The flowering plants that dominate modern vegetation possess leaf gas exchange potentials that far exceed those of all other living or extinct plants. The great divide in maximal ability to exchange CO 2 for water between leaves of nonangiosperms and angiosperms forms the mechanistic foundation for speculation about how angiosperms drove sweeping ecological and biogeochemical change during the Cretaceous. However, there is no empirical evidence that angiosperms evolved highly photosynthetically active leaves during the Cretaceous. Using vein density (D V ) measurements of fossil angiosperm leaves, we show that the leaf hydraulic capacities of angiosperms escalated severalfold during the Cretaceous. During the first 30 million years of angiosperm leaf evolution, angiosperm leaves exhibited uniformly low vein D V that overlapped the D V range of dominant Early Cretaceous ferns and gymnosperms. Fossil angiosperm vein densities reveal a subsequent biphasic increase in D V . During the first mid-Cretaceous surge, angiosperm D V first surpassed the upper bound of D V limits for nonangiosperms. However, the upper limits of D V typical of modern megathermal rainforest trees first appear during a second wave of increased D V during the Cretaceous-Tertiary transition. Thus, our findings provide fossil evidence for the hypothesis that significant ecosystem change brought about by angiosperms lagged behind the Early Cretaceous taxonomic diversification of angiosperms.angiosperm evolution | plant evolution | transpiration | tropical rainforest | venation P hotosynthesis and transpiration by leaves fundamentally influence the cycling of carbon and water in the terrestrial realm. Consequently, evolutionary changes in the rates at which leaves exchange water for carbon bear on the origin and maintenance of biodiversity by varying the size and resource stoichiometry of the primary productivity base. How leaves exchange gases also shape climate and atmospheric gas composition by changing the amounts of water vapor and carbon in the atmosphere (1-3). Recent evidence has suggested that the evolution of flowering plants involved a sharp rise in the capacity of leaves to transport water and extract CO 2 from the atmosphere (4, 5).The evolution of unrivaled CO 2 uptake and transpirational output by angiosperm leaves form the mechanistic cornerstone for a multitude of hypotheses citing angiosperms as agents of expansive ecosystem change during the Cretaceous (6-8). These hypotheses include (i) intensified mineral weathering by angiosperms that decreased global atmospheric CO 2 concentration; (ii) heightened transpirational input to the atmosphere that increased regional rainfall and favored the spread and diversity of tropical rainforest vegetation; (iii) the nearly complete competitive exclusion by angiosperms of diverse gymnosperms and ferns from high-productivity sites worldwide; and (iv) the spread of novel fire regimes that entrained a positive feedback on angiosperm takeover (3,4,6,(9)(10)(11)(12)(13)(14)(15).
Leaves with high photosynthetic capacity require high transpiration capacity. Consequently, hydraulic conductance, stomatal conductance, and assimilation capacities should be positively correlated. These traits make independent demands on anatomical space, particularly due to the propensity for veins to have bundle sheath extensions that exclude stomata from the local epidermis. We measured density and area occupation of bundle sheath extensions, density and size of stomata and subsidiary cells, and venation density for a sample of extant angiosperms and fossil and living nonangiosperm tracheophytes. For most nonangiosperms, even modest increases in vein density and stomatal conductance would require substantial reconfigurations of anatomy. One characteristic of the angiosperm syndrome (e.g. small cell sizes, etc.) is hierarchical vein networks that allow expression of bundle sheath extensions in some, but not all veins, contrasting with all-or-nothing alternatives available with the single-order vein networks in most nonangiosperms. Bundle sheath modulation is associated with higher vein densities in three independent groups with hierarchical venation: angiosperms, Gnetum (gymnosperm) and Dipteris (fern). Anatomical and developmental constraints likely contribute to the stability in leaf characteristics - and ecophysiology - seen through time in different lineages and contribute to the uniqueness of angiosperms in achieving the highest vein densities, stomatal densities, and physiological rates.
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