Hydraulic limitation of tree height: a critique

Abstract

Theoretical analysis indicates that the observed tapering of xylem conduits permits the total resistance of a tube running from trunk to petiole to remain constant, regardless of path length (tree height), so that water supply to all leaves is comparable if the xylem’s vulnerability to embolisation is disregarded ( West, Brown & Enquist 1999). Recently, however, Ryan & Yoder (1997) reviewed four major hypotheses to account for the cessation of tree height growth with increasing age and concluded that ‘hydraulic limitation’ was the most promising. Briefly, they argued that as tree height increases so does xylem path length and thereby hydraulic resistance owing to friction. Although trees compensate for their increased size by producing xylem elements with increased permeability ( Pothier, Margolis & Waring 1989), this was presumed to be insufficient to prevent total resistance from increasing with height. Consequently, stomata on tall trees must close early in the day to prevent xylem water potential from reaching a level that would lead to runaway embolisation and catastrophic failure of the transport system ( Yoder et al. 1994 ; but cf. Brodribb & Hill 1999). Stomatal closure reduces both loss of water and uptake of carbon dioxide so that daily carbon assimilation by leaves decreases. If foliage on tall trees produces less photosynthate, then less wood growth will result because other carbon costs do not change much with tree height ( Ryan & Waring 1992; Mencuccini & Grace 1996a). The hypothesis that height growth, net primary production and wood production may be constrained by hydraulic properties of tall trees is increasingly the subject of both experimental ( Yoder et al. 1994 ; unpublished reports cited by Ryan & Yoder 1997) and theoretical studies ( Friend 1993; Gower, McMurtrie & Murty 1996). We think that a whole-plant perspective, which also takes account of soil and atmospheric influences, is essential to understanding what controls water transport to tree crowns. We also believe that mechanistic explanations of plant growth (and ecosystem productivity) must be compatible with the operation of natural selection to maximize individual fitness. The formal hydraulic model of Whitehead, Edwards & Jarvis (1984) predicts that a homeostatic balance exists between transport capacity (sapwood cross-sectional area and permeability) and transpirational demand. Thus, any path-length effects on water transport could be fully compensated if this was advantageous to the plant. Here we show that available data generally do not support Ryan & Yoder’s (1997) version of the hydraulic limitation hypothesis and that leaf:sapwood area ratio, rather than path length, may dominate in determining whole-plant conductance. Next we present evidence and arguments that components of the soil–plant–atmosphere continuum, such as hydraulic resistance of the rhizosphere and leaves, and water storage in the stem, may reduce or eliminate the significance of axial resistance to water transport. We argue that the height of most tree species is more constrained by genetic, rather than physical limitations. When height growth ceases to offer a competitive advantage through avoidance of shading, then (genetically programmed) resource allocation will be adjusted to enhance tree survival and reproduction, not necessarily wood production. By analogy to Ohm’s law, absolute hydraulic conductance (the inverse of resistance) is the ratio of water flow rate through the plant or plant segment to the pressure difference causing flow. The absolute conductance increases as leaf area increases because a large leaf (and corresponding large root and shoot) has more parallel paths for water movement. Thus, normalization of conductance by leaf area is necessary to account for size effects and to indicate the sufficiency of water supply to leaves ( Becker, Tyree & Tsuda 1999). Regarding transport sufficiency, observations at the whole-plant level are more pertinent than those at the branch level which, unfortunately, are not a surrogate for the entire hydraulic pathway (cf. Panek 1996). Conifer branches are less conductive than those of angiosperms, as expected owing to the wider, longer and hence more efficient xylem conduits of the latter ( Wang, Ives & Lechowicz 1992; Becker et al. 1999 ). Nevertheless, for both tropical ‘saplings’ and temperate adults, leaf-area normalized whole-plant conductances (KP,LA) of conifers and angiosperms were statistically indistinguishable – differences at the branch level were apparently compensated by other aspects of hydraulic and plant architecture ( Becker et al. 1999 ). A simple compensatory response to diminished hydraulic conductance is to reduce leaf area (AL) relative to sapwood area (AS), a relationship that is frequently size-dependent ( Margolis et al. 1995 ; Cochard et al. 1997 ; Andrade et al. 1998 ). Conversely, an increase in AL/AS may reduce KP,LA in the absence of any substantial increase in axial resistance ( Fig. 1). Partial defoliation ( Meinzer & Grantz 1990; Pataki, Oren & Phillips 1998) and shading ( Whitehead et al. 1996 ) experiments that directly or effectively reduce AL/AS have shown that stomata can respond rapidly to the associated increase in KP,LA. These observations suggest that other architectural features such as AL/AS, and not path length per se, may dominate in determining KP,LA. Adjustments in AL/AS, and consequently the leaf-area based hydraulic properties and gas exchange described above, need not imply variation in gas exchange at the crown level ( Andrade et al. 1998 ), which may be more pertinent to height growth than responses at the leaf level. Also, aspects of tree growth other than height could be sacrificed to meet any costs associated with increased sapwood production. Regression line describing the relationship between whole-plant hydraulic conductance (KP,LA) and leaf area relative to sapwood area (AL/AS) for eight well-watered, taxonomically diverse woody species growing at three sites in the Brazilian savanna (F. C. Meinzer et al. and S. Bucci et al. unpublished data) and coffee (Coffea arabica L.) plants growing under full sun in Hawaii (P. Tausend et al. unpublished data). Values of KP,LA were determined from measurements of sap flow (normalized by leaf area) and the difference between predawn leaf water potential (a surrogate for soil water potential) and leaf water potential coinciding with the sap flow measurement. The influence of stored water release on the determination of KP,LA was assumed to have been minimal in these small plants (1·5–3 m tall, < 10 cm stem diameter). The initial steep decline in KP,LA may reflect the influence of increasing leaf area that must be supplied by the sapwood, and the subsequent gradual decline may reflect the increasing number of parallel resistances (leaves). The large range in KP,LA over a small range of plant height, comparable to that of the adult plants depicted in Fig. 2, points to the ambiguity that may arise when comparing KP,LA among plants of very different heights. Based on the above considerations, an appropriate initial test of the hydraulic limitation hypothesis would be to compare KP,LA of well-watered trees of different heights, but a negative relationship between KP,LA and height would not necessarily be attributable to path length. Only one of the studies cited by Ryan & Yoder (1997) in support of their hypothesis, that of Mattson-Djos (1982), satisfies the criteria for a preliminary test although it is unknown if the plants were well watered. Thus, hydraulic conductance of the soil could have been differentially limiting in the stands of different-sized trees. Moreover, some of the results in Mattson-Djos (1982, Fig. 2) were not consistent with increasing hydraulic limitation with increasing tree size. Mencuccini & Grace (1996a) found that leaf-area normalized wood growth decreased linearly as leaf-area normalized whole-shoot conductance decreased with tree age and height (2–24 m). Using pressure perfusion of water into whole shoots and leaves, Yang & Tyree (1994) found that leaf-area normalized whole-shoot conductance of two Acer species was independent of height (5–20 m). The studies by Mencuccini & Grace (1996a) and Yang & Tyree (1994) did not consider the below-ground component of plant hydraulic conductance. Hubbard, Bond & Ryan (1999) found that leaf-area normalized whole-plant conductance of 33 m-tall Pinus ponderosa was 60% lower than in 12 m-tall trees. An unpublished re-analysis to account for statistical non-independence of the data and to more fully characterize the negressions in their Fig. 4 supported the original conclusion that photosynthesis was more limited in tall trees than in short ones at a given vapour pressure deficit (Robert Hubbard, personal communication). Available data generally do not support the hydraulic limitation hypothesis. There was no significant correlation between ln-transformed KP,LA and tree height (2–25 m) for 17 trees of 11 temperate species ( Fig. 2, Pearson’s r = −0·16, P = 0·54). Values of KP,LA for tall temperate trees and short tropical plants overlapped ( 1, 2; Becker et al. 1999 ). Comparison within species is preferable; there were slight inverse trends between KP,LA and height for two species and large variation in KP,LA among studies for a third species with trees of similar height measured at four different sites ( Fig. 2). In a comparison of five tropical species, KP,LA was again uncorrelated with tree height (18–35 m), although some trees were not well-watered ( Andrade et al. 1998 ; Goldstein et al. 1998 ) so soil resistance may have become limiting. Whole-plant conductance normalized by LAI (leaf area per ground area) did not significantly differ between short (3–5 m) and tall (9–14 m) Acer saccharum (Fig. 5 in Dawson 1996). Saliendra, Sperry & Comstock (1995) did find that juveniles (< 1 m tall) of Betula occidentalis had lower KP,LA than saplings and adults (2–10 m tall), and path length was said to account for differences in shoot conductance although it is not clear if this effect operated over the entire height range of saplings and adults. In these studies, KP,LA was calculated from the slope of transpiration rate plotted against xylem water potential throughout the day or on different days, or from midday transpiration rate divided by the difference between predawn and midday xylem water potentials. As Mencuccini & Grace (1996b) noted, such calculations are sensitive to the method of sampling and averaging leaf water potential, which can vary widely in a crown. However, good agreement between measurements of KP,LA by the conventional evaporative flux method and the high pressure flowmeter, which imposes a known pressure gradient, increases confidence in both techniques ( Tsuda & Tyree 1997). Relationship between soil-to-leaf hydraulic conductance normalized by leaf area (KP,LA) and height of 11 adult temperate angiosperm (open symbols) and conifer (filled symbols) species under well-watered conditions. Symbols connected by a line represent conspecific trees measured at different sites: Pinus sylvestris (▴), P. pinaster (▾) and Picea abies (★). Data from Table 4 of Becker et al. (1999) , excluding a suspiciously high value of KP,LA for Betula alba. Water transport in trees will be controlled by whatever component of the soil–plant–atmosphere continuum is most limiting, and the interaction of soil and plant properties has recently been explored with a computer model in an important study by Sperry et al. (1998) . They found that below a threshold of root: leaf area, the loss of hydraulic conductivity in the rhizosphere limited the maximum rate of steady-state transpiration whereas, above this threshold, loss of xylem conductivity from cavitation was limiting. The root:leaf area threshold varied 200-fold depending on soil texture and the xylem’s vulnerability to embolisation. Water uptake by trees having non-vulnerable xylem or occurring on coarse soils might thus be independent of plant hydraulic conductance, even if this does vary with height. Irrigation experiments with Malus domestica showed that the soil-to-root pathway represents a major resistance to water uptake by roots, even at high soil water potentials ( Green, Clothier & McLeod 1997). Embolised conduits can be refilled overnight or more quickly, even when the xylem is under tension ( Salleo et al. 1996 ; Zwieniecki & Holbrook 1998), so disruption of water transport by cavitation need not be prolonged. At the branch level, leaf resistance usually represents the largest component of branch resistance ( Yang & Tyree 1994; Cochard et al. 1997 ), which tends to reduce the effect of path length on branch hydraulic conductance. In fact, a simple Ohm’s-law analogue of the resistance of a single leaf in series with the resistance of a single stem suggests that the dominating influence of leaf resistance will make even a relatively large change in stem resistance difficult to detect ( Fig. 3). According to the analogue, if the leaf resistance is 10 times the stem resistance, a 50% change in stem resistance would yield less than a 5% change in the total resistance measured. This partly explains why a large loss of hydraulic conductance in twigs and petioles of Quercus petraea had little impact on total water-use ( Bréda et al. 1993 ). Even when leaf and stem resistances are equal, only half of the change in stem resistance would be detectable as a change in total resistance. This situation leads to the apparent paradox that although leaf-area based measurements are necessary to assess potential hydraulic limitations on leaf-level processes, failure to partition hydraulic resistances among their foliar, axial and other components may yield misleading conclusions about size-related changes in stem hydraulic properties. Measuring the water status of covered, non-transpiring leaves concurrent with water flux may help to resolve this conundrum by eliminating the influence of leaf hydraulic resistance (see Turner & Long 1980; Turner 1981). An Ohm’s-law analogue for the hydraulic resistance of a single leaf (RL) in series with that of a single stem (RS) showing the relative change in total resistance (Rtot = RL + RS) as a proportion of the relative change in stem resistance. The diminished influence of RS on Rtot when RL/RS is high is analogous to the decoupling of transpiration from stomatal control when boundary-layer resistance is high in relation to stomatal resistance. Greater than expected stomatal closure may be required to control xylem tensions in compensation for low hydraulic conductance when transpiration is decoupled from stomatal control by low boundary-layer conductance, as seems often to be the case in tropical trees ( Jarvis & McNaughton 1986; Meinzer 1993; Meinzer et al. 1997 ). Dawson (1996) has suggested that decoupling should increase as trees get larger and their total transpiration rate increases, especially in closed stands. It is the actual flux of water vapour, not the stomatal conductance, that determines leaf water status at a given soil-to-leaf hydraulic conductance. Thus, any evaluation of potential hydraulic limitations on gas exchange should incorporate measurements of vapour fluxes independent of leaf-level porometric measurements. The Ohm’s-law analogue for calculating hydraulic conductance assumes steady-state conditions and cannot cope with the stored water component of hydraulic flux ( Running 1980). In Mencuccini & Grace’s (1996b) study, sapwood volume per unit leaf area increased with tree height, leaving unresolved the question of whether plant water relations were more closely linked to hydraulic conductance or storage. Water stored in sapwood buffered leaf deficits and contributed substantially to transpiration in temperate ( Waring, Whitehead & Jarvis 1979; Lo Gullo & Salleo 1992; Herzog, Häsler & Thum 1995) and tropical trees ( Tyree et al. 1991 ; Machado & Tyree 1994; Goldstein et al. 1998 ). Trees with large stem storage capacity maintained maximum rates of transpiration for longer periods than those with less capacity so stem water storage provides another means of compensating for any increase in hydraulic resistance with tree size ( Goldstein et al. 1998 ), and it also permits the plant to reduce its investment in root production ( Machado & Tyree 1994). In short, modelling the dynamics of water flow ( Tyree 1988; Meinzer 1993; Sperry et al. 1998 ) has underscored the importance of an integrated, whole-plant approach, which also takes account of soil and atmospheric components, to avoid misleading conclusions about the limiting components of water transport. There is little doubt that the maximum size attained by a tree is ultimately constrained by genetic, rather than physical considerations ( Greenwood 1989; Hara, & and this partly explains why as measured by the height on age ( 1994). Based on of the of water and the necessary to and water & (1995) that trees than m are and the measured trees to short of this height ( & tree species adult that are lower than the maximum by the of as for conifers in the ( Fig. varied for temperate trees of 1 m ( of of the tree of conifer species growing in the Data from shoots to be the and one of the that a to to the and more as plants and ( & 1997). This such as water and which a growth to influence The to may of a size by the tree ( & & but that in a to ( & 1997). growing can a or a but not so the of can a ( 1988; 1997). was or and growth in the of Betula ( and in trees with the of branch growth ( & the more in conifers are in the of the crown and the lower ( Thus, the crown or of some trees as height growth may be a of their reproduction, rather than hydraulic as by Ryan & Yoder experiments the growth of decreased with their of size and path-length show that is by and is ( Greenwood 1989; & 1994). is at an that plant and the and of ( & 1996). for is the primary for the and of the ( The of growth height growth ceases in with the inverse correlation among species between branch length and tree height ( et al. 1991 ; & suggests that adult tree height an balance between the costs and of ( plants could a its height growth on that of the other in a ( & A theoretical model that tree height growth would even wood production to there was no longer a competitive advantage of increased ( A for the of is the ratio of from which is known to height growth, at of ( a height to for from has been a tree to the of resource allocation ( Theoretical indicate as trees increase in height, their sapwood must a in both foliage and root growth, to a in height ( & 1994). In adult allocation of to and production has over primary and stem growth ( & In tropical tree species, there is some of an in the relationship the of reproduction, which is most of the crown is fully ( An of Ryan & (1997) arguments for the hydraulic limitation hypothesis is that carbon production plant This seems to be at in so as a between and growth has been photosynthesis in trees ( & & 1994). very production can even eliminate production ( Greater is to account for the height and size of to trees ( but size is not at low tree may not be limiting ( & The between and growth is so to plant that apparently some trees the relationship with – from their thereby and branch growth ( & Although Ryan & Yoder (1997) did not consider on as a potential on height growth, & (1997) it as an of of because costs vary growth with age and the carbon is a low of Nevertheless, large may growth both and because of ( As trees age and costs of wood increase relative to that of wood costs ( Ryan & Waring the allocation to costs may to of that for wood ( & Ryan et al. 1997 ). This could have a substantial impact on height growth, both directly and through root and foliage even if it does not fully account for the of We with Ryan et al. (1997) on the need for more data on as a of It is that a single can account for limitation of height growth in diverse for to is an important limiting growth and the architecture of conifers ( & In tropical maximum height and of trees to be than in temperate in for of trees is about 60% of tree were by by and only of trees that size and age limitations may be more linked to catastrophic failure than to hydraulic limitations on water supply to the crown ( & selection does not maximize that of it with survival and Even if whole-plant hydraulic conductance is found to with tree height, this will not be the so much of physical as of of resource allocation that growth, production of to Although we have on limiting tree height growth to an the arguments have for growth, which is partly the of individual that maximize the competitive of the individual also reduce the wood production of stands because of costs associated with height ( We for the by Mattson-Djos and Enquist for for on Fig. and Bond and Mencuccini for on of this 4 1999