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

For most of the Phanerozoic Eon, Earth's woody vegetation has been dominated by C-3 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 (Delta C-13) 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, [O-2] could have ranged from similar to 180 to 1100 ppm, and similar to 15 to 25%, respectively, across the past 250 Ma). Yet, differences in Delta C-13 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 comprehensive ab initio model of discrimination, with a recent model of plant eco-physiology based on least-cost optimality theory, to show how differences in D13C between angiosperms and gymnosperms arise. We train the comprehensive model using a very large (n > 7000) database of leaf and tree ring data spanning the past 110 years. We find that averaged differences in Delta C-13 between angiosperm and gymnosperms decrease modestly with atmospheric [O-2]:[CO2] ratios, and increase strongly with vapor pressure deficit (D). These relationships can be explained by three key physiological differences: (1) the ratio of cost factors for transpiration to carboxylation (higher in angiosperms); (2) the ratio of mesophyll to stomatal conductances of CO2 (lower in gymnosperms); and (3) differences in photorespiration. In particular, the amount of CO2 released from photorespiration per oxygenation reaction, k, is generally lower in gymnosperms than in angiosperms. As a result of these factors, Delta C-13 is more sensitive to [CO2] in angiosperms, and to D in gymnosperms. We propose a simplified empirical model to account for this behaviour, and test it against isotopic data from leaves, tree rings and previously-published plant chamber experiments, along with geological data from the Cenozoic. Overall, these data agree with our model over a range of [O-2]:[CO2] ratios from 100 to 650 mol mol(-1) (equivalent to a CO2 range around 323-2100 ppm at 21% O-2), and D levels between 0.45 and 1.1 kPa (R-2 = 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 effects of [O-2], phylogeny, and photorespiration. Lastly, the framework predicts that the average difference in Delta C-13 between woody C-3 plant groups will increase in the future if both [CO2] and global D continue to rise as suggested by projections. (C) 2021 Elsevier Ltd. All rights reserved.

Automated summary

The research indicates that the carbon isotope discrimination differences between angiosperms and gymnosperms may be larger across geological times, potentially associated with environmental and atmospheric changes. Physiological differences and ranges in Delta C-13 between the two plant groups have been revealed through models and experimental data, providing a new explanation for trends in the geological record.