A 23 m.y. record of low atmospheric CO 2

Current atmospheric CO 2 concentration is known to be higher than it has been during the past ∼ 800 k.y. of Earth history, based on direct measurement of CO 2 within ice cores. A comparison to the more ancient past is complicated by a deficit of CO 2 proxies that may be applied across very long spans of geologic time. Here, we present a new CO 2 record across the past 23 m.y. of Earth history based on the δ 13 C value of terrestrial C 3 plant remains, using a method applicable to the entire ∼ 400 m.y. history of C 3 photosynthesis on land. Across the past 23 m.y., CO 2 likely ranged between ∼ 230 ppmv and 350 ppmv (68% confidence interval: ∼ 170–540 ppm). CO 2 was found to be highest during the early and middle Miocene and likely below present-day levels during the middle Pliocene (84 th percentile: ∼ 400 ppmv). These data suggest present-day CO 2 (412 ppmv) exceeds the highest levels that Earth experienced at least since the Miocene, further highlighting the present-day disruption of long-established CO 2 trends within Earth’s atmosphere.


INTRODUCTION
Knowledge of atmospheric CO 2 concentration is vital for understanding Earth's climate system because it imparts a controlling effect on global temperatures across recent (Hegerl et al., 2006) and geologic (Foster et al., 2017) time scales. Proxies (Breecker et al., 2010) and models (Royer et al., 2014) indicate that CO 2 has varied widely during the geologic past. Direct measurement of CO 2 has been performed at the Mauna Loa Observatory (Hawaii, USA) for the past 60+ yr, and historical CO 2 has been sampled continuously from ice-core bubbles recording the past 800 k.y. (Petit et al., 1999;Lüthi et al., 2008), allowing for trends in CO 2 during the latter portion of the Quaternary to be evaluated in detail. Direct observations of atmospheric greenhouse gases are also now available from discontinuous ice up to 2 m.y. old from East Antarctica (Higgins et al., 2015;Yan et al., 2019).
Here, we present a method for calculating CO 2 that is based on a ubiquitous substrate, is sensitive across a wide range of CO 2 , and is rooted in a fully understood mechanism of response to changing CO 2 . We illustrate its efficacy by presenting a novel, high-resolution record of CO 2 for the Neogene through the Quaternary (i.e., the past 23 m.y.), a period that lacks a continuous record of CO 2 from any single proxy.
Our approach is centered upon the δ 13 C value of C 3 vascular land plants (hereafter δ 13 C p ), which is available from terrestrial sediments for most of the Phanerozoic (Nordt et al., 2016). Our calculations of CO 2 assumed that global changes in atmospheric composition affect the plant tissues of all terrestrial C 3 plants via the universally shared mechanism of photorespiration. Because CO 2 is well mixed in Earth's atmosphere, and diminished photorespiration with increasing CO 2 is fundamental to the biochemistry of photosynthesis, this mechanism is recorded globally (Keeling et al., 2017). Our previous growth chamber experiments, in combination with meta-analyses, established that the effect of CO 2 on δ 13 C p value is consistent across a wide range of species and environments Jahren, 2012, 2018). Recent works have also shown that the influence of CO 2 on δ 13 C p value is not affected by water availability (Lomax et al., 2019) or atmospheric O 2 levels (Porter et al., 2017), and it is recorded within multiple organic substrates (e.g., cellulose and collagen [Hare et al., 2018], hair [Zhao et al., 2019], and n-alkanes [Wu et al., 2017]) and inorganic substrates (e.g., speleothems [Breecker, 2017] and cave air [Bergel et al., 2017]). Consequently, researchers now correct δ 13 C values for changes in CO 2 across a myriad of fossil (e.g., ungulate teeth [Luyt et al., 2019;Sealy et al., 2019], soil-respired carbon [Caves Rugenstein and Page Chamberlain, 2018], soil carbonate [Basu et al., 2019], pyrogenic carbon and n-alkanes [Zhou et al., 2017], and pollen [Bell et al., 2019]), and modern (e.g., fungi [Hobbie et al., 2017] and leaves [Tibby et al., 2016]) substrates, and recent experiments have shown that the δ 13 C p value can produce accurate estimates of paleo-CO 2 concentration (Porter et al., 2019).

METHODS
We reconstructed CO 2 across the past 23 m.y. using a compilation of 700 δ 13 C measurements gathered from 12 previously published studies of terrestrial organic matter (TOM; n = 441) and plant lipids (n = 259) that spanned at least 1 m.y. of the Neogene (Table S1 in the Supplemental Material 1 ). We chose these substrates because both TOM and plant lipid δ 13 C values have been shown to respond similarly to changes in CO 2 (Schubert and Jahren, 2012;Wu et al., 2017;Chapman et al., 2019); these substrates also represent an integrated signal with multiple photosynthetic inputs, which has been shown to improve the accuracy of the proxy (Porter et al., 2019). For studies that reported δ 13 C p data for multiple n-alkanes (e.g., n-C 27 , n-C 29 , n-C 31 ), we selected only one record, or the weighted mean values (if reported), thus avoiding redundancy in our compiled data set. The δ 13 C p data set used for input exhibited a large range in δ 13 C p values (∼8‰), sampled from a wide range of environments; plant lipids generally exhibited lower δ 13 C p values than TOM of the same age, as is commonly observed (e.g., Chikaraishi and Naraoka, 2003). We limited our literature compilation to records with δ 13 C p values of TOM ≤ −22.0‰ and plant lipids ≤ −27.0‰, thus avoiding δ 13 C p values that reflected C 4 ecosystems (O'Leary, 1988). Less than 2% of all compiled δ 13 C p values fell above these thresholds, and these were determined to be statistical outliers (all values are reported in Figure 1 and in Table S1).
The approach used here to reconstruct atmospheric CO 2 concentration based on changes in δ 13 C p value was first described by Schubert and Jahren (2012) and then demonstrated by Schubert and Jahren (2015). This approach calculates CO 2 based on changes in δ 13 C p value (i.e., δ 13 C anomaly ) between two points in time, time t = 0 (for which CO 2 is known) and time t (for which CO 2 is not known): where A, B, and C are curve-fitting parameters (A = 28.26, B = 0.22, C = 23.9; Jahren, 2012, 2015;Cui and Schubert, 2016). When calculating δ 13 C anomaly , it is necessary to correct for (1) changes in the δ 13 C value of atmospheric CO 2 between time t [δ 13 C atm(t) ] and time t = 0 [δ 13 C atm(t = 0) ], and (2) any biosynthetic fractionation when comparing across different plant tissues (e.g., TOM and lipids). Therefore, δ 13 C anomaly represents the change in δ 13 C p value, after correcting for changes in the δ 13 C value of atmospheric CO 2 (δ 13 C atm ) and any systematic δ 13 C p offset between plant tissues (ε), such that We can then rewrite Equation 1 in order to solve for CO 2 at any time t (CO 2(t) ), as a function of δ 13 C p and δ 13 C atm :  Figure 1 shows a continuous record of CO 2 across the past 23 m.y. based on changes in δ 13 C p value (i.e., δ 13 C anomaly ). We calculated that the median CO 2 value was lower than that of today across the entirety of the past 23 m.y., and it likely never fell below levels experienced during Pleistocene glacial advances (∼170 ppm; Petit et al., 1999;Kawamura et al., 2007).

RESULTS
Our record commences at the start of the Neogene, when CO 2 was at a local high for the entire record (∼350 ppmv; 23.0-22.4 Ma; Fig. 1C). During the middle Miocene (i.e., 17.1-15.4 Ma), CO 2 reached a maximum and then steadily decreased to below the threshold for Northern Hemisphere glaciation (∼280 ppmv; DeConto et al., 2008) at the end of the Miocene. The middle Pliocene (ca. 5-3 Ma) experienced CO 2 levels that might have approached early 21 st century levels (∼400 ppmv; 84th percentile). This time period corresponds with elevated global temperatures as inferred from multiple models (Haywood et al., 2013), and sea levels up to 25 m higher than today (Miller et al., 2012;Grant et al., 2019). CO 2 declined to near or just-below pre-industrial levels during the late Pliocene, while Northern Hemisphere glaciation increased (Balco and Rovey, 2010;Bailey et al., 2013). Low CO 2 continued across the Quaternary glacial-interglacial cycles (Fig. 2) until the anthropogenic disruption in carbon cycling via the widespread use of fossil fuels (Keeling et al., 2001). Our overall record of the past 23 m.y. reveals a significant linear CO 2 decline equal to an average of 5 ppmv per million years (p < 0.0001). This contrasts with an average increase of 5 ppmv per decade experienced across the past 270 yr that has more than offset the CO 2 decline of the past 23 m.y.

DISCUSSION
The changes in CO 2 that we have constructed are corroborated by contemporaneous changes in various Earth cycles at the sub-epoch scale.
The most important change is the long-term global cooling in progress across the Neogene, as determined by Zachos et al. (2001) based on the δ 18 O value of foraminifera, that coincides with increased reactivity of the land surface In comparing our record to the sparse data available from other proxies (Fig. 3), we see that alkenone-and stomata-based reconstructions generally estimate higher CO 2 across much of the past 23 m.y., although with overlapping uncertainties, while the δ 11 B-and paleosol-based reconstructions do not show any consistent biases relative to our data set. In addition, the lack of continuous proxy data precludes identification of unequivocal, long-term changes in CO 2 over the past 23 m.y. (Figs. 3A-3C), except perhaps for a downward trend within the data set generated using stomatal indices (Fig. 3D).
Two key intervals of the past 23 m.y. have been cited as potential analogs for anthropogenic climate change (IPCC, 2013): the middle Miocene and Pliocene. A corresponding CO 2 increase across these two warm intervals, however, remains enigmatic (Fig. 3). For example, stomatal indices suggest CO 2 above pre-industrial levels during much of the middle Miocene (Fig. 3D), while paleosol carbonate data indicate very low CO 2 and no apparent trends (Fig. 3C). The δ 11 B-based reconstructions do not show any clear trends during the middle Miocene, with estimates ranging from ∼200 to 600 ppmv (Fig. 3B). High-resolution CO 2 data are generally lacking for the late Miocene, which makes inference of CO 2 trends during global cooling difficult to establish. In contrast, our reconstruction allows for a nearly continuous record of CO 2 that links the mid-Miocene and Pliocene warm intervals by a long-term CO 2 decline (Fig. 1C). Finally, our record reveals a CO 2 increase within the early Pliocene that is not evident when examining any single proxy, but that corresponds with mid-Pliocene warming and an inferred CO 2 increase (e.g., IPCC, 2013, their figure 5.2).

CONCLUSIONS
One of the most pressing messages that climate scientists attempt to convey to the public is that current CO 2 (2019 CE = 412 ppmv; Keeling et al., 2001) is elevated compared to the geologic past. The fact that current CO 2 is higher than it was at any time during the past ∼800 k.y. is a straightforward claim based upon direct CO 2 measurements from ice cores (Petit et al., 1999;Kawamura et al., 2007) and the Mauna Loa Observatory (Keeling et al., 2001); claims associated with the more distant geologic past have been variable, partially based on a lack of consensus within the paleoclimate community. Statements addressing values from 3 m.y. ago (Willeit et al., 2019) to 15 m.y. ago (Tripati et al., 2009) can be found, contributing to public confusion and skepticism.
Our results support the claim that CO 2 has been lower than present-day values at least across the past 7 m.y., and potentially during the entirety of the past 23 m.y.; however, CO 2 likely never fell below levels experienced during the greatest ice-sheet advances of the Pleistocene (∼170 ppm; Petit et al., 1999). Our results also indirectly imply that the major reorganizations of plant (e.g., Salzmann et al., 2008), animal (e.g., Stebbins, 1981, and hominid (e.g., White et al., 2009) ecosystems were not driven by large-amplitude changes in CO 2 . More meaningful, perhaps, is the inference that these reorganizations could have impelled, or been impelled by, relatively small-amplitude changes in CO 2 . Our CO 2 record differs from that gained by prior proxies in that it was produced from substrates that span 23 m.y. of uninterrupted Earth history. Our results also show good agreement with discontinuous marine and terrestrial CO 2 proxies, suggesting that the validity of the proposed mechanism underlying the effect of CO 2 on δ 13 C p values (Schubert and Jahren, 2018) may be comparable to those of these previously confirmed CO 2 proxies. Compared to these methods, however, our proxy has the advantage of relying upon a substrate (terrestrial fossil organic carbon) that is widely available both spatially and temporally (Strauss and Peters-Kottig, 2003;Nordt et al., 2016), allowing the possibility for a near-continuous reconstruction of CO 2 across the entire evolution of C 3 land plants.