temperature across mass extinction boundaries increasingly available, with the stomatal proxy being the most important terrestrial palaeo-pCO2 proxy in use (Woodward 1987; McElwain 1998; Roth-Nebelsick 2005; Beerling and Royer 2011). With the emergence of potential additional proxies for SO2, it is important to understand whether the presence of volcanic SO2 in the past may influence stomatal density based palaeo-pCO2 reconstructions. Previous studies on plant SD/SI responses when subjected to naturally elevated levels of SO2 in the vicinity of volcanic vents have been inconclusive, reporting decreased SI (Tanner et al. 2007) and SD (Ali et al. 2008), as well as no SD/SI response (Bettarini et al. 1997; Haworth et al. 2010) when compared to non-fumigated plants. The lack of SD/SI response was interpreted to potentially be the result of developmental resistance to SO2 fumigation by Haworth et al. (2010), who subsequently conducted a series of growth chamber experiments on several fossil-equivalent plant species with no prior exposure to SO2 (Haworth et al. 2012). Exposure to high pCO2 in combination with SO2 fumigation produced a variety of SD and SI responses between the plants, with SD increasing significantly in about half the plant species, as well as very variable SI responses, including a large SI increase in Ginkgo biloba (Haworth et al. 2012). However, all species showed an increase in the ratio between SD and SI (SD:SI), implying this ratio could be used to help detect SO2 responses recorded by plants in the geological record and that this effect could cause the underestimation of pCO2 using the stomatal method on material exposed to SO2 in the past.
Haworth et al. (2012) then tested this assumption using the data of Steinthorsdottir et al. (2011b) by plotting the SD:SI ratio of Ginkgoales fossil leaves across the Tr-J of Astartekløft, East Greenland, thus using the same cuticle database that we here investigate for potential SO2 damage, and found a very significant increase (>100%) in the SD:SI ratio in bed 6. Although the increase in SD:SI as an SO2 indicator in bed 6 is consistent with our observations of high levels of cuticle distortion, as well as with the highest reconstructed pCO2 (Steinthorsdottir et al. 2011b), there are important differences. The fossil Ginkgoales record a significant SI decrease in bed 6, in contrast to the large SI increase recorded by G. biloba under the Tr-J equivalent experimental conditions (high pCO2, high SO2) (Haworth et al. 2012).Therefore, pCO2 reconstructed across the Tr-J cannot be interpreted to be underestimated based on these experimental results. In addition, fossil Bennettitales record essentially parallel levels and variations of pCO2 to Ginkgoales across the Tr-J (Steinthorsdottir et al. 2011b), as well as illustrating the high levels of cuticle distortion reported here, but do not show an increased SD:SI ratio in bed 6, or any other bed across the Tr-J (see supplementary information S1). The very high variability in the response of SD and SI to various combinations of natural and experimental fumigation of SO2 as well as pCO2 needs to be further investigated. Although SD and SI often respond in parallel, changes in SD may be directly related to e.g. changes in leaf expansion, whereas SI is recognised as the more reliable recorder of atmospheric pCO2, the most important plant substrate (Salisbury 1928). It is thus advisable that the SD:SI ratio be recorded when reconstructing pCO2 in order to detect any deviation from the parallel response, with the potential to identify the presence of SO2 or other detrimental environmental pollutants in the past, and to evaluate any potential influence on stomatal proxy derived pCO2 (Haworth et al. 2012).
Significance of SO2 proxies for interpreting the fossil record
Despite linking large igneous province volcanism to three of the ‘big 5’ mass extinctions (the end-Permian, end-Triassic, and end-Cretaceous) the lack of detailed proxies mean that, although estimates of the volume of volcanic emissions (including pCO2 and SO2) can be made (e.g. Schmidt et al. 2016), the direct impact of these emissions on the environment and particularly the role of SO2 in causing or adding to the severity of mass extinctions has been difficult to determine. The development of SO2 proxies offers a means to begin to address this problem. It is important to understand the role of SO2 in mass extinction events so that we can fully interpret these major events in Earth history and so that we can make informed predictions about future climate change and potential mass extinctions in the Anthropocene (Bacon and Swindles 2016). Although considerably more work is needed, the potential cuticle SO2 proxy (presented here) and leaf physiognomy SO2 proxy (Bacon et al. 2013) represent the first steps towards developing plant-based SO2 proxies useful for interpreting environmental change mediated by SO2 in the fossil record. Future work, including targeted sampling of appropriate time intervals with more quantitative analyses of fossil plant material and experimental studies, are needed before these proxies can be applied with full confidence.
The fossil cuticle analysis presented here provides strong evidence for the detrimental effects of SO2 on Ginkgoales and Bennettitales cuticle surfaces across the Tr–J boundary at Astartekløft, East Greenland. When considered together with previously reported evidence for SO2-mediated leaf shape change of multiple plant taxa, the findings of this study provide compelling evidence for a major role of SO2 in the ecosystem response observed across this transition, which includes the end-Triassic mass extinction. These findings provide a means of investigating the role of SO2 in mass extinction events, something that has previously proven elusive.
We would like to thank Prof. Jennifer C. McElwain (University College Dublin, Ireland) for original field collection of the studied plant fossils, as well as useful advice and discussions. The manuscript was greatly improved by the comments and suggestions of Bas van de Schootbrugge and an anonymous reviewer. M. Steinthorsdottir gratefully acknowledges funding by EU Marie Curie Excellence Grant (MEXT-CT-2006-042531) and financial support from the Bolin Centre for Climate Research, Stockholm University.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
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