Current address: CREAF/Unitat d’Ecologia, Universitat Autònoma de Barcelona, Bellaterra 08193 (Barcelona), Spain.
Below-ground hydraulic conductance is a function of environmental conditions and tree size in Scots pine
Article first published online: 21 AUG 2007
Volume 21, Issue 6, pages 1072–1083, December 2007
How to Cite
MARTÍNEZ-VILALTA, J., KORAKAKI, E., VANDERKLEIN, D. and MENCUCCINI, M. (2007), Below-ground hydraulic conductance is a function of environmental conditions and tree size in Scots pine. Functional Ecology, 21: 1072–1083. doi: 10.1111/j.1365-2435.2007.01332.x
- Issue published online: 21 AUG 2007
- Article first published online: 21 AUG 2007
- Received 25 March 2007; accepted 19 July 2007; Handling Editor: James Richards
- root water transport;
- sap flow;
- stem diameter variations;
- tree height;
- variable hydraulic resistance
- 1Variations in water tension in a transpiring tree cause elastic changes in stem diameter. To better understand the dynamics of these variations, stem diameter changes and sap flow rates were monitored simultaneously in trees from two Scots pine chronosequences in Scotland.
- 2Tree below-ground hydraulic conductance (kbg) was estimated from the relationship between leaf-specific sap flow rates and the difference between stem and soil water potentials estimated from diameter variations in the stem.
- 3In a given tree, kbg varied both within and among days, with conductance increasing as a function of sap flow and evaporative demand. These patterns could be explained in terms of a composite model of root water transport and possible changes in the gating of aquaporins.
- 4We interpreted these trends of increasing kbg with evaporative demand as a mechanism to enhance the ability of trees to control leaf water potential and keep it within physiologically acceptable limits, with potential implications for our general understanding of plant water relations, and for the estimation and modelling of ecosystem water fluxes.
- 5Across trees, kbg declined with increasing tree age/size, but the proportional contribution of below-ground to whole-tree hydraulic resistance also declined. This is consistent with an increase in below-ground carbon allocation in old/tall trees and a partial acclimation of tall trees to hydraulic limitations. It is argued that these trends have to be considered when discussing the importance of tree height for water transport and growth.
The xylem of a plant is an elastic tissue, and thus it is subject to radial shrinkage and swelling as a result of the tensions or pressures that develop in the water columns within conduit lumina. Although most of the changes in stem diameter are known to be due to fluctuations in bark width or due to new growth, the diameter variations of the xylem of a transpiring plant can be detected and depend on the tension that pulls the water up along the transpiration stream (e.g. Irvine & Grace 1997; Offenthaler, Hietz & Richter 2001). These micro-variations have been widely used in the study of plant water relations (e.g. Zweifel, Item & Häsler 2001; Steppe & Lemeur 2004). In particular, changes in the pressure of water in the stem (ΔP) can be estimated from variations in wood diameter if the radial modulus of elasticity of the (functional) xylem (Er) is known (Irvine & Grace 1997):
- ( (eqn 1))
where d is the diameter of the (functional) xylem. This relationship is also frequently used to estimate plant water potential, making the reasonable approximation that water pressure and water potential in the xylem sap are identical, that is, the osmotic potential of xylem sap is small and, more importantly, unlikely to change significantly over the course of measurements (Irvine & Grace 1997).
The plant hydraulic system can be modelled as a series of hydraulic resistances where flow between any two locations in the pathway between roots and leaves is proportional to the water potential gradient linking them. If steady-state conditions are assumed, changes in xylem water potential at the base of the stem can be combined with sap flow measurements to estimate the hydraulic conductance of the root system (Irvine & Grace 1997) and to monitor how it changes as a function of environmental conditions. Most estimates suggest that below-ground hydraulic resistance frequently represents around half of whole-tree hydraulic resistance (Landsberg et al. 1976; Roberts 1977; Running 1980; Irvine & Grace 1997; Tsuda & Tyree 1997), but the proportion is species-dependent and varies with environmental conditions (Sperry et al. 1998). In particular, it is known that roots are more vulnerable to xylem embolism and operate closer to the point of hydraulic failure than stems or branches (e.g. Mencuccini & Comstock 1997; Martínez-Vilalta et al. 2002), so that the percent contribution of the root system to whole-tree hydraulic resistance tends to increase under water-stressed conditions. It is thus possible that roots hold the key to understand the water relations of trees and, specifically, their response to drought (Jackson, Sperry, & Dawson 2000).
It has long been known that roots may change their hydraulic conductivity in response to demands from the shoot and environmental conditions (e.g. Fiscus 1975; Passioura 1988; Steudle 2000, 2001). Tsuda & Tyree (2000), for example, reported diurnal changes in both shoot and root hydraulic conductances in sunflower, and hypothesized that plant hydraulic conductance might respond directly to the transpiration rate. However, little is known about how below-ground hydraulic conductance of trees varies seasonally or as a function of environmental conditions in the field (but see Hellkvist, Richards & Jarvis 1974). Several processes may potentially affect root hydraulic conductance. According to the composite transport model of water uptake by roots (Steudle 2000, 2001), root water transport switches from a purely osmotic to a predominantly hydraulic mechanism as transpiration rate increases. As a result, hydraulic conductance should increase with sap flow (Steudle 2000). Additionally, water channels (aquaporins) may change the hydraulic conductivity of the extravascular tissues of the roots to adjust it according to the demands from the shoot (Javot & Maurel 2002). Finally, xylem embolism would normally have the opposite effect, decreasing the conductivity of the roots under conditions of low water content in the soil and/or high evaporative demand (e.g. Jackson et al. 2000; Domec et al. 2006).
It is also reasonable to expect developmental changes in below-ground hydraulic resistance. Ryan & Yoder (1997) hypothesized that the increase in path length as trees grow taller, together with the direct gravitational effect of greater height, should increase the hydraulic resistance from the soil to the leaves and could explain the decline in growth and productivity in older (and taller) trees (hydraulic limitation hypothesis). Although most studies indicate an increase in whole-tree hydraulic resistance as a function of tree height, compensatory mechanisms do occur suggesting that increased path length does not directly limit the growth of old/tall trees (Ryan, Phillips & Bond 2006). Changes in biomass allocation below-ground with tree age may also affect these patterns. Using data on biomass production and above-ground hydraulic resistances, Magnani, Mencuccini & Grace (2000) inferred that substantial compensation must have occurred below-ground in a Scots pine chronosequence in England, such that proportional contribution of roots to total tree hydraulic resistance must have declined with tree age. While most studies have concentrated on changes on above-ground or whole-tree hydraulic conductance as a function of tree height, below-ground hydraulic conductance may also vary during development, either as a consequence of changes within the root system or as an effect of changed leaf-to-root area ratios.
In this study, we monitored sap flow and variations in wood diameter in Scots pines of different ages and sizes at two different sites in Scotland. The two sites correspond to different forest types: one of them is an old-growth, naturally regenerated woodland where trees of different ages grow together in an open stand, while the other one includes several plantations of closed-canopy, even-aged stands. Parallel studies have shown that leaf-specific growth efficiency and whole-tree hydraulic conductance decreased with tree age and height at both sites (Mencuccini et al. 2005; Martínez-Vilalta, Vanderklein & Mencuccini 2007; E. Korakaki et al., unpublished data). Our main objectives here were to estimate below-ground hydraulic conductance from sap flow and wood diameter variations, and to establish whether the hydraulic conductance of roots changed with environmental conditions and varied as a function of tree size. Specifically, we hypothesized: (i) that below-ground hydraulic conductance would increase as a function of evaporative demand; and (ii) that leaf-specific below-ground hydraulic resistance would increase in older (and taller) trees.
study sites and sampling design
This study was conducted at two different sites in Scotland: Guisachan and Selm Muir. The measurements were taken at Guisachan from late August to mid-October 2003, and 2 years later at Selm Muir, from mid-August to late November 2005.
The Guisachan forest is a native, old-growth Scots pine woodland in North Scotland (57°16′ N, 4°49′ W, altitude of 300 m a.s.l.), where the regional climate is relatively cold and wet, with an average annual temperature of 6·5 °C and an average rainfall of 1215 mm year−1 (data from the British Atmospheric Data Center, NERC, UK). The soil is a peaty podzolic ironpan, with predominantly clay texture. The vegetation consists of naturally regenerated Scots pine woodlands, with a tall understorey consisting of scattered Betula pendula Roth and Sorbus aucuparia L., and a bottom layer consisting mainly of Vaccinium myrtillus L. and Deschampsia flexuosa (L.) Trin. In the study site, Scots pine density was 344 trees ha−1, with a basal area of 19 m2 ha−1. Eight Scots pines ranging from 24 to 158 years of age and growing together within 200 m of each other were measured at this site (Table 1).
|Tree||Age (years)||DBH (cm)||Height (m)||Total projected leaf area (m2)||n days with LVDT data||n days with sap flow data|
The Selm Muir forest is located in southern Scotland (55°52′ N, 3°27′ W, altitude of 215 m a.s.l.) and consists of several planted stands of Scots pine trees. The climate is milder than at Guisachan (average temperature of 7·7 °C and average rainfall of 840 mm year−1). Soils are podzolic brown earth with clay-loam texture. Within each of the three studied stands, the tree layer was completely dominated by even-aged Scots pine trees, with a bottom layer consisting mainly of V. myrtillus L., grasses and sedges. The three study stands, aged 25, 50 and 80 years, were located within 300 m of each other. One to four trees were measured at each stand (Table 1).
At each site, a rain gauge and a 2-m high mast with standard meteorological sensors (Campbell Scientific Inc., Logan, UT, USA) were located in an opening within 200 m of all measured trees. Two thermocouples were also buried into the soil nearby the mast (depth c. 10 cm) to monitor soil temperature. Measurements were taken every 10 s and the averages stored every 15 min in a datalogger. Soil moisture was measured continuously at the two sites using water content probes with 30-cm-long rods (Campbell CS615 and CS616). Both the sensor models were calibrated in the laboratory using soil from one of the study sites to confirm that the standard calibration was applicable. Two to four soil moisture probes were located at each stand. Measurements were taken every 15 min and stored.
estimation of sapwood and leaf area
All measured trees were cored at breast height using standard techniques. Normally, a complete core was extracted spanning from the north to the south side of the tree. When this was impossible, two cores were extracted: one on the north side and the other one on the south side of the tree. Annual rings were counted under a dissecting scope, and their number was used to establish the age of the trees. The diameter of active sapwood was measured after staining the cores with o-toluidine (Shain 1967).
A destructive sampling of live branches was carried out in November 2003 at Guisachan and in July–August 2003 at Selm Muir to generate allometric equations for the estimation of the total leaf area of the measured trees. A total of 22 trees were climbed using fixed ropes (10 at Guisachan and 12 at Selm Muir). For all these trees, the diameter and whorl number of each primary branch were recorded. Additionally, two to four branches, depending on tree size, were harvested from each tree throughout the height profile of the crown. The needle biomass measured for these branches was then used to build a predictive model of branch leaf area using stepwise multiple regressions. These relationships (different for each site) were used to estimate the leaf area of all primary branches in the sampled trees. Since not all measured trees could be climbed, the average AL : Asw (leaf : sapwood area ratio, m2 cm−2) values for each site and age class were used to calculate total leaf area from sapwood area at breast height for those trees that were not sampled. See Martínez-Vilalta et al. (2007) for details on the methods and the predictive model used.
xylem diameter variations
Micro-variations in xylem diameter were monitored in all studied trees (Table 1) using dendrometers consisting of a linear displacement transducer (LVDT; DG/2·5 dc spring return LVDT, Solartron Metrology, West Sussex, UK) mounted on a metal frame as described in Irvine & Grace (1997). The measuring tip of the LVDT and a bolt attached to the frame on the opposite side were the only contact points with the stem in the measurement plane. Bark, phloem and cambium were removed at these two points prior to installation so that only xylem diameter changes were measured. The exposed xylem was covered with silicone grease to prevent water loss. All dendrometers were installed at approximately breast height. The LVDT output was logged every 10 s, and the averages were stored every 15 min. In each tree, thermocouples were placed in contact with the frame and in small, 3–4 mm deep holes in the xylem. These temperature readings were stored and used to correct for the thermal expansion of the frame and the wood using the linear expansion coefficients given in Irvine & Grace (1997) for the frame and in Sevanto et al. (2005) for Scots pine wood.
Xylem diameter variations were used to estimate diurnal changes in stem water potential as follows. The maximum stem diameter within a day (minimum shrinkage, occurring normally during early morning, before sun rise) was assumed to correspond to equilibrium conditions (i.e. stem water potential = soil water potential). The water pressure difference between the stem at breast height and the soil was estimated by dividing the within-day variation in stem diameter by the sapwood diameter of the stem and multiplying this ratio by the elastic modulus of elasticity in the radial direction (cf. eqn 1) (Irvine & Grace 1997). Irvine & Grace (1997) showed that there is no significant diameter change in the heartwood of Scots pine stems. A value of 0·75 GPa was used for the elastic modulus of elasticity, based on the laboratory measurements taken by Irvine & Grace (1997) on samples from another Scots pine forest in central Scotland (Devilla forest, Fife, 56°2′ N, 3°43′ W).
Xylem sap flux was monitored with 2-cm-long, Granier-type sensors (Granier 1985). Probe pairs were inserted radially into the stem at breast height. Sensors and stems were insulated to minimize natural temperature gradients. The temperature difference between the probes in each sensor was recorded every 10 s, stored every 15 min, and later used to obtain sap flux density by means of the equation derived empirically by Granier (1985). Daily maximum temperature difference was used as an estimate of the temperature difference under zero flow conditions. Natural temperature gradients were accounted for as explained in Martínez-Vilalta et al. (2007), where additional details can be found on the techniques employed.
At Selm Muir, a single sensor was installed in the north-facing side of each measured tree. At Guisachan, all studied trees (Table 1) had at least one sensor in the north-facing side of the stem. At this site, corrections were developed to account for radial patterns or aspect-related changes in sap flow, based on data from 15 trees from the same stand (including four of the trees studied here) that had a second sensor either at a greater depth (2–4 cm) into the sapwood or on the south-facing side of the tree [cf. Martínez-Vilalta et al. (2007) for details].
leaf water potentials
Pre-dawn and mid-day leaf water potentials (Ψpd and Ψmd, respectively) were measured with a pressure chamber (SKMP 1400, Skye Instruments, Powys, UK) on the same trees instrumented with LVDT and sap flow sensors. Measurements were taken once at Selm Muir (early November) and twice at Guisachan (July and August), although in the latter, only the August sampling campaign coincided with LVDT and sap flow measurements. At Guisachan, two shoot tips were sampled from each tree using a pole pruner or, for the tallest trees, a shot gun. At Selm Muir, where shot guns could not be used, only trees in the 25- and 80-year-old stands could be accessed with scaffolding towers. In all cases, shoot tips were immediately bagged in ziplock bags with damp paper inside and stored in a cooler. Measurements were taken within 30 min of collection.
For each tree, sap flow per unit leaf area (QL, g m−2 h−1) was calculated as the total sap flux divided by total leaf area. A seasonal correction of leaf area was implemented in which leaf area was considered to increase linearly from early May to early August, and to decrease linearly from mid-August till early November, based on phenological observations at the study sites and the observed distribution of leaf area into yearly cohorts. At Guisachan, peak leaf area was considered to be 50% greater than the measured winter value (cf. Beadle, Talbot & Jarvis 1982).
A preliminary exploration of the data showed that the within-day relationship between sap flow and ΔP was nonlinear at low sap flows. Accordingly, we decided to fit the data using a model based on the following equation (Fiscus 1975):
- ( (eqn 2))
where kbg is the below-ground hydraulic conductance (in g m−2 MPa−1 h−1), σ is the reflection coefficient, R is the gas constant (J K−1 mol−1), T the absolute temperature (K), Co is the external concentration of solutes (mol m−3) and JS* is an active solute uptake term (mol g m−5 h−1). This equation is based on a simple one-membrane two-compartment model, but is also consistent in many aspects with the composite model of root water transport (Steudle 2000, 2001). The main processes accounted for by the model are the following: (i) the effect of sap flow on the accumulation of solutes in the root; and (ii) the different effect of changes in the osmotic and pressure gradients on the flow (Tyree 2003).
The parameters σ, R, T, Co and JS* were assumed to be constant, and their values were combined into the constants c1 and c2. For mathematical convenience, the inverse of eqn 2 was used. The final fitted equation was thus:
- ( (eqn 3))
This equation was fitted only to daytime data (Photosynthetically Active Radiation > 50 µmol m−2 s−1). Different equations were fitted for each day and tree, and separately for ‘morning’ (up to the maximum daily QL value) and ‘afternoon’ values. In each case, a reference sap flow (QL,ref) was calculated as the flow expected at 0·5 MPa of pressure difference according to the fitted model. Morning and afternoon values of QL,ref and kbg were calculated separately for each day, and their difference tested by means of repeated measures anova with time of day as the repeated measures factor.
The percent contribution of below-ground resistance to whole-tree hydraulic resistance was estimated by comparing measured mid-day minus pre-dawn leaf water potentials and concurrent values of stem water pressure difference from the LVDT data (Irvine & Grace 1997). Association between variables was tested using Pearson correlation coefficients. Variables were log-transformed in some analyses to normalize their distribution. All analyses were carried out using the packages spss (v. 12, SPSS Inc., Chicago, IL, USA) and r (v. 2·5·0, R Foundation for Statistical Computing, Vienna, Austria).
Uncertainty analyses were conducted to assess the precision of our estimates and their consistency towards some potential biases in the data. A Monte Carlo approach was adopted in all cases. First, the uncertainty in the contribution of below-ground to whole-tree hydraulic resistance due to random errors was assessed by repeating the calculations sampling from a normal distribution centred around the observed means of the contributing variables (Er, Δd/d and Ψmd). The process was repeated 1000 times, using a coefficient of variation (CV) of 10% for all variables. As a comparison, the CV of Ψmd measured across trees, thus incorporating both intra- and inter-tree variability, was 17%. Second, the robustness of the within-day relationship between sap flow and ΔP (eqn 3) to random errors was checked separately for each day by multiplying each data point in the curve (QL and ΔP) by a random number sampled from a normal distribution with mean = 1 and standard deviation = 0·1. This process was repeated 100 times for each day on one single tree (G1B8), and the final kbg estimates were compared to the estimates obtained with the original data.
Finally, the robustness of our main results to systematic biases due to the possible underestimation of sap flow's temperature difference under zero flow conditions (ΔTmax) was also assessed. To achieve that, the sap flow values for one tree (G1B8) were recalculated assuming that the real ΔTmax was not the daily maximum but the absolute maximum observed over the whole study period (QL,rec). The new values were a linear function of the originally computed QL values (r2 > 0·999), and thus this potential bias could not change the shape of the within-day relationship between QL and ΔP. However, its impact on the changes in the estimated kbg across days could still be important. This potential effect was studied by repeating the uncertainty analysis of the within-day relationship between QL and ΔP (see above) but using a mean of 1·1 (instead of 1·0) to simulate the consistent underestimation of flow caused by any underestimation of ΔTmax. The 1·1 value corresponded approximately to the average discrepancy between QL,rec and QL observed for tree G1B8.
estimation of stem water potentials and comparison to leaf water potentials
The magnitude of the thermal expansion corrections (frame plus sapwood) was relatively small compared to the LVDT signal, as shown by the fact that the slope of the regression between corrected and uncorrected LVDT output values for each tree was 0·92 ± 0·06 (mean ± SE; average r2 = 0·97 ± 0·01).
Leaf water potentials ranged between –0·50 ± 0·02 and –1·20 ± 0·02 MPa at Guisachan, and between –0·35 ± 0·02 and –1·02 ± 0·08 MPa at Selm Muir. The LVDT estimates of daily maximum stem water pressure difference ranged between 0·22 and 0·46 MPa. As expected, these values were always less than the differences between pre-dawn and mid-day leaf water potentials measured on the same day and tree. The percent contribution of below-ground resistance to whole-tree hydraulic resistance estimated from the difference between leaf and stem water potentials for the single day in which these two variables were measured simultaneously was 57% ± 8% (mean ± SE; n = 6 trees) at Guisachan, and 40% ± 3% (n = 4 trees) at Selm Muir. If a random error of 10% around the mean was introduced in the three variables contributing to the calculation of the percent contribution of below-ground to whole-tree resistance (see Methods), the resulting CV of the estimate was 17·8%. If the error was increased to 20% for Δd/d, arguably the most uncertain variable, the resulting error increased to 25·4%.
relationship between sap flow and stem water potential
Variations in sap flow and stem water pressure difference estimated from stem diameter variations tracked environmental variables, particularly D (Fig. 1). In the early morning, the rate of stem shrinking was faster than the corresponding increase in sap flow, whereas in the afternoon and at night, sap flow values declined faster towards zero than the estimated stem pressure difference. This pattern was observed for the whole study period and was consistent across sites (Fig. 1).
Consequently, the within-day relationship between sap flow and stem pressure difference was strongly nonlinear, particularly for low values of sap flow (Fig. 2). In most cases, the shape of the relationship was remarkably similar to the function in eqn 3. Using this function, we were able to fit 81% and 56% of the ‘morning’ and ‘afternoon’ curves for the Guisachan data set, and 65% and 48% of the ‘morning’ and ‘afternoon’ curves for the Selm Muir one. Virtually, all cases when the fit did not converge or gave unreasonable parameters (e.g. negative conductivities) coincided with days with low Vapour Pressure Deficit and thus small diurnal changes and absolute values of sap flow and stem pressure difference. This increased the measuring error and generally made it more difficult to characterize the relationship between the two variables. The average r2 for the fitted ‘morning’ and ‘afternoon’ curves was, respectively, 0·81 and 0·80 for Guisachan, and 0·78 and 0·71 for Selm Muir. Changes in water viscosity due to temperature variations in the xylem were relatively small both within- and between-days (xylem and soil temperature variation was < 6·5 °C over the whole study period), and all the reported relationships remained similar after its effect on conductivity was taken into account (data not shown).
Although in some cases, the within-day relationships between sap flow and stem pressure difference were different for the morning and afternoon periods (i.e. hysteresis was observed), overall, neither below-ground hydraulic conductance (kbg) nor reference sap flow (QL,ref) differed between morning and afternoon curves (repeated measures anova, P > 0·2 in all cases). Furthermore, the ratio of morning to afternoon QL,ref values showed no consistent variation across trees and was uncorrelated to any environmental variable (not shown). We thus averaged morning and afternoon values into a single QL,ref value for each day and tree, and these average values were used in all the following analyses. The values of QL,ref were robust towards random error around the individual data points, as shown by the fact that in 19 out of 21 days (tree G1B8), the average parameter values from the Monte Carlo analysis were similar to the original values (average deviation from original value = 0·59%, maximum deviation = 42%; average CV across the 100 Monte Carlo estimates for each day = 17%, maximum CV = 43%). For the other 2 days, some combinations of values produced bad fits that resulted in very different parameter estimates, but even for these 2 days, > 40% of the runs produced final estimates within 50% of the original value.
responses to environmental variables
The estimated values of reference sap flow (QL,ref) for each day were used as a measure of below-ground hydraulic conductance. These QL,ref values were variable across days. QL,ref was positively correlated to ln(VPD) for each of the 14 trees with more than five data points, although the relationship was significant (P < 0·05) only in two trees from Guisachan and marginally significant (0·05 < P < 0·1) in two more trees. Overall, QL,ref was better related to VPD than to any other environmental variable, including daily PAR, net radiation, soil water content or average air and soil temperatures (data not shown). However, the relationships improved substantially when QL,ref was regressed against average daily sap flow (power fit; Table 2). At Guisachan, all seven trees showed a significant increase in predicted QL,ref with increasing average QL (average r2 = 0·67). At Selm Muir, four out of seven trees showed a positive and significant relationship between QL,ref and QL (average r2 = 0·44). The relationship between QL,ref and QL was reasonably robust against the potential bias associated with the underestimation of sap flow due to using maximum ΔT as an estimate of daily ΔTmax. This is shown by the fact that, for tree G1B8, a significant relationship between QL,ref and QL was retained in 52% of the runs (62% if the significance level was raised to 0·1; n = 300 runs) when the original QL values were increased by an average of 10% (CV = 10%), thus incorporating both directional and random errors.
The above-mentioned results imply that the relationship between sap flow and stem water pressure difference was not linear across days, with larger sap flows per unit pressure difference (i.e. larger below-ground hydraulic conductance) on days with higher sap flows. To check the consistency of this result, and also to avoid the potential problem of correlating two variables, QL,ref and QL, that were not obtained independently, a different approach was also taken: we studied the relationship between daily QL and ΔP. Maximum daily values of hourly sap flow and stem pressure difference were used to characterize the two variables. By using maximum daily values instead of, for example, mid-day values, we minimized problems due to time lags between the two variables and, at the same time, ensured that true peak values (within the temporal resolution of our measurements) were detected. Similar to our previous results, maximum daily sap flow was a power function of maximum daily stem pressure difference (P < 0·001 in all trees with n > 10 in Guisachan, and P < 0·05 in all Selm Muir trees), with an exponent always > 1 (mean ± SE: 1·96 ± 0·21 for Guisachan, and 1·67 ± 0·15 for Selm Muir) (Fig. 3). Very similar patterns were obtained if average daily values were used instead of maximum values (not shown), again suggesting that time lags were not a problem.
effect of tree age and size
It is apparent from Fig. 3 that older/taller trees tended to have lower values of sap flow for a given stem pressure difference (i.e. lower kbg). A reference value of daily sap flow for a pressure difference of 0·5 MPa (Fig. 3) was used to calculate kbg. Considering all trees from the two sites, this value was negatively correlated with tree age (r2 = 0·58, P = 0·002), tree height (r2 = 0·23, P = 0·082) and Diameter at Breast Height (r2 = 0·42, P = 0·012) (Fig. 4). Tree SP3_5, the only one from the intermediate age class at Selm Muir, was a clear outlier of the general trend. If this tree was not considered, all relationships improved substantially (Fig. 4). In particular, the r2 of the relationship with tree height increased to 0·58 (P = 0·002). Similar results were obtained if the fits from Table 2 (from within-day QL vs. ΔP relationships) were used instead of those from Fig. 3.
|Tree||n days||r2||P value||Slope||Intercept|
The maximum daily change in stem pressure was unrelated to tree age or size at both sites (P > 0·05 in all cases). At Guisachan, leaf water potentials (either Ψpd, Ψmd or Ψpd–Ψmd) were likewise uncorrelated to tree age or size (P > 0·05 in all cases). In contrast, at Selm Muir, Ψmd was lower, and (Ψpd–Ψmd) greater, for 80-year-old trees than for 25-year-old trees (P < 0·05). On average, (Ψpd–Ψmd) = 0·82 ± 0·10 MPa for 80-year-old trees, and 0·54 ± 0·02 MPa for 25-year-old ones. Overall, combining the data from the two sites, the contribution of below-ground resistance to whole-tree hydraulic resistance (%Rbg) declined significantly with tree height (r2 = 0·54, n = 10, P = 0·015) (Fig. 5). The relationships between %Rbg and diameter at breast height and tree age were also negative, but only marginally significant (r2 = 0·34, n = 10, P = 0·079; and r2 = 0·38, n = 10, P = 0·058, respectively) (Fig. 5).
Before exploring the implications of our results with regard to the variability of below-ground hydraulic conductance and its relationships with tree age and size, it is necessary to make some methodological considerations. Besides the issues related to the accuracy of the Granier and LVDT techniques, our analyses are based upon the following assumptions: (i) that the modulus of elasticity, used to convert diameter variations into changes in stem pressure, is constant over time; (ii) that equilibrium is reached at night, so that sap flow goes down to zero and water potential inside the plant equilibrates with soil water potential; and (iii) that any time lag between changes in sap flow or stem diameter and its detection is < 15 min or, at least, there is no consistent, differential lag for the two measures. These assumptions will be considered in the following paragraphs.
The modulus of elasticity (E) of conifer wood has been shown to change as a function of several variables. These variations, however, are unlikely to be relevant in the present study. For example, Silins, Lieffers & Bach (2000) detected no effect of temperature on stem E for temperatures above 0 °C in living lodgepole pines Pinus contorta. In addition, changes in xylem water content above the fibre saturation point have been shown to have very minor effects within a species [cf. Cannell & Morgan (1987) and Mencuccini (1995) for Scots pine].
It is well known that sap flow can be substantial at night [cf. Caird, Richards & Donovan (2007) and Dawson et al. (2007) for recent reviews], and that this can result in a disequilibrium between soil and plant pre-dawn water potential (e.g. Donovan, Richards & Linton 2003; Kavanagh, Pangle & Schotzko 2007). However, our main results are likely to be robust to this effect, since we are mostly concerned with the relationship between sap flow and stem shrinkage, not with their absolute values, and the equilibrium assumption made in their derivation has similar consequences for both variables. Besides, the disequilibrium in pre-dawn water potential is likely to be lower at the base of the stem, as studied here, than in leaves.
The presence of time lags in the measurements might be a more critical assumption, particularly with regard to the analysis of within-day relationships between sap flow and changes in stem water pressure (cf. Fig. 2). While the existence of time lags between changes in stem water pressure and the corresponding changes in total stem diameter has been demonstrated (e.g. Génard et al. 2001), we do not know of any study suggesting the presence of those lags when diameter variations are measured below the cambium. Sevanto et al. (2002, 2003) studied the time lags between xylem and whole-stem diameter changes in Scots pine, and concluded that they were due to the exchange of water between the phloem and the xylem (Münch flow). Regarding the detection of sap flow, the thermal capacitance of wood could potentially lead to time lags between changes in sap flow and their detection using the Granier technique (E. Nikinmaa, personal communication). However, we know of no studies examining this possibility and its potential impact on the detailed study of sap flow dynamics. At any rate, this problem might at most modify the relationships between sap flow and stem diameter within a day (cf. Fig. 2), never the between-day patterns reported in this study.
within-day variation of below-ground hydraulic resistance
The shape of the within-day relationship between stem pressure difference and sap flow found in this study (Fig. 2) is consistent with our current understanding of root water transport. According to the composite model of root water transport, when hydrostatic pressure gradients are low (e.g. in the early morning), the relatively inefficient cell-to-cell pathway dominates water transport across roots, resulting in low hydraulic conductance. As hydrostatic gradients increase in magnitude during the day, there is a switch to predominantly apoplastic transport, resulting in greater hydraulic conductance (Steudle 2001). This is exactly what is seen in Fig. 2. It is important to note, however, that our results are also totally consistent with the simpler one-membrane two-compartment model of Fiscus (1975), which was actually used to fit the data (eqn 2). While our data are not sufficient to distinguish between these two models, they provide a strong indication of within-day variation of root hydraulic conductance in full-grown trees in the field.
The shapes of our relationships (Fig. 2) are remarkably similar to those obtained by Kaufmann (1975) when relating xylem water potential to transpiration in Picea engelmanni. An alternative interpretation of Fig. 2 would be that the apparent changes in the slope of the relationship between sap flow and stem pressure difference are not due to processes occurring in the root system but to changes within the stem. The most obvious candidates would be the occurrence of xylem embolism and the radial redistribution of water within the stem. The second of those effects is likely to be very important when total stem diameter variations are considered (cf. Čermák et al. 2007), as opposed to xylem diameter changes. Herzog, Häsler & Thum (1995), for instance, related the diurnal hysteresis they found in the relationship between sap flow and stem diameter variations to the exchange of water between the xylem and the phloem. In our case, however, those effects are unlikely to be relevant. Although we sometimes observed substantial hystereses in the diurnal relationships between sap flow and stem pressure difference: (i) the magnitude of the effect was uncorrelated to any of the measured environmental variables; (ii) it was non-significant overall (i.e. across all days, the slope of the relationship was similar in the morning and in the afternoon for all trees); and (iii) it was not consistent. That is, the morning part of the curve in Fig. 2 was not consistently above (or below) the afternoon part, as would be expected if embolism or hydraulic redistribution were occurring in the stem. Within-day changes in the depth of active sapwood, which were not evaluated in this study, could also explain the nonlinearity in the relationships between stem pressure difference and sap flow (Fig. 2).
between-day changes in below-ground hydraulic resistance
Our results strongly suggest that below-ground hydraulic resistance is not only variable within a day but also among days. Importantly, the variation is in the direction of greater conductances in days with greater evaporative demand and greater sap flow (Table 2 and Fig. 3). Several authors have measured variable root, or whole-plant, hydraulic resistance in herbs, shrubs or small seedlings (e.g. Tsuda & Tyree 2000 and references cited therein). There is also some previous evidence suggesting increasing hydraulic conductance with sap flow in mature trees. Herzog et al. (1995), using a similar approach to ours, showed that the best fit between daily radius shrinkage and daily sap flow of Picea abies was obtained with a parabola with ever increasing slope. Note, however, that they measured total stem diameter changes, not just xylem variations as in our case. More recently, Franks, Drake & Froend (2007) showed that whole-plant hydraulic conductance, estimated from diurnal changes in leaf water potential and leaf-level transpiration data, increased also as a function of transpiration rate in mature Eucalyptus gomphocephala trees.
There are several mechanisms that could explain the increases in kbg. First, an increase in root hydraulic conductance with sap flow and evaporative demand is predicted by the composite transport model (Steudle 2000). Indeed, the nonlinearity in the within-day relationship between QL and ΔP (Fig. 2) explains, at least in part, why days with lower flows, and lower stem pressure difference, had lower hydraulic conductance. In that respect, it is interesting to note that most of the nonlinearity in the within-day (Fig. 2) and between-days relationships (Fig. 3) starts at similar stem pressure differences, around 0·2 MPa. This value is also roughly consistent with Fiscus’ (1977) results on soybean (Glycine max). Second, there is increasing evidence supporting that short-term changes in root hydraulic conductance are mediated by aquaporins (Javot & Maurel 2002). A cohesion–tension mechanism has been proposed for the gating of water channels that predicts the inhibition of aquaporin activity at high solute concentrations (Ye, Wiera & Steudle 2004), and could potentially explain the increase of hydraulic conductance at high flows.
Alternative mechanisms, such as the direct effect of changing electrolyte concentrations in sap (Zwieniecki, Melcher & Holbrook 2001), the effect of phloem-mediated signals, changes at the soil–root interface or the positive effect of embolism as a water source to rehydrate the sapwood under certain conditions (T. Hölttä, unpublished data), could also explain the short-term changes in kbg. Morphological changes (e.g. growth of new roots) seem unlikely to play a role in such short-term responses.
Our evidence for variable root hydraulic conductance of trees adds to many recent studies showing variable hydraulic conductance of other plant parts, most notably leaves (e.g. Nardini, Salleo & Andri 2005). The implications of plant hydraulic conductance being a positive function of sap flow are potentially very important. For the plant, such dependence would provide relatively stable water potential gradients over a wide range of evaporative demand conditions. The advantages of this behaviour are obvious [see Franks et al. (2007) for a detailed discussion]. For instance, it would greatly decrease the likelihood of suffering dangerous levels of xylem embolism. On a different note, if variable tree hydraulic conductance was shown to be a general phenomenon, it should be considered when interpreting whole-plant conductance estimated from sap flow and water potentials data, and should be taken into account in the modelling of plant water relations and of plant and ecosystem responses to drought.
The predictions from Fig. 5 are consistent with the 53% contribution of below-ground to whole-tree resistance measured by Roberts (1977) and the 40% value obtained by Irvine & Grace (1997) on Scots pine trees (Fig. 5). Our results are also in general agreement with those by Hellkvist et al. (1974) on Picea sitchensis. The comparison of the water potential profiles they obtained suggests that most of the resistance below-ground might be near the bole, but this remains to be tested for other species and situations.
Our results show that whereas the total below-ground hydraulic resistance per unit leaf area increases with tree age and height (Fig. 4), the contribution of below-ground to whole-tree hydraulic resistance actually declines with tree age/height (Fig. 5). These findings are indicative of a relative increase in below-ground carbon allocation with age/height in Scots pine, in agreement with some empirical data (Vanninen & Makela 1999; Makkonen & Helmisaari 2001) and with the optimality hypothesis put forward by Magnani et al. (2000).
Some words of caution are, however, required. The modulus of elasticity (Er), for instance, is known to change as a function of tree age/size. However, Mencuccini, Grace & Fioravanti (1997) found that the variation was limited to trees younger than 30 years in Scots pine, whereas most of our trees were older than that. In fact, the significance of the relationships in Figs 4 and 5 remained the same if the values for the youngest trees were corrected according to the patterns found by Mencuccini et al. (1997). Second, we assumed that stem water potentials equilibrated with soil water potentials every night and, thus, that there was no day-to-day storage of water below-ground. This is potentially problematic because it is well known that the contribution of storage to water use increases in taller trees (e.g. Phillips et al. 2003). However, (i) we only considered below-ground tissues, and the effect of this component of storage is likely to be smaller than for the whole tree; and (ii) in all cases, our assumptions were consistent, in the sense that in Fig. 5 we also assumed that leaf water potentials equilibrated with soil water potentials overnight, and in all the other calculations (e.g. Fig. 4), we assumed that sap flow declined to zero when stem and soil water potentials equilibrated.
The age-related increase in hydraulic resistance below-ground (cf. Fig. 4) should be included, along with the increase in path length above-ground, in any explanation of the changes of tree hydraulics and growth with tree age and size (cf. Ryan et al. 2006). Our study also suggests a decline in the contribution of roots to whole-tree hydraulic resistance with tree age/size, probably at the cost of increased below-ground carbon allocation. Allocating carbon above- vs. below-ground is likely to have implications in terms of costs and overall hydraulic effects, since root xylem tends to best less costly in terms of carbon and much more efficient in terms of water transport (Martínez-Vilalta et al. 2002; McElrone et al. 2004). All these aspects deserve further study and have to be considered if we are to understand the implications of increasing size for tree growth and function.
In this paper, we have provided evidence that below-ground hydraulic conductance in mature Scots pine trees in the field varies over several temporal scales. We found significant variation both within and between days, in the direction of greater conductance when sap flow rates (and evaporative demands) were higher. The implications of this result are wide ranging, from general tree water relations to studies and models of seasonal ecosystem water use. On the other hand, below-ground hydraulic resistance increased during tree development, although its contribution to whole-tree resistance tended to decline in old/tall trees, with potential implications in the study of tree ageing and the functional implications of tree size. Several aspects of our results remain to be addressed in more detail in future studies. Those aspects include the ecophysiological implications of variable kbg, as well as the mechanism underlying these variations (physiological processes vs. processes taking place in the root–soil interface, for example), and the integration of our results with other age- and size-related patterns previously reported, such as the increased reliance on stored water with tree development.
We would like to thank Johanna Pulli, Nick Weir, Chris Kettle, Dr Rosa Maria Roman Cuesta, Dr Hazandy A. Hamid, Georgios Xenakis, Manuel E. Lucas Borja, Craig Menzie, Hanna M. Stark & Jamie Gardiner for field and laboratory assistance, and Prof. James Richards and three anonymous reviewers for their comments on an earlier version of the manuscript. Georgios Xenakis provided the soil descriptions. The UK Forestry Commission allowed access to the field sites and was helpful throughout the study. Mr Alexander Grigg kindly allowed us to install our meteorological station in his property at Guisachan. This research was funded by NERC (UK) competitive grant NER/A/S/2001/01193 to M.M.
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