Fossil evidence for low gas exchange capacities for Early Cretaceous angiosperm leaves

Abstract

The photosynthetic gas exchange capacities of early angiosperms remain enigmatic. Nevertheless, many hypotheses about the causes of early angiosperm success and how angiosperms influenced Mesozoic ecosystem function hinge on understanding the maximum capacity for early angiosperm metabolism. We applied structure-functional analyses of leaf veins and stomatal pore geometry to determine the hydraulic and diffusive gas exchange capacities of Early Cretaceous fossil leaves. All of the late Aptian—early Albian angiosperms measured possessed low vein density and low maximal stomatal pore area, indicating low leaf gas exchange capacities in comparison to modern ecologically dominant angiosperms. Gas exchange capacities for Early Cretaceous angiosperms were equivalent or lower than ferns and gymnosperms. Fossil leaf taxa from Aptian to Paleocene sediments previously identified as putative stem-lineages to Austrobaileyales and Chloranthales had the same gas exchange capacities and possibly leaf water relations of their living relatives. Our results provide fossil evidence for the hypothesis that high leaf gas exchange capacity is a derived feature of later angiosperm evolution. In addition, the leaf gas exchange functions of austrobaileyoid and chloranthoid fossils support the hypothesis that comparative research on the biology of living basal angiosperm lineages reveals genuine signals of Early Cretaceous angiosperm ecophysiology.

Recurrent patterns of phylogenetic habitat filtering in woody plant communities across phytogeographically distinct grassland-forest ecotones

“…This pattern likely reflects their lower efficiency in water use and photosynthetic capacity when compared to other angiosperms of more recent diversification (Boyce et al 2009, Brodribb andFeild 2010). Basal angiosperms, such as Magnolianae, have a tendency to have lower density of leaf veins (Boyce et al 2009), low capacity of gas exchange (Feild et al 2011) and low photosynthetic capacity (Brodribb and Feild 2010), when compared to angiosperms of more recent diversification as Rosanae and Asteranae. Such characteristics of basal clades may probably confer plants tolerance to drought, since mechanisms to avoid water loss in environments of high rates of evapotranspiration are less efficient.…”

Rise to dominance of angiosperm pioneers in European Cretaceous environments

“…One may question whether the earliest angiosperms were shade tolerant as proposed by the "damp, dark, and disturbed habitats" hypothesis (36,38). An ecophysiological study of hypothetical living relatives of the zone I Potomac (Aptian-Albian) group angiosperms indicates that, if the assumed living related angiosperms are a good model of the physiology of the earliest angiosperms, they may have been shade tolerant (40). Furthermore, the three phases proposed here for the angiosperm rise to dominance show an interesting synchronism with the progressive increase of escalation in angiosperm leaf hydraulic capacity also noted by Feild et al (41) that reflects an escalation in ecological range.…”

The Developmental Basis of Stomatal Density and Flux

“…The g max estimated this way strongly predicted the operating stomatal conductance measured with leaf gas exchange systems (g op ) across Arabidopsis (Arabidopsis thaliana) genotypes under low CO 2 , high humidity, and high red and blue light (Dow et al, 2014). However, across diverse species, the g max values estimated by Equation 2 tend to be much higher than g op (Feild et al, 2011;McElwain et al, 2016) for several reasons. First, for typical leaves transpiring even under the best conditions, the effective area of the stomatal pore (a') is smaller than the anatomical maximum a max , by an amount that varies across species, particularly as the actual pore geometry usually deviates from simplified cylindrical geometry (Franks and Farquhar, 2007).…”

“…Second, as guard cells close under adverse conditions, a' declines (Fanourakis et al, 2015). Third, there may be a substantial contribution of diffusion resistances in the intercellular airspaces, especially in the case of a partly cutinized substomatal chamber (Roth-Nebelsick, 2007;Feild et al, 2011). Fourth, leaf surface features such as hairs or papillae surrounding the stomata, or encryption of stomata, may affect the diffusion through stomata, and especially will influence the boundary layer, which in addition to stomatal conductance determines overall diffusional conductance and therefore gas exchange (Kenzo et al, 2008;Hassiotou et al, 2009;Maricle et al, 2009).…”