Global and Planetary Change 189 (2020) 103177

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Global and Planetary Change

journal homepage: www.elsevier.com/locate/gloplacha

Research article

Deep time perspective on rising atmospheric CO2 T ⁎ Gregory J. Retallack , Giselle D. Conde

Department of Earth Sciences, University of Oregon, Eugene 97307, USA

ARTICLE INFO ABSTRACT

Keywords: The accuracy of CO2 hindcasting using fossil stomatal index is ripe for revision for three reasons: ex- Stomatal index ponential rise in atmospheric CO2 over the past decade, discovery of a Kew herbarium specimen of Ginkgo picked Greeenhouse spikes in 1754, and increased sophistication of a pedogenic CO2 paleobarometer as an independent parallel record. Past Gingko mass extinctions coincide with revised CO2 spikes of 1500 ppm or more. Increases such as the middle Miocene Mass exinction level of 640 ± 71 ppm expected before the year 2100 resulted in biome shifts, with expansion of tropical forests northward, and of grasslands into deserts. Deep time records from paleosols and from stomatal index reveal that

CO2 levels less than 180 ppm and more than 1500 ppm are toxic to the biosphere.

1. Introduction create deformed stomata (Barclay and Wing, 2016). This study is mainly based on herbarium specimens now extending back to 1754

Atmospheric CO2 from fossil fuel burning, forest fires, agricultural (Fig. 1), but is also well constrained because of non-linear decline in ploughing, and oxidation of methane from ruminants and rice paddies stomatal index of Ginkgo over the past two decades newly presented has increased dramatically in the past decade (Ciais et al., 2013). Since here (Fig. 2). observations began in 1958 with 316 ppm, atmospheric CO2 levels at Stomatal size also increases with increasing CO2 (Franks and Mauna Loa have continually climbed with ± 2 ppm seasonal variation Beerling, 2009a, 2009b), and provides another useful CO2 proxy to a peak of 415 ppm in May 2019 (NOAA, 2020). By the year 2100, (Franks et al., 2014), but requires many additional measurements of atmospheric CO2 concentrations could reach 936 ± 140 ppm, based studied specimens not currently available. Stomatal and cell size also on RCP 8.5 emission scenario of a heterogeneous world with continued increase with genome size, especially for polyploids (Beaulieu et al., population growth (Meinshausen et al., 2011). Such changes are un- 2008), which can show dramatic stepwise increases within closely re- precedented in Quaternary ice core measurements showing fluctuation lated fossil leaves (Roth and Dilcher, 1979). Such dramatic differences between 180 and 280 ppm (Lüthi et al., 2008), and their effects can be in cell size were not seen in our data of Ginkgo and other taxa with assessed by proxies for atmospheric CO2 deep in geological time similar cuticles, in which cell size differences were only noted at very (Breecker and Retallack, 2014; Franks et al., 2014). Deep time records high levels (> 1000 ppm) of CO2. give a unique perspective on natural variation and limits of atmospheric A significant refinement of the Ginkgo stomatal index proxy is of-

CO2. fered here from herbarium specimens of unprecedented temporal range A useful proxy for ancient CO2 is stomatal index, or percent stomata from 1754 to 2015, when observed CO2 had turned the corner to its normalized to other cells, of the living fossil Ginkgo and fossils with current dramatic rise (NOAA, 2020). Our new calibration allows a new similar cuticle anatomy (Retallack, 2001). Stomatal index declines with reconstruction of atmospheric CO2 over the past 300 million years as rising CO2 because minimize water loss by deploying the fewest evidence of past greenhouse crises (Retallack, 2009a), their effects in stomata needed for CO2 intake to sustain photosynthesis, and is dif- biodiversity crises (Peters and Foote, 2002), and their role in biogeo- ferent for different woodland species as discovered by Salisbury (1927). graphic shifts (Retallack et al., 2016). For application to deep time “living fossils” such as Ginkgo have been evaluated for this effect (McElwain and Chaloner, 1996; McElwain, 2. Material and methods 2018), using live and dated herbarium leaves, as well as leaves from greenhouse experiments under different CO2 levels (Beerling et al., A recently discovered Kew Herbarium specimen of Ginkgo biloba 1998; Retallack, 2001; Royer et al., 2001). Some doubt about green- picked in 1754 is well enough preserved to count stomata, despite house experiments has arisen because they have been harsh enough to fungal damage (Fig. 1). All images counted (Conde, 2016) were

⁎ Corresponding author. E-mail address: [email protected] (G.J. Retallack). https://doi.org/10.1016/j.gloplacha.2020.103177 Received 23 August 2019; Received in revised form 18 March 2020; Accepted 20 March 2020 Available online 21 March 2020 0921-8181/ © 2020 Elsevier B.V. All rights reserved. G.J. Retallack and G.D. Conde Global and Planetary Change 189 (2020) 103177

Fig. 1. Scanning electron micrograph and herbarium sheet for Gingko biloba collected in Japan in 1754 (Kew Botanical Garden, London). Elongate cells at the bottom of the SEM are above veins, and interveinal stomatal openings are dark holes surrounded by raised bumps (papillae).

trajectory (NOAA, 2020). That trajectory has also been guided by greenhouse studies of stomatal index of Ginkgo grown under different

levels of CO2, but some of those greenhouse studies are suspect because of unnatural malformation of stomata produced by the experiment (Barclay and Wing, 2016). Other greenhouse studies did not attempt

such extreme CO2 levels (Beerling et al., 1998), and had unrealistic Arctic light regimes, but fall close to extrapolation from herbarium

observations (Fig. 2). Data on atmospheric CO2 for all the years of herbarium leaves studied came from direct observations back to 1958 (NOAA, 2020), supplemented by ice core data back to 1754 (Lüthi et al., 2008).

Curve fitting to the relationship between CO2 and stomatal index has taken many forms (Barclay and Wing, 2016), but an inverse power function based on the principles of Fickian diffusion is most appro- priate, with constants and power varied to fit data (Wynn, 2003). An- other key feature of our method is counting images with about 600 cells and 60 stomata in both stomatiferous and astomatic areas as a proxy for total leaf conductance. Counting smaller areas of cuticle with as few as 5 stomata gives unacceptable systematic errors of stomatal index:

Fig. 2. Relationship between atmospheric CO2 (ppm) and stomatal index of about ± 20% depending on whether 5 or 6 stomata are accidently in Ginkgo leaves (%) from herbarium (closed symbols herein) and greenhouse data the image. This may account for high errors from counting 5–18 sto- (open symbols). The recommended function is based only on our herbarium mata by Barclay and Wing (2016). The stomatal index CO2 paleoba- data (see Supplementary Information Online), but an alternative function in- rometer estimates atmospheric CO2 (C in ppm) from stomatal index (I in cludes both herbarium and greenhouse data of Beerling et al. (1998) and Royer % from Eq. (1)) of fossil plants with preserved cell impressions or cu- (2002). Other recent transfer functions are also shown (Retallack, 2009a; ticle in which number of stomata (n ) and number of epidermal cells Barclay and Wing, 2016), but not their data points. s (ne) in the same area can be counted. This inverse relationship (Eq. (2)) has an algebraically simplified equivalent (Eq. (3)) between Gingko scanning electron micrographs using an environmental instrument, stomatal index (I) and atmospheric CO2 (C). Standard deviations (1σ)of which did not require metal sputter coating. Such images show papillae CO2 concentration (Sc ) were calculated by Gaussian error propagation more clearly than standard macerated preparations, which is important (Eqs. (4) and (5)). Eq. (5) is the partial derivative of Eq. (3) (Wolfram because there is not a 1:1 correspondence between papillae and cells Alpha, 2019). (Fig. 1). Our 1754 leaf anchors the calibration curve for calculating n atmospheric CO from Gingko stomatal index published previously I =×100 s 2 nn+ (1) (Retallack, 2009a), and includes new estimates for the intervening se years (Fig. 2). This 264-year record of Ginkgo stomatal index turned 1 C =+239.7 −74.79 sharply within the recent two decades of CO2 rise to constrain its future 2.75255×× 10 I (2)

2 G.J. Retallack and G.D. Conde Global and Planetary Change 189 (2020) 103177

Fig. 3. Estimated atmospheric CO2 from independent evidence of paleosols and

Ginkgo stomatal index, including two high-CO2 paleosols of the , Chinle

Group in New Mexico (Cotton and Sheldon, 2012), and five low-CO2 paleosols of the Miocene, Railroad Canyon Formation in Idaho (Retallack, 2009b).

Fig. 4. Time series over the past 300 Ma of (a) atmospheric CO2 concentration (ppm) inferred from stomatal index of fossil Lepidopteris (blue and left) and CI=+239.7 3, 633, 000 ×−4.79 (3) Ginkgo (red and right) leaves. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) ∂C 2 ScI= ⎛ × S ⎞ ⎝ ∂I ⎠ (4) with a y axis of less than half the magnitude of that earlier calibration. ∂C −17, 402, 070 The Ginkgo record goes back only to (226 Ma). = ∂II5.79 (5) Lepidopteris has similar stomatal index to Ginkgo at two localities in , and related plants with identical cuticles can be used to extend the record back 300 Ma to latest (Retallack, 3. Independent validation 2009a). Some species of Lepidopteris have been considered vines (McElwain et al., 2007), rather than trees like Ginkgo, but other species CO2 calculated from our new transfer function (Eq. (3) above) can of Lepidopteris were dominant plants of low-diversity woodland vege- be checked against estimates of CO2 from a revised model of carbon tation (Retallack, 2002). Each ancient species used to infer CO2 was isotopic fractionation in paleosols using new paleosol-specific pro- different from modern Ginkgo in some way, but the uniformity of their ductivity estimates (Breecker and Retallack, 2014), which considerably stomatal morphology is remarkable (Retallack, 2009a). About 60% of improves the correlation of paleosol and stomatal index measures the past estimates of CO2 in Fig. 4 and Table S1 are relatively low (Beerling and Royer, 2011). Our newly calibrated estimates of atmo- (between 180 and 600 ppm), within the limits of the calibration curve spheric CO2 from Gingko stomatal index are compared with paleosol (Fig. 2). As expected, the lowest levels are in the and Pleis- estimates for the same geological times in Fig. 3: two high-CO2 paleo- tocene ice ages (Fig. 4). The spread of deserts and ice caps, marked by sols of the Triassic, Chinle Group in New Mexico (Cotton and Sheldon, widespread Aridisol and Gelisol paleosols at those times (Retallack, 2012), and five low-CO2 paleosols of the Miocene, Railroad Canyon 2007), may have reduced global carbon sequestration to a minimum,

Formation in Idaho (Retallack, 2009b). These are the only two sets of but could not go lower because of continued CO2 emissions from vol- paleosol estimates available using this new method (Breecker and canoes and global respiration. Retallack, 2014). These independent lines of evidence confirm new CO2 estimates from stomatal index lower than previously thought

(Retallack, 2009a), and in line with other CO2 proxies, such as marine 4. Greenhouse spikes alkenones, marine boron isotopes, and liverwort carbon isotopes

(Royer, 2010). Our best estimate for the early Lutetian (50 Ma) of Numerous transient spikes in CO2 (Fig. 4) are now well controlled 847 ± 235 ppm CO2 (supplementary Information Table S1) is lower stratigraphically not only by improved dating of Ginkgo leaves, but by than an estimate from lacustrine nahcolite+halite of 2055 ± 930 ppm evidence of warm-wet spikes in sequences of paleosols, and in carbon (Lowenstein and Demicco, 2006), which may be unduly high because of isotopic time series (Retallack, 2009a). Our result may be contrasted respiration, either within water of the ancient lake, or within the Gypsid with another pilot study proposing values “below 1000 ppm for most of soil of the dry lake bed (Breecker and Retallack, 2014). Another dis- the Phanerozoic, from the onwards” (Franks et al., 2014), but crepancy is the Changhsingian (252 Ma) spike with our stomatal index that result for the Late Triassic, for example, was obtained by averaging estimate of 2109 ± 1267 ppm for maximum CO2 of the past 300 Ma, estimates from 10 different fossils and localities, including one of but modelled from marine carbon isotopic data as 2800 to 8300 ppm 1585 ppm CO2. The rapidity of both onset and decline of paleoclimatic CO2 (Cui et al., 2014). spikes is confirmed by carbon isotopic composition of organic matter Our new transfer function gives a refined perspective on the history within varved shales, which show greenhouse onset and decline within of atmospheric CO2, which has fluctuated dramatically in deep time millennia (Retallack and Jahren, 2008). These Late Permian shale (Fig. 4). The new data are comparable with sedimentary mass balance varves are known to be annual because they contain abscised deciduous estimates of CO2 (Berner, 1997), if degraded by a 5 point running leaves of Glossopteris. Other confirmation of rapid onset of greenhouse average to approximate the 10-million-year steps of mass balance spikes comes from the paleoprecipitation proxy of depth to Bk horizon modelling (Retallack, 2001). These new data include more points, and in 3718 paleosols in Utah and adjacent states over the past 300 million are topologically very similar with the data of Retallack (2009a), but years with sufficient resolution to show very short term (< million

3 G.J. Retallack and G.D. Conde Global and Planetary Change 189 (2020) 103177 year) transients (Retallack, 2009a). The outlier deep calcic paleosols are not experimental, nor observational errors, because deep-calcic paleo- sols can be traced as stratigraphic markers throughout the Colorado Plateau of North America (Retallack, 2009a).

Many extreme CO2 transients coincide in time with eruption of large igneous provinces, such as the Late Permian Siberian Traps (Ivanov et al., 2013) and Late Deccan Traps (Renne et al., 2015). Such unusually large eruptions may have created transient greenhouse

CO2 spikes and carbon isotopic excursions by thermogenic cracking of coal and carbonaceous shale (Retallack and Jahren, 2008), or release of methane clathrates (Krull et al., 2000). Radiometric dating of the Late Permian Siberian Traps (Ivanov et al., 2013) and latest Cretaceous Deccan Traps (Renne et al., 2015) shows that eruptions were focused in time to less than two million years. Some spikes, such as the Late

Cretaceous CO2 transient, coincide in time with asteroid impact, which would have vaporized biomass to CO2 at ground zero, and added to oxidized carbon by promoting forest fires (Retallack, 1996). Not only do the spikes rise within thousands of years due to atmo- spheric injection of CO2 or CH4, but they also fall within thousands of years (Fig. 4). Geologically rapid decline coincides in time with spread of more productive ecosystems into arid lands, where they weathered soil of nutrients (including calcium) more deeply (Retallack, 2009a), and also migration of tropical forests and their deeply weathered soils into high latitudes (Retallack, 2010; Retallack et al., 2016). Greenhouse spikes raised temperatures and humidity to promote hydrolytic weathering, growth, and thus carbon consumption and seques- tration. A previously published quantification of these relationships from paleosols in Utah (Retallack, 2009a), now must be revised to predict that doubling of CO2 will result in 1.1 °C increase in MAT, and 110 mm increase in MAP from paleosol carbonate depth, and 221 mm increase in MAP from paleosol chemistry (equations in Fig. 5). Doubling estimates are often called “sensitivity”, and have not otherwise been estimated for mean annual precipitation. Global sensitivity of tem- perature to CO2 doubling has been estimated in other studies (Royer, 2010; Franks et al., 2014) as 3 °C, which is twice our estimate for deep time records of Utah (Fig. 5). Comparable multiproxy studies from elsewhere will be needed to determine whether this is real a dis- crepancy, but there are now reasons to suspect Utah climate is not globally representative. With current planetary warming, mid-latitude regions have been spared sterilizing heat waves of low latitudes (Frölicher and Laufkötter, 2018; McWhorter et al., 2018) and dramatic deglaciation of polar regions (Overland et al., 2014; Hanna et al., 2014; Retallack, 2010).

Of concern in our century of rapidly rising CO2 are biotic effects of greenhouse spikes, and particularly their effects on biodiversity (Retallack, 2007). The best available metric for defining mass extinc- tions in deep time is the fossil record of shelled marine invertebrates

(Peters and Foote, 2002). CO2 transients above 1500 ppm by our esti- mation appear to be a planetary Rubicon for mass extinctions (Fig. 6)of the Capitanian (Middle Permian, 262 Ma), Changsinghian (Late Per- mian, 253 Ma), Smithian (Early Triassic, 251 Ma), Rhaetian (Late Fig. 5. Correlation of atmospheric CO2 from Ginkgo stomatal index (ppm) and paleoclimate from paleosols of Utah (Retallack, 2009a). Mean annual tem- Triassic, 202 Ma), and perhaps also Maastrichtian (Late Cretaceous, perature (°C) was calculated from alkali index (a), and mean annual pre- 66 Ma). Doubts about the Maastrichtian come from inadequate data cipitation (mm) from both chemical ratio of CIA-K (b), and from compaction- from stomatal index of Ginkgo (Retallack, 2009a) and ferns (Beerling corrected depth to Bk horizon (c). et al., 2002). Thus an earlier documentation of the relationship between magnitude of greenhouse spikes and mass extinction (Retallack, 2007), the Middle Miocene (Breecker and Retallack, 2014), when transient is also revised here (Fig. 6). A variety of kill mechanisms are ex- atmospheric injections of CO2, perhaps from Columbia River Group acerbated by unusually high levels of atmospheric CO2: marine anoxia flood basalt eruptions (Retallack et al., 2016), created modest mam- (Song et al., 2014), coral bleaching (Veron, 2008), wetland tree suffo- malian and floral overturn (Retallack, 2013). These crises were fol- cation (Retallack and Jahren, 2008), acid rain (Retallack, 1996), and lowed by diversity-enriching polar migrations and expanded carbon intense storms (Kim et al., 2014). sinks from geographical expansion of tropical forests, polar wetlands, and mid-continental grasslands (Retallack et al., 2016). Deep time re- 5. Conclusions cords provide useful expectations for toxic highs and lows of atmo-

spheric CO2. The message from the past 300 million years is that CO2, Coming atmospheric levels of 450–950 ppm CO2 by 2100 due to essential for photosynthesis, can be harmful to life on Earth in very anthropogenic forcing (Meinshausen et al., 2011) were last seen during

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