Research on the degree to which carbon (C) availability limits growth in trees, as well as recent trends in climate change and concurrent increases in drought-related tree mortality, have led to a renewed focus on the physiological mechanisms associated with tree growth responses to current and future climate. This has led to some dispute over the role of stored non-structural C compounds as indicators of a tree's current demands for photosynthate. Much of the uncertainty surrounding this issue could be resolved by developing a better understanding of the potential functions of non-structural C stored within trees. In addition to functioning as a buffer to reconcile temporal asynchrony between C demand and supply, the storage of non-structural C compounds may be under greater regulation than commonly recognized. We propose that in the face of environmental stochasticity, large, long-lived trees may require larger C investments in storage pools as safety margins than previously recognized, and that an important function of these pools may be to maintain hydraulic transport, particularly during episodes of severe stress. If so, survival and long-term growth in trees remain a function of C availability. Given that drought, freeze-thaw events and increasing tree height all impose additional constraints on vascular transport, the common trend of an increase in non-structural carbohydrate concentrations with tree size, drought or cold is consistent with our hypothesis. If the regulated maintenance of relatively large constitutive stored C pools in trees serves to maintain hydraulic integrity, then the minimum thresholds are expected to vary depending on the specific tissues, species, environment, growth form and habit. Much research is needed to elucidate the extent to which allocation of C to storage in trees is a passive vs. an active process, the specific functions of stored C pools, and the factors that drive active C allocation to storage.

We investigated how water transport capacity, wood density and wood anatomy were related to leaf photosynthetic traits in two lowland forests in Panama. Leaf-specific hydraulic conductivity (k L ) of upper branches was positively correlated with maximum rates of net CO 2 assimilation per unit leaf area (A area ) and stomatal conductance (g s ) across 20 species of canopy trees. Maximum k L showed stronger correlation with A area than initial k L suggesting that allocation to photosynthetic potential is proportional to maximum water transport capacity. Terminal branch k L was negatively correlated with A area /g s and positively correlated with photosynthesis per unit N, indicating a trade-off of efficient use of water against efficient use of N in photosynthesis as water transport efficiency varied. Specific hydraulic conductivity calculated from xylem anatomical characteristics (k theoretical ) was positively related to A area and k L , consistent with relationships among physiological measurements. Branch wood density was negatively correlated with wood water storage at saturation, k L , A area , net CO 2 assimilation per unit leaf mass (A mass ), and minimum leaf water potential measured on covered leaves, suggesting that wood density constrains physiological function to specific operating ranges. Kinetic and static indices of branch water transport capacity thus exhibit considerable co-ordination with allocation to potential carbon gain. Our results indicate that understanding tree hydraulic architecture provides added insights to comparisons of leaf level measurements among species, and links photosynthetic allocation patterns with branch hydraulic processes.

Summary1. The xylem pressure inducing 50% loss of hydraulic conductivity due to embolism (P 50 ) is widely used for comparisons of xylem vulnerability among species and across aridity gradients. However, despite its utility as an index of resistance to catastrophic xylem failure under extreme drought, P 50 may have no special physiological relevance in the context of stomatal regulation of daily minimum xylem pressure and avoidance of hydraulic failure under non-extreme conditions. Moreover, few studies of hydraulic architecture have accounted for the buffering influence of tissue hydraulic capacitance on daily fluctuations in xylem pressure in intact plants. 2. We used data from 104 coniferous and angiosperm species representing a range of woody growth forms and habitat types to evaluate trends in three alternative xylem hydraulic safety margins based on features of their stem xylem vulnerability curves and regulation of daily minimum stem water potential (W stem min ) under non-extreme conditions: (i) W stem min ) P 50 , (ii) W stem min ) P e , the difference between W stem min and the threshold xylem pressure at which loss of conductivity begins to increase rapidly (P e ) and (iii) P e ) P 50 , an estimate of the steepness of the vulnerability curve between P e and P 50 . Additionally, we assessed relationships between xylem capacitance, species-specific set-points for daily minimum stem water potential and hydraulic safety margins in a subset of species for which relevant data were available. 3. The three types of hydraulic safety margin defined increased with decreasing species-specific set-points for W stem min , suggesting a diminishing role of stem capacitance in slowing fluctuations in xylem pressure as W stem min became more negative. The trends in hydraulic safety were similar among coniferous and angiosperm species native to diverse habitat types. 4. Our results suggest that here is a continuum of relative reliance on different mechanisms that confer hydraulic safety under dynamic conditions. Species with low capacitance and denser wood experience greater daily maximum xylem tension and appear to rely primarily on xylem structural features to avoid embolism, whereas in species with high capacitance and low wood density avoidance of embolism appears to be achieved primarily via reliance on transient release of stored water to constrain transpiration-induced fluctuations in xylem tension.

Tree hydraulic architecture exhibits patterns that propagate from tissue to tree scales. A challenge is to make sense of these patterns in terms of trade-offs and adaptations. The universal trend for conduits per area to decrease with increasing conduit diameter below the theoretical packing limit may reflect the compromise between maximizing the area for conduction versus mechanical support and storage. Variation in conduit diameter may have two complementary influences: one being compromises between efficiency and safety and the other being that conduit tapering within a tree maximizes conductance per growth investment. Area-preserving branching may be a mechanical constraint, preventing otherwise more efficient top-heavy trees. In combination, these trends beget another: trees have more, narrower conduits moving from trunks to terminal branches. This pattern: (1) increases the efficiency of tree water conduction; (2) minimizes (but does not eliminate) any hydraulic limitation on the productivity or tissue growth with tree height; and (3) is consistent with the scaling of tree conductance and sap flow with size. We find no hydraulic reason why tree height should scale with a basal diameter to the two-thirds power as recently claimed; it is probably another mechanical constraint as originally proposed. The buffering effect of capacitance on the magnitude of transpiration-induced xylem tension appears to be coupled to cavitation resistance, possibly alleviating safety versus efficiency trade-offs.

Weighing lysimeters, large-tree potometers, ventilated chambers, radioisotopes, stable isotopes and an array of heat balance/heat dissipation methods have been used to provide quantitative estimates of whole-tree water use. A survey of 52 studies conducted since 1970 indicated that rates of water use ranged from 10 kg day(-1) for trees in a 32-year-old plantation of Quercus petraea L. ex Liebl. in eastern France to 1,180 kg day(-1) for an overstory Euperua purpurea Bth. tree growing in the Amazonian rainforest. The studies included in this survey reported whole-tree estimates of water use for 67 species in over 35 genera. Almost 90% of the observations indicated maximum rates of daily water use between 10 and 200 kg day(-1) for trees that averaged 21 m in height. The thermal techniques that made many of these estimates possible have gained widespread acceptance, and energy-balance, heat dissipation and heat-pulse systems are now routinely used with leaf-level measurements to investigate the relative importance of stomatal and boundary layer conductances in controlling canopy transpiration, whole-tree hydraulic conductance, coordinated control of whole-plant water transport, movement of water to and from sapwood storage, and whole-plant vulnerability of water transport to xylem cavitation. Techniques for estimating whole-tree water use complement existing approaches to calculating catchment water balance and provide the forest hydrologist with another tool for managing water resources. Energy-balance, heat dissipation and heat-pulse methods can be used to compare transpiration in different parts of a watershed or between adjacent trees, or to assess the contribution of transpiration from overstory and understory trees. Such studies often require that rates of water use be extrapolated from individual trees to that of stands and plantations. The ultimate success of this extrapolation depends in part on whether data covering short time sequences can be applied to longer periods of time. We conclude that techniques for estimating whole-tree water use have provided valuable tools for conducting basic and applied research. Future studies that emphasize the use of these techniques by both tree physiologists and forest hydrologists should be encouraged.