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Global and Planetary Change

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Research article

Deep time perspective on rising atmospheric CO2Gregory J. Retallack⁎, Giselle D. CondeDepartment of Earth Sciences, University of Oregon, Eugene 97307, USA

A R T I C L E I N F O

Keywords:Stomatal indexGreeenhouse spikesGingkoMass exinction

A B S T R A C T

The accuracy of CO2 hindcasting using fossil Ginkgo stomatal index is ripe for revision for three reasons: ex-ponential rise in atmospheric CO2 over the past decade, discovery of a Kew herbarium specimen of Ginkgo pickedin 1754, and increased sophistication of a pedogenic CO2 paleobarometer as an independent parallel record. Pastmass extinctions coincide with revised CO2 spikes of 1500 ppm or more. Increases such as the middle Miocenelevel of 640 ± 71 ppm expected before the year 2100 resulted in biome shifts, with expansion of tropical forestsnorthward, and of grasslands into deserts. Deep time records from paleosols and from stomatal index reveal thatCO2 levels less than 180 ppm and more than 1500 ppm are toxic to the biosphere.

1. Introduction

Atmospheric CO2 from fossil fuel burning, forest fires, agriculturalploughing, and oxidation of methane from ruminants and rice paddieshas increased dramatically in the past decade (Ciais et al., 2013). Sinceobservations began in 1958 with 316 ppm, atmospheric CO2 levels atMauna Loa have continually climbed with±2 ppm seasonal variationto a peak of 415 ppm in May 2019 (NOAA, 2020). By the year 2100,atmospheric CO2 concentrations could reach 936 ± 140 ppm, basedon RCP 8.5 emission scenario of a heterogeneous world with continuedpopulation growth (Meinshausen et al., 2011). Such changes are un-precedented in Quaternary ice core measurements showing fluctuationbetween 180 and 280 ppm (Lüthi et al., 2008), and their effects can beassessed by proxies for atmospheric CO2 deep in geological time(Breecker and Retallack, 2014; Franks et al., 2014). Deep time recordsgive a unique perspective on natural variation and limits of atmosphericCO2.

A useful proxy for ancient CO2 is stomatal index, or percent stomatanormalized to other cells, of the living fossil Ginkgo and fossils withsimilar cuticle anatomy (Retallack, 2001). Stomatal index declines withrising CO2 because plants minimize water loss by deploying the feweststomata needed for CO2 intake to sustain photosynthesis, and is dif-ferent for different woodland species as discovered by Salisbury (1927).For application to deep time “living fossils” such as Ginkgo have beenevaluated for this effect (McElwain and Chaloner, 1996; McElwain,2018), using live and dated herbarium leaves, as well as leaves fromgreenhouse experiments under different CO2 levels (Beerling et al.,1998; Retallack, 2001; Royer et al., 2001). Some doubt about green-house experiments has arisen because they have been harsh enough to

create deformed stomata (Barclay and Wing, 2016). This study ismainly based on herbarium specimens now extending back to 1754(Fig. 1), but is also well constrained because of non-linear decline instomatal index of Ginkgo over the past two decades newly presentedhere (Fig. 2).

Stomatal size also increases with increasing CO2 (Franks andBeerling, 2009a, 2009b), and provides another useful CO2 proxy(Franks et al., 2014), but requires many additional measurements ofstudied specimens not currently available. Stomatal and cell size alsoincrease with genome size, especially for polyploids (Beaulieu et al.,2008), which can show dramatic stepwise increases within closely re-lated fossil leaves (Roth and Dilcher, 1979). Such dramatic differencesin cell size were not seen in our data of Ginkgo and other taxa withsimilar cuticles, in which cell size differences were only noted at veryhigh levels (> 1000 ppm) of CO2.

A significant refinement of the Ginkgo stomatal index proxy is of-fered here from herbarium specimens of unprecedented temporal rangefrom 1754 to 2015, when observed CO2 had turned the corner to itscurrent dramatic rise (NOAA, 2020). Our new calibration allows a newreconstruction of atmospheric CO2 over the past 300 million years asevidence of past greenhouse crises (Retallack, 2009a), their effects inbiodiversity crises (Peters and Foote, 2002), and their role in biogeo-graphic shifts (Retallack et al., 2016).

2. Material and methods

A recently discovered Kew Herbarium specimen of Ginkgo bilobapicked in 1754 is well enough preserved to count stomata, despitefungal damage (Fig. 1). All images counted (Conde, 2016) were

https://doi.org/10.1016/j.gloplacha.2020.103177Received 23 August 2019; Received in revised form 18 March 2020; Accepted 20 March 2020

⁎ Corresponding author.E-mail address: gregr@uoregon.edu (G.J. Retallack).

Global and Planetary Change 189 (2020) 103177

Available online 21 March 20200921-8181/ © 2020 Elsevier B.V. All rights reserved.

T

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scanning electron micrographs using an environmental instrument,which did not require metal sputter coating. Such images show papillaemore clearly than standard macerated preparations, which is importantbecause there is not a 1:1 correspondence between papillae and cells(Fig. 1). Our 1754 leaf anchors the calibration curve for calculatingatmospheric CO2 from Gingko stomatal index published previously(Retallack, 2009a), and includes new estimates for the interveningyears (Fig. 2). This 264-year record of Ginkgo stomatal index turnedsharply within the recent two decades of CO2 rise to constrain its future

trajectory (NOAA, 2020). That trajectory has also been guided bygreenhouse studies of stomatal index of Ginkgo grown under differentlevels of CO2, but some of those greenhouse studies are suspect becauseof unnatural malformation of stomata produced by the experiment(Barclay and Wing, 2016). Other greenhouse studies did not attemptsuch extreme CO2 levels (Beerling et al., 1998), and had unrealisticArctic light regimes, but fall close to extrapolation from herbariumobservations (Fig. 2). Data on atmospheric CO2 for all the years ofherbarium leaves studied came from direct observations back to 1958(NOAA, 2020), supplemented by ice core data back to 1754 (Lüthiet al., 2008).

Curve fitting to the relationship between CO2 and stomatal indexhas taken many forms (Barclay and Wing, 2016), but an inverse powerfunction 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 cellsand 60 stomata in both stomatiferous and astomatic areas as a proxy fortotal leaf conductance. Counting smaller areas of cuticle with as few as5 stomata gives unacceptable systematic errors of stomatal index:about± 20% depending on whether 5 or 6 stomata are accidently inthe image. This may account for high errors from counting 5–18 sto-mata by Barclay and Wing (2016). The stomatal index CO2 paleoba-rometer estimates atmospheric CO2 (C in ppm) from stomatal index (I in% from Eq. (1)) of fossil plants with preserved cell impressions or cu-ticle in which number of stomata (ns) and number of epidermal cells(ne) in the same area can be counted. This inverse relationship (Eq. (2))has an algebraically simplified equivalent (Eq. (3)) between Gingkostomatal index (I) and atmospheric CO2 (C). Standard deviations (1σ) ofCO2 concentration (Sc ) were calculated by Gaussian error propagation(Eqs. (4) and (5)). Eq. (5) is the partial derivative of Eq. (3) (WolframAlpha, 2019).

= ×+

I nn n

100 ss e (1)

= +× ×−

CI

239.7 12.75255 10 7 4.79 (2)

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

Fig. 2. Relationship between atmospheric CO2 (ppm) and stomatal index ofGinkgo leaves (%) from herbarium (closed symbols herein) and greenhouse data(open symbols). The recommended function is based only on our herbariumdata (see Supplementary Information Online), but an alternative function in-cludes both herbarium and greenhouse data of Beerling et al. (1998) and Royer(2002). Other recent transfer functions are also shown (Retallack, 2009a;Barclay and Wing, 2016), but not their data points.

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

2

= + × −C I239.7 3, 633, 000 4.79 (3)

= ⎛⎝

∂∂

× ⎞⎠

S CI

Sc I2

(4)

∂∂

= −CI I

17, 402, 0705.79 (5)

3. Independent validation

CO2 calculated from our new transfer function (Eq. (3) above) canbe checked against estimates of CO2 from a revised model of carbonisotopic fractionation in paleosols using new paleosol-specific pro-ductivity estimates (Breecker and Retallack, 2014), which considerablyimproves the correlation of paleosol and stomatal index measures(Beerling and Royer, 2011). Our newly calibrated estimates of atmo-spheric CO2 from Gingko stomatal index are compared with paleosolestimates for the same geological times in Fig. 3: two high-CO2 paleo-sols of the Triassic, Chinle Group in New Mexico (Cotton and Sheldon,2012), and five low-CO2 paleosols of the Miocene, Railroad CanyonFormation in Idaho (Retallack, 2009b). These are the only two sets ofpaleosol estimates available using this new method (Breecker andRetallack, 2014). These independent lines of evidence confirm new CO2estimates from stomatal index lower than previously thought(Retallack, 2009a), and in line with other CO2 proxies, such as marinealkenones, marine boron isotopes, and liverwort carbon isotopes(Royer, 2010). Our best estimate for the early Lutetian (50 Ma) of847 ± 235 ppm CO2 (supplementary Information Table S1) is lowerthan an estimate from lacustrine nahcolite+halite of 2055 ± 930 ppm(Lowenstein and Demicco, 2006), which may be unduly high because ofrespiration, either within water of the ancient lake, or within the Gypsidsoil of the dry lake bed (Breecker and Retallack, 2014). Another dis-crepancy is the Changhsingian (252 Ma) spike with our stomatal indexestimate of 2109 ± 1267 ppm for maximum CO2 of the past 300 Ma,but modelled from marine carbon isotopic data as 2800 to 8300 ppmCO2 (Cui et al., 2014).

Our new transfer function gives a refined perspective on the historyof atmospheric CO2, which has fluctuated dramatically in deep time(Fig. 4). The new data are comparable with sedimentary mass balanceestimates of CO2 (Berner, 1997), if degraded by a 5 point runningaverage to approximate the 10-million-year steps of mass balancemodelling (Retallack, 2001). These new data include more points, andare topologically very similar with the data of Retallack (2009a), but

with a y axis of less than half the magnitude of that earlier calibration.The Ginkgo record goes back only to Late Triassic (226 Ma).

Lepidopteris has similar stomatal index to Ginkgo at two localities inSouth Africa, and related plants with identical cuticles can be used toextend the record back 300 Ma to latest Carboniferous (Retallack,2009a). Some species of Lepidopteris have been considered vines(McElwain et al., 2007), rather than trees like Ginkgo, but other speciesof Lepidopteris were dominant plants of low-diversity woodland vege-tation (Retallack, 2002). Each ancient species used to infer CO2 wasdifferent from modern Ginkgo in some way, but the uniformity of theirstomatal morphology is remarkable (Retallack, 2009a). About 60% ofthe past estimates of CO2 in Fig. 4 and Table S1 are relatively low(between 180 and 600 ppm), within the limits of the calibration curve(Fig. 2). As expected, the lowest levels are in the Permian and Pleis-tocene ice ages (Fig. 4). The spread of deserts and ice caps, marked bywidespread Aridisol and Gelisol paleosols at those times (Retallack,2007), may have reduced global carbon sequestration to a minimum,but could not go lower because of continued CO2 emissions from vol-canoes and global respiration.

4. Greenhouse spikes

Numerous transient spikes in CO2 (Fig. 4) are now well controlledstratigraphically not only by improved dating of Ginkgo leaves, but byevidence of warm-wet spikes in sequences of paleosols, and in carbonisotopic time series (Retallack, 2009a). Our result may be contrastedwith another pilot study proposing values “below 1000 ppm for most ofthe Phanerozoic, from the Devonian onwards” (Franks et al., 2014), butthat result for the Late Triassic, for example, was obtained by averagingestimates from 10 different fossils and localities, including one of1585 ppm CO2. The rapidity of both onset and decline of paleoclimaticspikes is confirmed by carbon isotopic composition of organic matterwithin varved shales, which show greenhouse onset and decline withinmillennia (Retallack and Jahren, 2008). These Late Permian shalevarves are known to be annual because they contain abscised deciduousleaves of Glossopteris. Other confirmation of rapid onset of greenhousespikes comes from the paleoprecipitation proxy of depth to Bk horizonin 3718 paleosols in Utah and adjacent states over the past 300 millionyears with sufficient resolution to show very short term (

year) transients (Retallack, 2009a). The outlier deep calcic paleosols arenot experimental, nor observational errors, because deep-calcic paleo-sols can be traced as stratigraphic markers throughout the ColoradoPlateau of North America (Retallack, 2009a).

Many extreme CO2 transients coincide in time with eruption of largeigneous provinces, such as the Late Permian Siberian Traps (Ivanovet al., 2013) and Late Cretaceous Deccan Traps (Renne et al., 2015).Such unusually large eruptions may have created transient greenhouseCO2 spikes and carbon isotopic excursions by thermogenic cracking ofcoal and carbonaceous shale (Retallack and Jahren, 2008), or release ofmethane clathrates (Krull et al., 2000). Radiometric dating of the LatePermian Siberian Traps (Ivanov et al., 2013) and latest CretaceousDeccan Traps (Renne et al., 2015) shows that eruptions were focused intime to less than two million years. Some spikes, such as the LateCretaceous CO2 transient, coincide in time with asteroid impact, whichwould have vaporized biomass to CO2 at ground zero, and added tooxidized 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 ofyears (Fig. 4). Geologically rapid decline coincides in time with spreadof more productive ecosystems into arid lands, where they weatheredsoil of nutrients (including calcium) more deeply (Retallack, 2009a),and also migration of tropical forests and their deeply weathered soilsinto high latitudes (Retallack, 2010; Retallack et al., 2016). Greenhousespikes raised temperatures and humidity to promote hydrolyticweathering, plant growth, and thus carbon consumption and seques-tration. A previously published quantification of these relationshipsfrom paleosols in Utah (Retallack, 2009a), now must be revised topredict that doubling of CO2 will result in 1.1 °C increase in MAT, and110 mm increase in MAP from paleosol carbonate depth, and 221 mmincrease in MAP from paleosol chemistry (equations in Fig. 5). Doublingestimates are often called “sensitivity”, and have not otherwise beenestimated 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 deeptime records of Utah (Fig. 5). Comparable multiproxy studies fromelsewhere will be needed to determine whether this is real a dis-crepancy, but there are now reasons to suspect Utah climate is notglobally representative. With current planetary warming, mid-latituderegions have been spared sterilizing heat waves of low latitudes(Frölicher and Laufkötter, 2018; McWhorter et al., 2018) and dramaticdeglaciation 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 ofgreenhouse 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) ofthe Capitanian (Middle Permian, 262 Ma), Changsinghian (Late Per-mian, 253 Ma), Smithian (Early Triassic, 251 Ma), Rhaetian (LateTriassic, 202 Ma), and perhaps also Maastrichtian (Late Cretaceous,66 Ma). Doubts about the Maastrichtian come from inadequate datafrom stomatal index of Ginkgo (Retallack, 2009a) and ferns (Beerlinget al., 2002). Thus an earlier documentation of the relationship betweenmagnitude of greenhouse spikes and mass extinction (Retallack, 2007),is also revised here (Fig. 6). A variety of kill mechanisms are ex-acerbated by unusually high levels of atmospheric CO2: marine anoxia(Song et al., 2014), coral bleaching (Veron, 2008), wetland tree suffo-cation (Retallack and Jahren, 2008), acid rain (Retallack, 1996), andintense storms (Kim et al., 2014).

5. Conclusions

Coming atmospheric levels of 450–950 ppm CO2 by 2100 due toanthropogenic forcing (Meinshausen et al., 2011) were last seen during

the Middle Miocene (Breecker and Retallack, 2014), when transientatmospheric injections of CO2, perhaps from Columbia River Groupflood basalt eruptions (Retallack et al., 2016), created modest mam-malian and floral overturn (Retallack, 2013). These crises were fol-lowed by diversity-enriching polar migrations and expanded carbonsinks from geographical expansion of tropical forests, polar wetlands,and mid-continental grasslands (Retallack et al., 2016). Deep time re-cords provide useful expectations for toxic highs and lows of atmo-spheric CO2. The message from the past 300 million years is that CO2,essential for photosynthesis, can be harmful to life on Earth in very

Fig. 5. Correlation of atmospheric CO2 from Ginkgo stomatal index (ppm) andpaleoclimate from paleosols of Utah (Retallack, 2009a). Mean annual tem-perature (°C) was calculated from alkali index (a), and mean annual pre-cipitation (mm) from both chemical ratio of CIA-K (b), and from compaction-corrected depth to Bk horizon (c).

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large (> 1500 ppm) and very small (< 180 ppm) doses.

Acknowledgements

Greg Bothun, Dan Gavin, and Pat Bartlein offered stimulating dis-cussions. Jonathan Wynn, Joshua Roering, and Edward Davis profferedmathematical advice. Chrissie Prychid and Nicola Kuhn provided SEMimages of a Ginkgo leaf of the Kew Herbarium picked in 1754 in Japan.Arne Arneberg provided leaf fragments from the Swedish NaturalHistory Museum picked in 1829 from “Hortus Botanicus Augustinus”,Amsterdam. Sarena Campbell, John Donovan, and Julie Chouinardaided with scanning electron microscopy. Scott Morrison, Phil Knutson,Regan Dunn, and Bill Rember provided access to fossil Ginkgo leaves.

Appendix A. Supplementary material

Supplementary data to this article can be found online at https://doi.org/10.1016/j.gloplacha.2020.103177.

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Fig. 6. Relationship between estimated atmospheric CO2 (ppmv) and marineinvertebrate extinction (% after Peters and Foote, 2002). Late Cretaceous CO2 isinadequately documented, and problematic estimates from stomatal index areshown (Retallack, 2009a; Beerling et al., 1998). See Supplementary InformationOnline for data.

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Deep time perspective on rising atmospheric CO2IntroductionMaterial and methodsIndependent validationGreenhouse spikesConclusionsAcknowledgementsSupplementary materialReferences