On xylem hydraulic efficiencies, wood space-use and the safety-efficiency tradeoff: Comment on Gleason etal. (2016) 'Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species'.

Abstract

In a recent issue of New Phytologist, Gleason et al. (2016) compiled a remarkable data set of wood traits to investigate the tradeoffs between xylem hydraulic safety and xylem hydraulic efficiency, measured as xylem specific hydraulic conductivity (Ks; molH20 mlength s−1 mtranversal−2 Pa−1). This tradeoff is expected and somewhat studied at the conduit level, but how this should propagate to other plant levels is not known. In their paper, Gleason et al. (2016) compared the relationship between two tissue level traits emerging from conduit level traits, hydraulic safety, and Ks, to test for this tradeoff. The authors show conclusively that it is not possible to have high efficiency and high safety in plant hydraulic systems. Nevertheless, many species present low efficiency and low safety, which suggests the existence of other axes of variation affecting hydraulic efficiency and safety. In a commentary in the same issue of New Phytologist, Brodersen (2016) highlights the complexity of traits and contexts that may be affecting the hydraulic and safety tradeoff. Brodersen (2016) also proposes that there may actually be other traits that can better represent hydraulic safety. Here, we look at other xylem hydraulic efficiencies that may help explain Gleason et al.'s (2016) results and propose new questions. Efficiency may be defined as achieving maximum productivity with minimum wasted effort or expense (Oxford Dictionaries, 2015). What kind of efficiency is measured by Ks? What ‘waste’ is reduced by increasing this efficiency? Here Ks is flow per unit area and unit pressure gradient. Unit pressure gradient can be considered as longitudinal xylem efficiency, as higher longitudinal efficiency leads to smaller pressure gradients and higher Ks. Then Ks integrates transversal and longitudinal water supply efficiency. This can be clearly seen in the following sentence of Gleason et al. (2016, p. 132) ‘efficient xylem can transport the same volume of water as inefficient xylem, but does so with a smaller cross-section of living wood’, or, we add, can transport the same volume of water as inefficient xylem through longer wood section, or, yet, can supply a greater leaf area with the same wood diameter and height. Thus Ks is a measure of space-use efficiency and possible tradeoffs or relations should be analyzed from the viewpoint of wood space use. By redefining what efficiency we are actually measuring, many new questions arise from Gleason et al. (2016). First, acknowledging that the authors compared hydraulic space-use efficiency, we can rather say that there is a weak (r2 < 0.09) tradeoff between hydraulic space use of 0.4–1.0 cm branches (data selection criterion used) and hydraulic safety. Either, space of branches of this size class is not under selection (they can increase or decrease branch length/diameter freely or with small consequences), or other tradeoffs are acting. For example, branches of wider diameter have a longer diffusive pathway to O2, which may limit O2 supply to living cells (Hook et al., 1972) whereas smaller diameter branches have a larger area to volume ratio with possible consequences related to stem photosynthesis (Schmitz et al., 2012; Wittmann & Pfanz, 2014). An implicit assumption of Gleason et al. (2016) and many other studies is that higher Ks should be selected because it has a lower energetic cost. Considering that hydraulic space-use efficiency is different from energy-use efficiency, should higher Ks imply higher energy efficiency? At a first glance this is true as higher Ks can allow for a plant to reduce its volume of wood and this should lead to a relationship between Ks and stem and branch diameters. But the real picture may be more complex and, to our knowledge, the energy cost of a plant water-transport system has never been measured (but see the analysis of mass-specific hydraulic conductance and the cost of being higher in Mencuccini (2003)). If the assumption that higher Ks also leads to lower energetic costs is not always true, higher Ks would be free to vary in the boundaries set by hydraulic safety, as seen in Fig. 2 of Gleason et al. (2016). As Ks is a space-use efficiency and is not necessarily related to energetic efficiency, would there be situations where wood space is under selection that are not related to energetic costs? We believe that to understand Ks variability we have to look at factors that (1) limit available wood space or (2) affect wood space use. Considering point (1), we ask, when is wood space limiting to plants? When can plants afford to avoid regulating hydraulic conductance by either having larger cross-sectional area and/or smaller lengths? While space limitations on 0.4–1.0 cm branches, as in Gleason et al.'s (2016) data, may not seem to be directly limiting to plants, root space is probably limiting because smaller roots can better penetrate the soil and increase surface area (Chimungu et al., 2015). At the same time, due to allometric scaling, space limitations or constraints on stem size may be projected to branch size, or vice-versa, and space limitations may actually be indirectly affecting small branches (Sperry et al., 2008; Savage et al., 2010). Also, as Larjavaara & Muller-Landau (2010) notice, changing stem and branch diameter would allometrically change bark surface and thus bark functioning may be constraining wood space. Regarding point (2), Ks depends both on fractional space allocated to conduits and on the efficiency of the conduits present in this space. Space allocation to conduits thus necessarily conflicts with space allocation to parenchyma, fibers and cell walls. Any situation that constrains fiber and parenchyma allocation must tradeoff with space available for conduits. Changes in conduit number and efficiency may accommodate for increases or decreases in conduit-available space to regulate Ks and this is actually an interesting pathway for future research. Maybe the crucial question regarding hydraulic space-use efficiency would be what other functions are related to wood space? One way to approach this question is to partition Ks between the different tissues that are invested to sustain hydraulic conductance (Fig. 1). Then Ks as a measure of total space invested to conductance integrates fiber, parenchyma and conduit volume invested to conductance. By analyzing its individual constituents new insights may be possible. Lumen space invested to conductance is key to understand overall conduit hydraulic efficiency. Fiber and conduit wall space allocated to conductance may be important to understand implosion–efficiency tradeoffs. Parenchyma space allocated to conductance may be related to refilling efficiency or to water supply by capacitance. How different wood space allocation setups relate to hydraulic safety and efficiency, and to different environmental and phylogenetic contexts, may be the next steps to build upon Gleason et al.'s (2016) findings. Particularly interesting will be to compare belowground and aboveground wood space use as they are subject to different mechanical constraints on space use (Sperry et al., 2008; Larjavaara & Muller-Landau, 2010). We believe future investigations on some of the hydraulic efficiency traits proposed here (summarized in Table 1) will contribute to those next steps. We propose that xylem space use does coordinate with hydraulic safety in some species, but not in all, and this generates a limit, and not a direct relationship between hydraulic safety and hydraulic space-use efficiency. This line can be roughly imagined as a quantile linear fit in Fig. 2 of Gleason et al. (2016) with hydraulic safety setting the boundaries of Ks variability. Or inversely, with Ks setting boundaries in which hydraulic safety can vary. In this case a different mechanism than the one explored by Gleason et al. (2016) would be required, for example, assuming that Ks directly correlates with leaf water supply capacity, higher Ks would allow a plant to operate in higher water potentials and, consequently, allow it to survive with lower hydraulic safety. In this mechanism, the causal order is inversed and Ks determines hydraulic safety. As Brodersen (2016) highlights, an important aspect of wood space use is space allocation to mechanical support of the plant body. The fibers (or tracheid walls in gymnosperms), which are related to mechanical support, compose c. 70% of the wood (Ziemińska et al., 2013) and the variability in mechanical resistance explains up to 77% of the variability in wood density (Chave et al., 2009). Another aspect of plant mechanical resistance supporting this view can come from the perspective of plant inner mechanic stress, that is, the stress generated inside its tissues due to water transport. Tension in the water transport system of plants generates implosive forces (Hacke et al., 2001). Besides implosive forces, other forces occur due to water tension, particularly if gas spaces with positive pressures occur inside the wood (Pereira et al., 2016). For example, a nonembolized conduit in contact with an embolized one will cause moment force in the embolized one. The implosive force acting on the tissue that connects both vessels will force the embolized one to rotate longitudinally and this rotation force would need to be counteracted by other plant tissues. The interplay between negative and positive pressures inside the stem leads to a complex mechanical system whose resulting forces should increase with the degree of embolism and with the decrease of water potential inside the wood. The formation of cracks larger than tracheids and vessels does occur during the drying process of wood material (Hanhijärvi et al., 2003) and their occurrence decreases with wood density (Ilic, 1999). Cracks are often observed in cut dehydrating branches, indicating propagation of stress from conduits to other tissues. Although we do not know of any work that studied inner mechanical stresses other than implosive ones in living plants, plants that operate in lower water potentials should have a higher inner mechanical stress over all its tissues, and not only the vessels. We believe inner mechanical stress may play an important role in the hydraulic safety–efficiency limit relationship. Plants that operate under more negative water potentials due to higher hydraulic safety have to deal with stronger implosive and moment forces in the xylem. For this, they would need reinforced conduits with high thickness : span ratio (Hacke et al., 2001) and/or thicker fibers (Jacobsen et al., 2005) to resist both forces (Fig. 2). Higher thickness : span ratio can be achieved either with thicker walls or reduced cell diameter, which would, respectively, reduce space available to conduit and conduit efficiency. The limit relationship between Ks and hydraulic safety would thus be mediated by the tradeoff between Ks and mechanical resistance and the synergy between inner mechanical stress and hydraulic safety (Fig. 2). This would allow a high variance in Ks in plants with low hydraulic safety, as possible xylem space setups are less inner-mechanically constrained, and a small variance in Ks of plants with high hydraulic safety due to high inner mechanical constraint of space use. Another way to look at the limit relationship between Ks and hydraulic safety is by considering parenchyma space. Water storage in parenchyma makes the water-transport system operate in a nonsteady state, effectively buffering the plant from high xylem tensions and uncoupling diurnal xylem water potential from plant conductance (Sperry et al., 2008). Water storage in wood gives plants access to a water source that is closer to leaves and thus, accessed with a higher efficiency than the soil. Thus, low Ks with high parenchyma could also be associated with low hydraulic safety because water storage is increasing water-transport efficiency under nonsteady state conditions. Although water storage can buffer plants against water stress due to air water deficits, it cannot buffer against soil water deficits. How xylem space-use and the hydraulic efficiency vs safety relationship changes in situations where soil or air water deficits drives most of xylem water potential variation is certainly an important next step to investigate. Why then did Gleason et al. (2016) find a tradeoff between Ks and hydraulic safety for Acer? As Brodersen (2016) asks, ‘why Acer?’ Is it just a false positive? One possible explanation lies in its xylem space setup. If this genus has a more conserved xylem space setup, space allocation variability not related to water transport would be reduced and the safety–efficiency tradeoff signal may be visible. Either way, we highlight the need to further study wood space allocation setups, how they are related to water transport and the traits of plants that are in the boundary of the Ks–hydraulic safety limit relationship. This work was supported by the São Paulo Research Foundation (FAPESP) (grant no. 10/17204-0), FAPESP/Microsoft Research (grant no. 11/52072-0) awarded to R.S.O., and the Higher Education Co-ordination Agency (CAPES) (scholarship to P.R.L.B.). R.S.O. received a research productivity scholarship from CNPq. P.R.L.B., L.P. and R.S.O. designed and wrote the manuscript.