Pit membrane structure is highly variable and accounts for a major resistance to water flow through tracheid pits in stems and roots of two boreal conifer species

The flow of xylem sap in conifers is strongly dependent on the presence of a low resistance path through bordered pits, particularly through the pores present in the margo of the pit membrane. A computational fluid dynamics approach was taken, solving the Navier–Stokes equation for models based on the geometry of pits observed in tracheids from stems and roots of Picea mariana (black spruce) and Picea glauca (white spruce). Model solutions demonstrate a close, inverse relationship between the total resistance of bordered pits and the total area of margo pores. Flow through the margo was dominated by a small number of the widest pores. Particularly for pits where the margo component of flow resistance was low relative to that of the torus, pore location near the inner edge of the margo allowed for greater flow than that occurring through similar-sized pores near the outer edge of the margo. Results indicate a surprisingly large variation in pit structure and flow characteristics. Nonetheless, pits in roots have lower resistance to flow than those in stems because the pits were wider and consisted of a margo with a larger area in pores

Hydraulic consequences of vessel evolution in angiosperms

We tested two hypotheses for how vessel evolution in angiosperms influenced xylem function. First, the transition to vessels decreased resistance to flow-often considered the driving force for their evolution. Second, the transition to vessels compromised safety from cavitation-a constraint emerging from the \"pit area hypothesis\" for vulnerability to cavitation. Data were obtained from branch wood of 17 basal taxa with vessels and two eudicots possessing \"primitive\" perforation plates. Results were compared with previous data from vesselless angiosperms and eudicots with simple perforation plates. Contrary to the first hypothesis, basal taxa did not have significantly lower sapwood-specific resistivity than vesselless angiosperms, despite vessels being wider than tracheids. Eudicot resistivity was ca. 4.5 times lower. On a vessel-area basis, resistivity of \"primitive\" vessels (435 +/- 104 MPa s m(-2)) was lower than angiosperm tracheids (906 +/- 89 MPa s m(-2)) but still greater than eudicot vessels (91 +/- 9 MPa s m(-2)). High resistivity of primitive vessels could be attributed to their being shorter per diameter than eudicots and to high perforation plate resistivity (57% 6 15% of total) in the species with scalariform plates. In support of the second hypothesis, primitive vessels had a cavitation pressure 1.4 MPa more vulnerable than angiosperm tracheids. This \"vulnerability bottleneck\" may have been even more extreme without a shift in vessels to less porous interconduit pit membranes. Vessel evolution was not driven by lower flow resistance, and it may have been limited to wet habitats by cavitation risk. A subtle, context-dependent advantage to primitive vessels is consistent with the distribution of the vesselless condition in the angiosperm tree. The results imply that truly efficient and safe vessels evolved much later than vessels per se, perhaps in concordance with larger radiations among core angiosperms

Water transport in vesselless angiosperms: conducting efficiency and cavitation safety

Two structure-function hypotheses were tested for vesselless angiosperm wood. First, vesselless angiosperm wood should have much higher flow resistance than conifer wood because angiosperm tracheids lack low-resistance torus-margo pits. Second, vesselless wood ought to be exceptionally safe from cavitation if the small cumulative area of pits between tracheids confers safety (the pit area hypothesis). Data were obtained from branch wood of 19 vesselless angiosperms: Amborella trichopoda, Trochodendron aralioides, Tetracentron sinense, and 16 Winteraceae from Tasmannia, Zygogynum, Bubbia, Pseudowintera, and Drimys. Contrary to the first hypothesis, vesselless and conifer species with narrow tracheids (below ca. 18 mu m) had similar area-specific resistivities. The reason was that vesselless angiosperms had an intertracheid pit resistance (mean 16 +/- 2 MPa s m(-1)) that was nearly as low as that of conifers (6 +/- 1 MPa s m(-1)) and much lower than that of eudicot intervessel pits ( 336 +/- 81 MPa s m(-1)). Low pit resistance was associated with greater pit membrane porosity inferred from scanning electron microscopy observations and silicone penetration and may represent incipient pit membrane loss. Pit resistance was often greater in wider angiosperm tracheids and obscured any drop in wood resistivity with tracheid width. In support of the second hypothesis, vesselless woods averaged a cavitation pressure of -3.4 +/- 0.3 MPa, which is low for their wet habitats. In agreement with the pit area hypothesis, resistance to cavitation increased with decreasing total pit area between conduits. However, vesselless angiosperms were more vulnerable for a given pit area than eudicots, consistent with their more permeable pit membranes. Small total pit area between conduits may allow angiosperm tracheids to have more porous membranes for conducting efficiency without creating a cavitation problem

A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

Widespread tree mortality associated with drought 92 has been observed on all forested continents, and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere-atmosphere interactions of carbon, water, and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analyzed across species and biomes using a standardized physiological framework. Here we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function

A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

Widespread tree mortality associated with drought 92 has been observed on all forested continents, and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere-atmosphere interactions of carbon, water, and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analyzed across species and biomes using a standardized physiological framework. Here we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function

Responses of wood anatomy and carbon isotope composition of Quercus pubescens saplings subjected to two consecutive years of summer drought

International audienceTo withstand and to recover from severe summer drought is crucial for trees, as dry periods are predicted to occur more frequently over the coming decades.* In order to better understand growth-related tree responses to drought, wood formation, vessel characteristics and stable carbon isotope composition (δ13C) in tree rings of Quercus pubescens saplings imposed to two consecutive summer droughts were compared with regularly watered control trees.* In both years, photosynthetic activity was strongly inhibited during the drought periods of five to seven weeks but quickly restored after re-watering, reinitiating wood formation. Stress caused more than a 20% reduction in ring width, a 0.5‰ increase in latewood δ13C and changes in vessels characteristics in both the current year latewood and the next year earlywood. The latewood displayed up to 90% increased hydraulic conductivity than control trees, likely to compensate for a cavitation-induced reduction of water transport.* The earlywood after the first drought year was characterized by more but smaller vessels suggesting the attempt of restoring conductivity while minimizing the risk of hydraulic failure. However, after the second year, the reduction of hydraulic conductivity and the increased δ13C values indicate a structural adjustment towards a reduced growth induced by exhaustion of carbon reserves