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 Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely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.
Ecology letters (2010) 13: 175-183 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 (Dv) evolution in angiosperms, and predict that this leaf plumbing innovation enabled a major shift in the capacity of leaves to assimilate CO₂. Reconstructing leaf vein evolution from an examination of 504 angiosperm species we found a rapid three- to fourfold increase in Dv 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.
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.
The evolution of lignified xylem allowed for the efficient transport of water under tension, but also exposed the vascular network to the risk of gas emboli and the spread of gas between xylem ...conduits, thus impeding sap transport to the leaves. A well‐known hypothesis proposes that the safety of xylem (its ability to resist embolism formation and spread) should trade off against xylem efficiency (its capacity to transport water). We tested this safety–efficiency hypothesis in branch xylem across 335 angiosperm and 89 gymnosperm species. Safety was considered at three levels: the xylem water potentials where 12%, 50% and 88% of maximal conductivity are lost. Although correlations between safety and efficiency were weak (r² < 0.086), no species had high efficiency and high safety, supporting the idea for a safety–efficiency tradeoff. However, many species had low efficiency and low safety. Species with low efficiency and low safety were weakly associated (r² < 0.02 in most cases) with higher wood density, lower leaf‐ to sapwood‐area and shorter stature. There appears to be no persuasive explanation for the considerable number of species with both low efficiency and low safety. These species represent a real challenge for understanding the evolution of xylem.
Increases in drought‐induced tree mortality are being observed in tropical rain forests worldwide and are also likely to affect the geographical distribution of tropical vegetation. However, the ...mechanisms underlying the drought vulnerability and environmental distribution of tropical species have been little studied. We measured vulnerability to xylem embolism (P50) of 13 woody species endemic to New Caledonia and with different xylem conduit morphologies. We examined the relation between P50, along with other leaf and xylem functional traits, and a range of habitat variables. Selected species had P50 values ranging between −4.03 and −2.00 MPa with most species falling in a narrow range of resistance to embolism above −2.7 MPa. Embolism vulnerability was significantly correlated with elevation, mean annual temperature and percentage of species occurrences located in rain forest habitats. Xylem conduit type did not explain variation in P50. Commonly used functional traits such as wood density and leaf traits were not related to embolism vulnerability. Xylem embolism vulnerability stands out among other commonly used functional traits as a major driver of species environmental distribution. Drought‐induced xylem embolism vulnerability behaves as a physiological trait closely associated with the habitat occupation of rain forest woody species.
Increases in drought‐induced tree mortality are being observed in tropical rain forests worldwide and are also likely to affect the geographical distribution of tropical vegetation. However, the mechanisms underlying the drought vulnerability and environmental distribution of tropical species have been little studied. Trueba et al. measured vulnerability to xylem embolism, along with other easy‐to‐measure wood and leaf functional traits, of 13 species endemic to the tropical archipelago of New Caledonia. This study shows that xylem embolism vulnerability stands out among other functional traits as a major driver of species environmental distribution. Drought‐induced xylem embolism vulnerability behaves as a physiological trait closely associated with the habitat occupation of rain forest woody species.
High vein density (DV) evolution in angiosperms represented a key functional transition. Yet, a mechanistic account on how this hydraulic transformation evolved remains lacking. We demonstrate that a ...consequence of producing high DV is that veins must become very small to fit inside the leaf, and that angiosperms are the only clade that evolved the specific type of vessel required to yield sufficiently conductive miniature leaf veins. From 111 species spanning key divergences in vascular plant evolution, we show, using analyses of vein conduit evolution in relation to vein packing, that a key xylem innovation associated with high DV evolution is a strong reduction in vein thickness and simplification of the perforation plates of primary xylem vessels. Simple perforation plates in the leaf xylem occurred only in derived angiosperm clades exhibiting high DV (> 12 mm mm⁻²). Perforation plates in the vessels of other species, including extant basal angiosperms, consisted of resistive scalariform types that were associated with thicker veins and much lower DV. We conclude that a reduction in within‐vein conduit resistance allowed vein size to decrease. We suggest that this adaptation may have been a critical evolutionary step that enabled dramatic DV elaboration in angiosperms.
More than 40000km³ 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.
Leaf water contains naturally occurring stable isotopes of oxygen and hydrogen in abundances that vary spatially and temporally. When sufficiently understood, these can be harnessed for a wide range ...of applications. Here, we review the current state of knowledge of stable isotope enrichment of leaf water, and its relevance for isotopic signals incorporated into plant organic matter and atmospheric gases. Models describing evaporative enrichment of leaf water have become increasingly complex over time, reflecting enhanced spatial and temporal resolution. We recommend that practitioners choose a model with a level of complexity suited to their application, and provide guidance. At the same time, there exists some lingering uncertainty about the biophysical processes relevant to patterns of isotopic enrichment in leaf water. An important goal for future research is to link observed variations in isotopic composition to specific anatomical and physiological features of leaves that reflect differences in hydraulic design. New measurement techniques are developing rapidly, enabling determinations of both transpired and leaf water δ18O and δ2H to be made more easily and at higher temporal resolution than previously possible. We expect these technological advances to spur new developments in our understanding of patterns of stable isotope fractionation in leaf water.
Brief Summary Statement
Leaf water contains naturally occurring stable isotopes of oxygen and hydrogen in abundances that vary spatially and temporally. When sufficiently understood, these can be harnessed for a wide range of applications. Here, we review the current state of knowledge of evaporative enrichment of heavy isotopes in leaf water, and its relevance for isotopic signals incorporated into plant organic matter and atmospheric gases.
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.
• Premise of the study: Phylogenetic incongruence between "gene trees" and "species trees" has been widely acknowledged in phylogenetic research. Conflicts may emerge from several processes including ...paralogy, hybridization, and incomplete lineage sorting. Although phylogenetic incongruence appears common, its impact on many phylogeny-based analyses remains poorly understood. • Methods: We examined the occurrence of phylogenetic conflict between nuclear (ribosome ITS) and plastid (rbcL, trnL-F, rpl20-rpsl2, and rps16 intron) loci in the ancient angiosperm family Chloranthaceae. Then we investigated how phylogenetic conflict bears on taxonomie classification within the family as well as on inferences on biogeographical history, floral evolution, and measures of phylogenetic diversity (PD). • Key results: We found evidence for significant phylogenetic incongruence between plastid and nuclear data in the genus Hedyosmum. Within Hedyosmum, our results did not support previous subgeneric classification of the genus. Division of sections within subgenus Tafalla was supported by the ITS data but not by the plastid data set. As a consequence, we showed that inferring the evolution of key floral characters and geographical history within Hedyosmum depends on the phylogenetic data used. Both data sets yielded similar PD measures across genera, but we found contrasting PD measures in Hedyosmum, even after correcting for rate heterogeneity. • Conclusions: Our study demonstrated that phylogenetic conflict not only affects the inference of organismal relationships but also impacts our understanding of biogeographical history, morphological evolution, and phylogenetic diversity.
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