Leaf fossil record suggests limited influence of atmospheric CO ₂ on terrestrial productivity prior to angiosperm evolution

Abstract

Declining CO 2 over the Cretaceous has been suggested as an evolutionary driver of the high leaf vein densities (7-28 mm mm −2 ) that are unique to the angiosperms throughout all of Earth history. Photosynthetic modeling indicated the link between high vein density and productivity documented in the modern low-CO 2 regime would be lost as CO 2 concentrations increased but also implied that plants with very low vein densities (less than 3 mm mm −2 ) should experience substantial disadvantages with high CO 2 . Thus, the hypothesized relationship between CO 2 and plant evolution can be tested through analysis of the concurrent histories of alternative lineages, because an extrinsic driver like atmospheric CO 2 should affect all plants and not just the flowering plants. No such relationship is seen. Regardless of CO 2 concentrations, low vein densities are equally common among nonangiosperms throughout history and common enough to include forest canopies and not just obligate shade species that will always be of limited productivity. Modeling results can be reconciled with the fossil record if maximum assimilation rates of nonflowering plants are capped well below those of flowering plants, capturing biochemical and physiological differences that would be consistent with extant plants but previously unrecognized in the fossil record. Although previous photosynthetic modeling suggested that productivity would double or triple with each Phanerozoic transition from low to high CO 2 , productivity changes are likely to have been limited before a substantial increase accompanying the evolution of flowering plants. Role of CO 2 in Plant Evolution and Productivity over Geological Time ScalesA tmospheric CO 2 concentrations have fluctuated greatly over the past 400 million years: CO 2 levels are thought to have decreased by a factor of 10 or more as a result of the Devonian evolution of deep rooting plants and, subsequently, to have varied between levels somewhat less than and fivefold greater than preindustrial levels (1, 2). Just as land plant evolution has been a primary driver of these changes, in turn, CO 2 has often been assigned a dominant role in plant evolution. CO 2 changes have been implicated for the radiation of vascular plants, seed plants, and flowering plants; for the spread of C 4 photosynthesis and grasslands; and for the evolution of arborescence and both laminate leaves in general and the high vein density leaves of angiosperms in particular (3-12). Furthermore, models of plant function have repeatedly predicted that large swings in terrestrial productivity of 200-300% accompany these changes in atmospheric CO 2 (13-16).Plants require CO 2 , and productivity can be adversely affected by the CO 2 minima of the recent geological past that have approached the CO 2 compensation point for plant growth (17, 18), but did the positive relationship with CO 2 carry to a doubling or tripling of current productivity during the Mesozoic highs in CO 2 concentration? This suggestion raises a number of complications. Fo...

Weak coordination among petiole, leaf, vein, and gas‐exchange traits across Australian angiosperm species and its possible implications

“…2008; Boyce et al. 2009; Boyce and Zwieniecki 2012; Brodribb et al. 2013; Feild and Brodribb 2013; Sack et al.…”

“…Photosynthesis might saturate at low vein densities (ca <2 mm·mm −2 ) if CO 2 assimilation becomes either biochemically limited (e.g., Rubisco‐mediated carboxylation capacity; Vcmax) or becomes limited by the maximal rates of CO 2 conductance through stomata and mesophyll tissue, rather than by the supply of water delivered via the vein network (Boyce and Zwieniecki 2012). Our data are in rough agreement with this idea, considering that all but two of our species exhibited vein densities >8 mm·mm −2 .…”

Paleophysiology: From Fossils to the Future

“…Before the mid-Cretaceous (110-100 Ma), photosynthetic capacity was evidently low, as indicated by low vein densities on fossil leaves. Thereafter, with the evolution of angiosperms (especially dicots), it increased three-to fourfold as conducting structures became smaller [67,71]. This transition began when CO 2 levels were high but continued as those levels reduced during the Cenozoic [67], in part because angiosperms and, to a lesser extent, gymnosperms achieved active control over stomatal opening and closing [72][73][74].…”

“…One of the most useful proxies for inferring paleophysiology has been established in land plants. Experiments have demonstrated a fundamental link between the density of veins (total vein length per unit leaf area) and photosynthetic capacity [67][68][69][70]. Before the mid-Cretaceous (110-100 Ma), photosynthetic capacity was evidently low, as indicated by low vein densities on fossil leaves.…”

Diversity in neotropical wet forests during the Cenozoic is linked more to atmospheric CO 2 than temperature

“…angiosperms, the dominant group in the pollen record), diversity should be stimulated by CO 2 , but across groups large differences in physiological performance may cause one group to outcompete another when CO 2 drops. In fact, because of their uniquely high photosynthetic rates, angiosperms may be the only plant group whose productivity is strongly stimulated by CO 2 [40], and by extension whose diversity is positively linked to CO 2 . Additional palaeobotanical studies with non-angiosperm groups are needed to test this physiological prediction.…”