Taylor S. Feild

Global convergence in the vulnerability of forests to drought.

Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow (<1 megapascal) hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk.

Leaf Maximum Photosynthetic Rate and Venation Are Linked by Hydraulics

Leaf veins are almost ubiquitous across the range of terrestrial plant diversity, yet their influence on leaf photosynthetic performance remains uncertain. We show here that specific physical attributes of the vascular plumbing network are key limiters of the hydraulic and photosynthetic proficiency of any leaf. Following the logic that leaf veins evolved to bypass inefficient water transport through living mesophyll tissue, we examined the hydraulic pathway beyond the distal ends of the vein system as a possible limiter of water transport in leaves. We tested a mechanistic hypothesis that the length of this final traverse, as water moves from veins across the mesophyll to where it evaporates from the leaf, governs the hydraulic efficiency and photosynthetic carbon assimilation of any leaf. Sampling 43 species across the breadth of plant diversity from mosses to flowering plants, we found that the post-vein traverse as determined by characters such as vein density, leaf thickness, and cell shape, was strongly correlated with the hydraulic conductivity and maximum photosynthetic rate of foliage. The shape of this correlation provided clear support for the a priori hypothesis that vein positioning limits photosynthesis via its influence on leaf hydraulic efficiency.

Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification

Angiosperm evolution transformed global ecology, and much of this impact derives from the unrivalled vegetative productivity of dominant angiosperm clades. However, the origins of high photosynthetic capacity in angiosperms remain unknown. In this study, we describe the steep trajectory of leaf vein density (D(v)) evolution in angiosperms, and predict that this leaf plumbing innovation enabled a major shift in the capacity of leaves to assimilate CO(2). Reconstructing leaf vein evolution from an examination of 504 angiosperm species we found a rapid three- to fourfold increase in D(v) occurred during the early evolution of angiosperms. We demonstrate how this major shift in leaf vein architecture potentially allowed the maximum photosynthetic capacity in angiosperms to rise above competing groups 140-100 Ma. Our data suggest that early terrestrial angiosperms produced leaves with low photosynthetic rates, but that subsequent angiosperm success is linked to a surge in photosynthetic capacity during their early diversification.

Angiosperm leaf vein evolution was physiologically and environmentally transformative

The veins that irrigate leaves during photosynthesis are demonstrated to be strikingly more abundant in flowering plants than in any other vascular plant lineage. Angiosperm vein densities average 8 mm of vein per mm2 of leaf area and can reach 25 mm mm−2, whereas such high densities are absent from all other plants, living or extinct. Leaves of non-angiosperms have consistently averaged close to 2 mm mm−2 throughout 380 million years of evolution despite a complex history that has involved four or more independent origins of laminate leaves with many veins and dramatic changes in climate and atmospheric composition. We further demonstrate that the high leaf vein densities unique to the angiosperms enable unparalleled transpiration rates, extending previous work indicating a strong correlation between vein density and assimilation rates. Because vein density is directly measurable in fossils, these correlations provide new access to the physiology of extinct plants and how they may have impacted their environments. First, the high assimilation rates currently confined to the angiosperms among living plants are likely to have been unique throughout evolutionary history. Second, the transpiration-driven recycling of water that is important for bolstering precipitation in modern tropical rainforests might have been significantly less in a world before the angiosperms.

Dark and disturbed: a new image of early angiosperm ecology

Abstract Better understanding of the functional biology of early angiosperms may clarify ecological factors surrounding their origin and early radiation. Phylogenetic studies identify Amborella, Nymphaeales (water lilies), Austrobaileyales, and Chloranthaceae as extant lineages that branched before the radiation of core angiosperms. Among living plants, these lineages may represent the best models for the ecology and physiology of early angiosperms. Here we combine phylogenetic reconstruction with new data on the morphology and ecophysiology of these plants to infer early angiosperm function. With few exceptions, Amborella, Austrobaileyales, and Chloranthaceae share ecophysiological traits associated with shady, disturbed, and wet habitats. These features include low and easily light-saturated photosynthetic rates, leaf anatomy related to the capture of understory light, small seed size, and clonal reproduction. Some Chloranthaceae, however, possess higher photosynthetic capacities and seedlings that recruit in canopy gaps and other sunny, disturbed habitats, which may have allowed Cretaceous Chloranthaceae to expand into more diverse environments. In contrast, water lilies possess ecophysiological features linked to aquatic, sunny habitats, such as absence of a vascular cambium, ventilating stems and roots, and floating leaves tuned for high photosynthetic rates in full sun. Nymphaeales may represent an early radiation into such aquatic environments. We hypothesize that the earliest angiosperms were woody plants that grew in dimly lit, disturbed forest understory habitats and/or shady streamside settings. This ecology may have restricted the diversity of pre-Aptian angiosperms and living basal lineages. The vegetative flexibility that evolved in the understory, however, may have been a key factor in their diversification in other habitats. Our inferences based on living plants are consistent with many aspects of the Early Cretaceous fossil record and can be tested with further study of the anatomy, chemistry, and sedimentological context of Early Cretaceous angiosperm fossils.

Viewing leaf structure and evolution from a hydraulic perspective

More than 40 000 km3 year–1 of water flows through the intricate hydraulic pathways inside leaves. This water not only sustains terrestrial productivity, but also constitutes nearly 70% of terrestrial evapotranspiration, thereby influencing both global and local climate (Chapin et al. 2002). Thus, the central role played by leaf vascular systems in terrestrial biology provides an important context for research into the function and evolution of water transport in leaves. Significant progress has been made recently towards understanding the linkages between anatomy and water transport efficiency in leaves, and these discoveries provide a novel perspective to view the evolution of land plants.

Pigment dynamics and autumn leaf senescence in a New England deciduous forest, eastern USA

The leaves of woody plants at Harvard Forest in Central Massachusetts, USA, changed color during senescence; 70% (62/89) of the woody species examined anatomically contained anthocyanins during senescence. Anthocyanins were not present in summer green leaves, and appeared primarily in the vacuoles of palisade parenchyma cells. Yellow coloration was a result of the unmasking of xanthophyll pigments in senescing chloroplasts. In nine red-senescing species, anthocyanins were not detectable in mature leaves, and were synthesized de novo in senescence, with less than 20 µg cm−2 of chlorophyll remaining. Xanthophyll concentrations declined in relation to chlorophyll to the same extent in both yellow- and red-leaved taxa. Declines in the maximum photosystem II quantum yield of leaves collected prior to dawn were only slightly less in the red-senescing species, indicating no long-term protective activity. Red-leaved species had significantly greater mass/area and lower chlorophyll a/b ratios during senescence. Nitrogen tissue concentrations in mature and senescent leaves negatively correlated to anthocyanin concentrations in senescent leaves, weak evidence for more efficient nitrogen resorption in anthocyanic species. Shading retarded both chlorophyll loss and anthocyanin production in Cornus alternifolia, Acer rubrum, Acer saccharum, Quercus rubra and Viburnum alnifolium. It promoted chlorophyll loss in yellow-senescing Fagus grandifolia. A reduced red : far-red ratio did not affect this process. Anthocyanins did not increase leaf temperatures in Q. rubra and Vaccinium corymbosum on cold and sunny days. The timing of leaf-fall was remarkably constant from year to year, and the order of senescence of individual species was consistent.

Evolution of stomatal responsiveness to CO2 and optimization of water‐use efficiency among land plants

The stomata of angiosperms respond to changes in ambient atmospheric concentrations of CO(2) (C(a)) in ways that appear to optimize water-use efficiency. It is unknown where in the history of land plants this important stomatal control mechanism evolved. Here, we test the hypothesis that major clades of plants have distinct stomatal sensitivities to C(a) reflecting a relatively recent evolution of water-use optimization in derived angiosperms. Responses of stomatal conductance (g(s)) to step changes between elevated, ambient and low C(a) (600, 380 and 100 micromol mol(-1), respectively) were compared in a phylogenetically and ecologically diverse range of higher angiosperms, conifers, ferns and lycopods. All species responded to low C(a) by increasing g(s) but only angiosperm stomata demonstrated a significant closing response when C(a) was elevated to 600 micromol mol(-1). As a result, angiosperms showed significantly greater increases in water-use efficiency under elevated C(a) than the other lineages. The data suggest that the angiosperms have mechanisms for detecting and responding to increases in C(a) that are absent from earlier diverging lineages, and these mechanisms impart a greater capacity to optimize water-use efficiency.

Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution

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 CO2 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 (DV) measurements of fossil angiosperm leaves, we show that the leaf hydraulic capacities of angiosperms escalated several-fold during the Cretaceous. During the first 30 million years of angiosperm leaf evolution, angiosperm leaves exhibited uniformly low vein DV that overlapped the DV range of dominant Early Cretaceous ferns and gymnosperms. Fossil angiosperm vein densities reveal a subsequent biphasic increase in DV. During the first mid-Cretaceous surge, angiosperm DV first surpassed the upper bound of DV limits for nonangiosperms. However, the upper limits of DV typical of modern megathermal rainforest trees first appear during a second wave of increased DV 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.

Stem water transport and freeze-thaw xylem embolism in conifers and angiosperms in a Tasmanian treeline heath

The effect of freezing on stem xylem hydraulic conductivity and leaf chlorophyll a fluorescence was measured in 12 tree and shrub species from a treeline heath in Tasmania, Australia. Reduction in stem hydraulic conductivity after a single freeze-thaw cycle was minimal in conifers and the vessel-less angiosperm species Tasmannia lanceolata (Winteraceae), whereas mean loss of conductivity in vessel-forming angiosperms fell in the range 17–83%. A positive linear relationship was observed between percentage loss of hydraulic conductivity by freeze-thaw and the average conduit diameter across all 12 species. This supports the hypothesis that large-diameter vascular conduits have a greater likelihood of freeze-thaw cavitation because larger bubbles are produced, which are more likely to expand under tension. Leaf frost tolerances, as measured by a 50% loss of maximum PSII quantum yield, varied from –6 to –13°C, indicating that these species were more frost-sensitive than plants from northern hemisphere temperate forest and treeline communities. There was no evidence of a relationship between frost tolerance of leaves and the resilience of stem water transport to freezing, suggesting that low temperature survival and the resistance of stem water transport to freezing are independently evolving traits. The results of this study bear on the ecological importance of stem freezing in the southern hemisphere treeline zones.