Differences in carbon isotope discrimination between angiosperm and gymnosperm woody plants, and their geological significance

Abstract

For most of the Phanerozoic Eon, Earth’s woody vegetation has been dominated by C3 plants - predominantly gymnosperms -with angiosperms only emerging as the dominant plant group as CO2 declined during the Cenozoic (66 Ma onward). At present, differences in carbon isotope discrimination (D13C) between angiosperm and gymnosperm plants are relatively small (2–3‰), but an increasing body of evidence points to larger differences across geological times (up to 6–7‰), potentially associated with varying environmental conditions and atmospheres (i.e. concentrations of atmospheric carbon dioxide, [CO2], and oxygen, [O2] could have ranged from 180 to 1100 ppm, and 15 to 25%, respectively, across the past 250 Ma). Yet, differences in D13C between the two plant groups, and their potential link to climatic and environmental changes, have not yet been fully explored and understood.Here, we combine a comprehensiveab initiomodel of discrimination, with a recent model of plant eco-physiology based on least-cost optimality theory, to show how differences inD13C between angiosperms and gymnosperms arise. We train the comprehensivemodel using a very large (n>7000) database of leaf and tree ring data spanning the past 110 years. We find that averaged dif-ferences inD13C between angiosperm and gymnosperms decrease modestly with atmospheric [O2]:[CO2] ratios, and increasestrongly with vapor pressure deficit (D). These relationships can be explained by three key physiological differences: (1) the ratioof cost factors for transpiration to carboxylation (higher in angiosperms); (2) the ratio of mesophyll to stomatal conductances ofCO2(lower in gymnosperms); and (3) differences in photorespiration. In particular, the amount of CO2released from photores-piration per oxygenation reaction,k, is generally lower in gymnosperms than inangiosperms. As a result of these factors,D13Cismore sensitive to [CO2]inangiosperms,andtoDin gymnosperms. We propose a simplified empirical model to account for thisbehaviour, and test it against isotopic data from leaves, tree rings and previously-published plant chamber experiments, along withgeological data from the Cenozoic. Overall, these data agree with our model over a range of [O2]:[CO2] ratios from 100 to650 mol mol 1(equivalent to a CO2range around 323–2100 ppm at 21% O2), andDlevels between 0.45 and 1.1 kPa(R2=0.51,RMSE=1.49‰). Our simplified empirical model offers a new explanation for secular trends in the geological record,and suggests a way forward to improve paleo-[CO2] proxies based on terrestrial discrimination models by incorporating the effectsof [O2], phylogeny, and photorespiration. Lastly, the framework predicts that the average difference inD13C between woody C3plant groups will increase in the future if both [CO2] and globalDcontinue to rise as suggested by projections.