Journal of Experimental Botany, Vol. 53, No. 379, pp. 2369-2379,
December 1, 2002
© 2002 Oxford University Press
How do water transport and water storage differ in coniferous earlywood and latewood?
Received 10 May 2002; Accepted 23 July 2002
Department of Wood Science and Engineering, Oregon State University, Corvallis, OR 97331, USA
1 To whom correspondence should be addressed. Fax: +1 541 737 3385. E-mail: jc.domec{at}orst.edu
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The goal of this research project was to determine the water transport behaviour of earlywood versus latewood in the trunk of 21-year-old Douglas-fir [Pseudostuga menziesii (Mirb.) Franco] trees. Specific conductivity (ks) and the vulnerability of xylem to embolism were measured on a single growth ring and in a subset of earlywood and latewood samples within the same ring. Earlywood/latewood ratio, trunk water potential (
) and relative water content (RWC) were used to predict differences in conductivities and vulnerability to embolism. Earlywood has about 11 times the ks of latewood, and up to 90% of the total flow occurred through the earlywood. Earlywood’s vulnerability to embolism followed the same trend as that of the whole wood, with 50% loss of conductivity at –2.2 MPa (P50). Latewood was more vulnerable to embolism than earlywood at high , but as decreased, the latewood showed very little further embolism, with a P50 <–5.0 MPa. The lowest trunk estimated in the field was about –1.4 MPa, indicating that latewood and earlywood in the field experienced about 42% and 16% loss of ks, respectively. The higher vulnerability to embolism in latewood than in earlywood at field was associated with higher water storage capacity (21.8% RWC MPa–1 versus 4.1% RWC MPa–1, latewood and earlywood, respectively). The shape of the vulnerability curve suggests that air seeding through latewood may occur directly through pores in the margo and seal off at lower pressure than earlywood pores. Key words: Cavitation, earlywood, embolism, hydraulic conductivity, latewood, relative water content.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
There are two distinct zones of growth within a tree ring: earlywood and latewood. The early season growth in a tree, which produces earlywood (periclinal growth), accounts for 40–80% of a ring’s growth in width for a year. As the growth rate slows and stops during autumn, the cells laid down are smaller, denser, and mechanically stronger (therefore appearing darker).
Water is the most limiting ecological resource for most tree and forest sites (Richter, 1976; Waring and Running, 1998). Change in earlywood/latewood growth patterns reflect, in part, the control of wood properties by water availability. Factors such as temperature, sunlight conditions, and the slope of the hillside also can affect the width of tree rings and the amount of earlywood or latewood (Larson, 1962). Numerous studies have shown that for conifers, in general, higher wood density, as a consequence of a greater proportion of latewood, is triggered by drought stress (see review by Zobel and Van Buijtenen, 1989). Latewood formation appears to be more sensitive to climate than earlywood formation (Bannan, 1967; Lebourgeois, 2000). In growing periods with lower precipitation than normal and excessively low temperatures, tree growth is diminished and the proportion of latewood is higher. Conversely, when growing conditions are ideal, tree growth is enhanced and the proportion of latewood reduced (Kennedy, 1961).
Although the significance of the outermost ring to the hydraulic conductivity and earlywood and latewood to xylem embolism of the whole stem have been quantified in ring porous trees (Ulmus americana, Ellmore and Ewers, 1986; Quercus cerris, Lo Gullo et al., 1995), no study has investigated it in a conifer species or within the earlywood and the latewood of the same ring. Furthermore, there are no reports of a direct measurement of vulnerability to embolism within a single ring and within its components. It is logical to infer that earlywood and latewood would have very different hydraulic properties.
The differences in hydraulic conductivity and vulnerability to embolism between earlywood and latewood have been linked to differences in xylem anatomy (Zimmermann, 1983). Hydraulic conductivity is proportional to the fourth power of the radius of xylem conduits (Gibson et al., 1985; Tyree and Ewers, 1991). Earlywood tracheids have wider lumen diameters than latewood tracheids (Panshin and de Zeuuw, 1980; Ewers et al., 1997). The trade-off, however, is that conduits with high conductivity might be more vulnerable to embolism (Schulte and Gibson, 1988; Sperry and Saliendra, 1994; Hargrave et al., 1994). These data suggest that earlywood can transport a large proportion of water to the main trunk when plant-water status is favourable, but might limit plant water use during drought. In hardwoods, the small-diameter latewood vessels and the small-diameter vasicentric tracheids near the larger vessels are thought to provide water transport once the earlywood and/or wider vessels have become air-filled (Carlquist, 1985; Cochard et al., 1997). In softwoods, the question remains unsolved. Does latewood remain conductive after the earlywood becomes air filled, or does it not?
Embolism due to drought is thought to be caused by air seeding at inter-conduit pit membranes (Zimmermann, 1983; Crombie et al., 1985). Air seeding in conifers occurs through inter-tracheid pit membrane when the torus becomes displaced from its normal sealing position (Sperry and Tyree, 1990). They found that non-sealing of bordered pits in latewood in conifers could account for 20% of the total hydraulic conductivity after the earlywood had sealed off at low water potential (). The shape of the vulnerability curves varies among and within species and it is thought that they reflect the water stress environment under which the plants grew (Tyree and Sperry, 1988; Tyree et al., 1994; Matzner et al., 2001).
Much less is known about earlywood versus latewood responses to embolism, and about how much embolism occurs in these two zones of a growth ring at field . The proportion of earlywood versus latewood within a ring and xylem anatomy might be adaptive hydraulic traits and not simply the consequences of water balance in the field. Earlywood and latewood might regulate water transport under stress, based on their influence on hydraulic conductivity, embolism vulnerability, and internal storage capacity. It is hypothesized that, on an anatomical basis, as predicted by the ‘air-seeding’ hypothesis, hydraulic functions are directly linked to bordered pit functioning and on the mechanical properties of the pit membrane structure proposed by Petty (1972). Embolism developing in earlywood tracheid would not spread to adjacent tracheids because the air-seeding tension created between a water-filled tracheid and an empty one would exceed the mechanical tension required to pull an air bubble through the margo. The torus would seal off the chamber before air can be drawn through the pores. Therefore, reduction in hydraulic conductivity in earlywood would be linked to the mechanical properties of the membrane. Within the latewood, air would go through the pores before the torus can be sealed because of its high mechanical resistance to displacement. Thus, reduction in hydraulic conductivity in latewood will be more a function of the size of the pores through the margo. Because of their bordered pit structure, earlywood tracheids are therefore expected to be both more efficient and safer from embolism than latewood. If, as expected, embolism resistance is higher within earlywood, a safe xylem is not costly in term of carbon investment.
The objectives of this study were to compare earlywood and latewood water transport capacities within a single growth ring in fast-growing Douglas-fir trees [Pseudostuga menziesii (Mirb.) Franco]. Hydraulic parameters (conductivity, vulnerability to embolism, water storage capacity) were measured on entire wood samples, as well as within earlywood and latewood samples. Field data measurements of and relative water content were used to confirm laboratory results and to describe earlywood and latewood water transport and storage when water is under tension.
This research was designed to test the following three hypotheses: (1) sapwood conductivities are lower in latewood and in whole wood than in earlywood, (2) earlywood and latewood conductivities weighted by the proportion of earlywood/latewood explain the whole wood conductivity, and (3) vulnerability to embolism is higher for latewood than for earlywood.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Plant material and sample preparation
The study was carried out in an even-aged (21-year-old) Douglas-fir stand (elevation 277 m, 44°43' N, 123°20' W) 15 km northwest of Corvallis, Oregon, growing on an inceptisol soil. The mean annual temperature and annual rainfall (1961–1996) are 12.4 °C and 1800 mm, respectively (Table 1; www.orst.edu/Dept/IPPC/wea/). Douglas-fir was chosen because of its fast growth, which gives wide growth rings with distinct latewood. In mid-June 2001 (before the start of the summer drought), five trees were selected randomly and felled. A disc 20 cm thick was cut at breast height from each tree and transported immediately in a wet plastic bag to the laboratory where blocks were prepared. From each cross-sectional disc, six blocks, at approximately 60° intervals around the circumference, were cut within the same single ring with a hammer and chisel (Domec and Gartner, 2001).
|
The samples were chiselled out of the wood with the long axis parallel to the grain, then submerged in water and put under vacuum for 48 h to refill some of the embolized tracheids. Their original dimensions were 150 mm (axial direction), 10 mm tangential direction, and 7–9 mm radial direction (the width of one growth ring). Samples were randomly designated as A–F. All hydraulic measurements on sample A were done on the entire sample, i.e. both the earlywood and the latewood were left intact. Before the final measurements, samples B–F were sawn in half, to 75 mm in the axial direction. One half was designated B1–F1 and the other half B2–F2. Using a chisel and razor blades, the latewood was removed from samples B1–F1, leaving just earlywoood, and the earlywood was removed from samples B2–F2, leaving just latewood (Fig. 1).
|
Specific and hydraulic conductivities
Specific conductivity (ks, in m2), is a measure of the hydraulic efficiency of the xylem in relation to the cross-sectional area of the wood and was calculated according to Darcy’s law (Edwards and Jarvis, 1982). Initial specific conductivity (ks(i)) was measured on each 130–150 mm segment (intact segments A–F, before they were sawn in half) using the membrane-lined pressure sleeve needed to ensure fluid did not leak from the sides of samples (Spicer and Gartner, 1998a). Samples were soaked in water, then ks(i) was measured at a pressure difference of 2.8 kPa, using filtered (0.22 µm) water adjusted with HCl to pH 2 to prevent microbial growth. The hydraulic pressure head has been preselected as low enough to avoid any refilling of the embolized tracheids. Efflux was collected in a 1 ml-graduated micropipette (0.01 ml graduation). When the flow was steady, the time required for the meniscus to cross six consecutive graduation marks was recorded. Hydraulic conductivity, kh (in m4), which expresses the volume flow–pressure relationship, but not on an area basis (Tyree and Ewers, 1991), was defined as kh=Axks, where A is the cross-sectional area (m2) of the sample.
Vulnerability curves and water storage capacity
Vulnerability curves (VCs) of the wood samples were constructed by means of the air injection method (Salleo et al., 1992; Sperry and Saliendra, 1994) adapted for samples taken directly from the trunk (Domec and Gartner, 2001). The air injection method is based on the theory that the negative water potential () required to pull air into a conduit and cause embolism is equal to the positive air pressure required to push air into the conduit when is equal to the atmospheric pressure. The objective was to measure the percentage loss of conductivity (PLC) on segments by moving the sample alternately between the membrane-lined pressure sleeve for determining ks and the double-ended pressure chamber for causing embolism. The segments were inserted into the air-injection chamber, with both ends protruding. The air-tight chamber was sealed with rubber gaskets at both ends, held in place by stainless end caps. Pressure was induced into the chamber stepwise, and held constant for 1 min. After each air injection ks was remeasured and the percentage that ks(i) was below ks(i) gave the sample’s PLC. The temperature of the solution, the fresh mass (Mf), the volume (Vf), determined by water displacement (Archimedes’s principle), and the length of each sample were recorded before and after each conductivity measurement. The samples always weighed the same before and after, giving no evidence of refilling. VCs were determined by means of plotting PLC versus , where is predicted as the negative of the applied air pressure (Pockman and Sperry, 2000).
After ks(i) had been measured on intact samples A–F, VCs were constructed in two ways. First, sample A was used to construct an entire VC, subjecting it to air pressures ranging from 0.5–5.0 MPa. Second, different samples B–F were used for different air pressures to construct one curve (Fig. 2). After ks had been determined for samples B and C, they were sawn in half to prepare samples B1 and C1 (only earlywood) and B2 and C2 (only latewood), and ks was measured again (samples B, C, B1, B2, C1, and C2) were used as replicates for ks at full saturation). After ks had been determined for sample D, it was pressurized to 0.5 MPa, its ks was remeasured, then it was sawn in half to prepare samples D1 and D2, on which ks was measured. Likewise, after ks had been determined for samples E and F, they were pressurized to 1.0 and 3.0 MPa, respectively, their ks was remeasured, then they were sawn in half to prepared samples E1, E2, F1, and F2, on which ks was measured. For earlywood and latewood samples, PLC was determined by means of the paired segments methods, which compared ks(i) of samples D1, D2, E1, E2, F1, and F2 to the average ks(i) of samples B1, B2, C1, and C2 from the same disc (Fig. 2). To test for differences between the paired segment method and the regular method (consisting of measuring PLC within the same samples at different ), a comparison was made at each between samples A and intact samples B–F.
|
Embolized area estimated by the staining method
Following each final conductivity measurement, each sample was perfused with filtered (0.22 µm) safranin-O (0.5% aqueous solution) under 15 kPa pressure head for 20 min while still enclosed in the pressure sleeve apparatus. The hydraulic pressure head has been preselected as high enough to allow safranin-O to flow without refilling any of the embolized tracheids. For the initial measurements, the samples always stained completely, giving no evidence of embolism. The percentage of unstained wood area of each sample used for the VCs was analysed with an image analysis system consisting of a compound microscope, a video camera, a computer, and the software NIH Image (v. 1.60, Rasband, 1996).
Earlywood and latewood proportion
Total widths of the earlywood, latewood, and total ring were determined for each sample before its halves were cut down to just latewood or just earlywood. These measurements were made with the tree-ring measuring device as follows. The sample was placed on a moving Velmex measuring table equipped with an AcuRite ENC 150 linear encoder and a QuickCheck-1000 digital measuring device and display. By watching the image of the growth ring on a monitor projecting the sample’s magnified video image, and then by moving the stage, one can read out the growth ring width to 0.01 mm precision. Average earlywood proportion for each sample was then calculated.
Moisture content, relative water content and water storage
Moisture content (MC) is defined as the mass of water present in a piece of wood expressed as a percentage of the mass of ovendry wood (Md):
Relative water content (RWC) is the mass of water in the sample divided by the potential maximum values of water in the sample. To get a rate of change in RWC associated with cavitation, RWC was determined for each sample used to construct a VC, initially and after each pressure, by recording Vf (cm3) and Mf (g). Following final pressurization, Md (g) was recorded after drying at 104 °C. Length was used to back-calculate the volume of cell wall material (Vs, cm3) and Md (g) at each given pressure. RWC can then be calculated as follows:
where DH2O is the density of water (g cm–3). Vs was calculated from Md assuming that latewood and earlywood dry-cell-wall material has a density of 1.53 g cm–3 (Kennedy and Warren, 1969; Kellog et al., 1975; Siau, 1984).
Water storage capacity, defined as the amount of water withdrawn from the stem at given water potential (Holbrook, 1995), was expressed as the change in RWC per unit . This definition of capacitance made it possible to compare differences in storage capacities that are related to a difference not only in total water volume, but also in tissue density (Domec and Gartner, 2001). The volumetric RWC-based capacitances (CRWC) for a given range of pressures were determined after each conductivity point as follows (Edwards and Jarvis, 1982):
Capillary water changes cannot be estimated accurately by using the pressure chamber, because positive pressure cannot displace capillary water (Zimmermann, 1983; Tyree and Yang, 1990). The hypothesis of capillary water storage states that water storage comes from the change in the radius of the meniscus between the cell wall and the gas space (Zimmermann, 1983). If this hypothesis is correct, then maximum capillary water storage is released at a pressure close to zero, and stops before 0.6 MPa (Holbrook, 1995; Tyree and Yang, 1990). Therefore, to determine whether the slope of the dehydration curve was constant throughout its range, and to avoid underestimating capillary water at low applied pressure, capacitance values were computed for three phases in each dehydration curve: a phase from 0–0.5 MPa (C0–0.5), a phase from 0.5–1.0 MPa (C0.5–1.0) and a phase from 1.0–3.0 MPa (C1.0–3.0).
Wood density and volume occupied by cell wall material, by water and by gas
Wood density values were determined for each sample tested hydraulically:
For each type of sample, the volume occupied by water, cell wall material, and gas (on a fresh volume basis) was calculated as:
Vgas(%) = (1–Vcell wall + VH2O) 100(7)
Field measurements
To examine the RWC in earlywood and latewood, eight dominant trees were cored with a 12 mm increment borer during winter (10–15 March 2001, before the growing season), and during summer (25–30 September 2001, before the rain started). Cores were wrapped in plastic wrap immediately after removal and placed in a cooler. They were returned to the laboratory the same day and processed. The last growth ring was removed and the next two growth rings were divided into earlywood and latewood. As described previously, Vf, Mf, and Md were measured and RWC was calculated. The same days and on the same trees, trunk at breast height was estimated (on leaves bagged in aluminium foil to prevent transpiration) with a pressure chamber (PMS Instrument Company, Corvallis, Oregon). Three foliage-bearing branches per tree were measured. The relationship between the negative of the applied pressure and RWC and PLC was determined from samples tested in the laboratory, then PLC was estimated, based on the measured and RWC of standing trees in the field.
Statistical analysis
Least squares methods were used to fit relationships between the hydraulic parameters and the applied pressure, as well as the linear and non-linear relationships between hydraulic parameters. Analysis of variance (ANOVA) was used to determine differences in hydraulic parameters between the entire samples and the subset of samples, with tree as a blocking factor. Paired t-tests were used specifically to test the difference in hydraulic parameters between earlywood and latewood. All statistical procedures were conducted with Statistical Analysis Systems software ((SAS Institute Inc, 1997).
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Sample shape, staining tests
The average latewood made up 33% of the ring (±2%; ranged from 26% to 40%) (Table 1). The sum of the measured ks in earlywood and latewood, weighted by the proportion of earlywood/latewood, was a good estimate of ks measured within the whole samples (Fig. 3a). The slope of the regression line was not significantly different from 1 (P=0.26). Neither the hydraulic parameters nor the estimated capacitances differed between the whole samples (B–F) and the subsample pieces (B1, B2 to F1, F2; P >0.62, data not shown). Whole long samples (A) and small subsample pieces (D–F) had similar PLC at 0.5, 1.0, and 3.0 MPa (Fig. 3b). There was a strong relationship between the estimated PLC based on the unstained part of the samples (non-functional wood) and the actual PLC measured (Fig. 4). The slope of the regression line, however, was significantly lower than 1 (P=0.04).
|
|
Hydraulic parameters within earlywood and latewood
Earlywood had significantly higher ks than latewood (P <0.001, Table 2). Latewood had less than 9% of the ks of earlywood and 13% of the ks of whole wood. At the ring scale, latewood (accounting for 33% of the surface area) provided only 5% of the total kh (Table 2).
|
Vulnerability to embolism varied among wood type samples. Latewood samples were more vulnerable to embolism than earlywood samples at 0.5 MPa and 1.0 MPa, but not a 3.0 MPa (Table 2; Fig. 5a). Earlywood samples were not significantly different from the whole wood sample (P >0.21), and followed the same trend. The xylem pressures causing 50 PLC (P50) for the entire VC and earlywood were –2.3±0.1 and –2.1±0.2 MPa, respectively (Fig. 5a). At any applied pressure, whole wood samples and earlywood samples were significantly different from latewood samples (P <0.04).
|
Water deficit (100–RWC) showed a sigmoidal change with applied pressure within whole wood samples. The steepest slope occurred between 2.0 and 3.0 MPa (Fig. 5b). For latewood, water deficit increased exponentially with higher applied pressures to reach a maximum at 40% (Fig. 5b). Earlywood had a smaller decrease in water deficit at 0.5 and 1.0 MPa than latewood, but it had a much greater decrease and was significantly different than latewood at 3.0 MPa (P=0.03). Earlywood samples had water deficit similar to that of whole-wood samples at 0.5 and 1.0 MPa, but they had significantly lower values at 3.0 MPa (P <0.01). Latewood had significantly different values in water deficit than whole-wood samples for the three different applied pressures (P <0.05, Fig. 5b).
Latewood had a much higher water storage capacity than earlywood between 0.5 and 1.0 MPa (22 versus 4% RWC MPa–1, latewood and earlywood, respectively). This trend was reversed between 1.0 and 3.0 MPa (5% versus 23% RWC MPa–1, latewood and earlywood, respectively; Table 3). There was no significant difference between earlywood and latewood for C0–0.5 (Table 3). There was no significant difference between whole sample and latewood for C0.5–1.0, but there was a significant difference between the whole sample and earlywood and between the whole sample and latewood for C0–0.5 and C1.0–3.0 (P <0.05). Within the earlywoodsamples, there was a significant difference in water storage capacity between C0–0.5, C0.5–1.0 and C1.0–3.0 (P <0.006). Water storage capacities were not significantly different between the first two phases for the latewood samples (P=0.9) and between the last two phases for the whole wood samples (P=0.7)
|
Latewood and earlywood composition
Percentages of air and RWC at full saturation were the same within both types of wood, however all other wood properties were statistically different (P <0.01; Table 4). The latewood had a higher percentage of cell wall and a lower percentage of water. At 3.0 MPa, latewood had a lower percentage of air, but the same percentage of water. Latewood had more than twice the density of earlywood (0.26 g cm–3 versus 0.60 g cm–3).
|
Comparisons between field measurements and laboratory estimates
Minimum trunk
measured at the end of the summer never dropped below –1.4±0.2 MPa, for a calculated minimum RWC of 69±3% for the whole ring. Latewood RWC was significantly lower than earlywood RWC (P=0.002). There were 4% and 8% seasonal decreases in RWC in earlywood and latewood, respectively (Table 5). The calculated PLC values from summer trunk were 16% and 42% in earlywood and latewood, respectively (Table 5). There was close agreement between the estimated PLCs from the measured and RWC for earlywood, but not for latewood.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Methodological issues
Using small or long samples gave statistically inseparable results for ks or vulnerability to embolism (Fig. 3b). Cutting the samples in two pieces (one to be used for earlywood, the other for latewood) did not affect the degree of embolism, which made it possible to continue with the data analysis. This finding shows that damage to sample edges has no significant effect on ks or vulnerability to embolism, validating the appropriateness of this method (Domec and Gartner, 2001).
Earlywood/latewood segmentation to conductivity and vulnerability to embolism
As expected, latewood had much lower ks than earlywood. The very low ks found in latewood can be explained by the small tracheid diameter of its cells compared to earlywood cells. Hagen–Poiseuille’s law predicts that the large earlywood tracheids are responsible for most of the water flow within a single ring (Zimmermann, 1983). Earlywood ks exceeded latewood ks 11-fold, which would correspond to a 1.8-fold increase in tracheid diameter (Hagen–Poiseuille’s law), all other factors being equal. This result agrees with the ratio of tracheid diameters described in the literature for conifers (McMillan, 1968; Cown, 1975).
The results supported the hypothesis that earlywood transports water more efficiently and is less vulnerable to embolism than latewood at occurring in the field under normal conditions (Tables 2, 5). This result contrasts with that reported in a ring-porous species ((Lo Gullo et al., 1995). Using the staining method, they showed that latewood vessels of young trees of Quercus cerris were narrower, shorter and less vulnerable to embolism than earlywood ones.
Within a growth ring, there was a positive relationship between ks and safety, and there is no trade-off between the two. However, the margin of safety between the measured in the field and the beginning of embolism was less than 0.5 MPa. This study confirmed that wood from the trunk base of Douglas-fir trees may operate close to the edge of hydraulic safety because of the high vulnerability to embolism of earlywood below –2.0 MPa ((Domec and Gartner, 2002a).
Embolism formation is thought to be related not to conduit size, but rather to pore size at the interface of two tracheids through the bordered pits (Tyree et al., 1994). Indeed, the low resistance to embolism is correlated with structural features of the bordered pit membrane (Petty, 1972; Bolton and Petty, 1978; (Domec and Gartner, 2002b). The small and thick torus and strands of the bordered pits found in latewood might not allow the margo to act as a valve, preventing air bubbles from spreading from one embolized tracheid to another. It has been reported that in Pinus sylvestris (L.), latewood membranes were more rigid than earlywood ones and that they could not seal off completely at field values (Gregory and Petty, 1973). Pores between the strands of the membrane are smaller in latewood than in earlywood (Petty and Puritch, 1970; Fengel, 1972), suggesting that air-seeding occurs directly through these pores. The mechanical resistance of the torus would exceed the mechanical tension required to pull an air bubble through the membrane. The mechanism of water-stress-induced embolism in latewood would then be similar to that of vessel-bearing plants (Sperry and Tyree, 1988). The resistance of embolism in latewood would then be proportional to the size of the pores in latewood, which can explain the observed decrease of conductivity commencing immediately at 0 MPa and below. The shape of the curve before reaching the plateau (0–1.0 MPa, Fig. 5b) might reflect the pore size distribution within the strands of the membrane in latewood. The membranes were probably completely deflected at <–1.0 MPa and the sealed torus probably created a closed system, protecting the tracheids responsible for the remaining 40% of conductivity. Regarding the earlywood, it has been reported that the porosity of the membrane that holds the torus is too large to prevent the air meniscus passage at values lower than –0.1 MPa, but it is elastic enough to be completely deflected and to seal off the torus (Sperry and Tyree, 1990). The slippage of the torus from its sealed position created gaps big enough to develop cavitation in adjacent tracheids. This result might explain why there was a complete loss of conductivity for lower applied pressures in earlywood but not in the latewood (Fig. 5a). The thicker torus of latewood would prevent it from slipping off from its sealed position (Domec and Gartner, 2002b).
Back-calculation of the part of latewood in the remaining ks at –3.0 MPa (Fig. 5a) indicated that non-sealing of latewood bordered pits in Douglas-fir appeared to account for 30% of the total hydraulic conductivity that remained. With its very low ks and proportion (33%) in a ring, however, fully conductive latewood can account for only 5% of the initial conductivity at full saturation, although it can account for 16% of the remaining conductivity at –3.0 MPa. This remaining conductivity in latewood represents only 2% of the initial conductivity, which is far from the 20% calculated by Sperry and Tyree (1990). By taking a mature tree with small growth rings and a higher proportion of latewood (close to 55%) (De Kort, 1993), latewood would still account for only 11% of the total ring conductivity at –3.0 MPa (during severe drought). To account for 50% of the whole ring conductivity, latewood would have to represent 90% of the whole ring area at full saturation, and 75% at –3.0 MPa. Such a high proportion of latewood within a growth ring is unlikely to be found in normal conifer wood, but it can often occur in compression wood, which forms on the lower sides of branches or in leaning trunks (Westing, 1968; Timell, 1986).
Compression wood of stems has wide annual rings and is much denser than normal wood because of the elevated proportion of latewood (Park, 1984; Yoshizawa et al., 1987). It has been shown that compression wood in branches and seedlings of Douglas-fir had significantly lower ks than normal wood (Spicer and Gartner, 1998b). It can be hypothesized that compression wood in trunks would be more vulnerable to embolism than normal wood at high . On the other hand, it might be more resistant to severe drought because of the higher latewood resistance to embolism at low . Old growth trees also have a generally higher proportion of latewood than young or mature trees, which could limit their water transport but increase their resistance to embolism at very low . A higher latewood/earlywood ratio could be a strategy for species such as Douglas-fir growing in wet conditions during the spring and dry conditions during the summer. It could also explain why vulnerability to embolism in mature Douglas-fir trees was higher at the base of the trunk than at the top of the trunk (under the crown), whereas its ks was lower (Domec and Gartner, 2001).
Differences in water storage capacities between earlywood and latewood
The high water storage capacity observed at high (–0.5 MPa) has been described as capillary water (Tyree and Yang, 1990) and has no adaptive implication because it occurs before the plant becomes water stressed. Therefore, even though the first values of capacitance were not explained between 0 and 0.5 MPa, the other two estimated capacitance values ( = 0.5–1.0, and 1.0– 3.0 MPa) were suitable.
The research described in this paper showed that within a growth ring, latewood had a higher water storage capacity than earlywood (Fig. 5b) and was more vulnerable to embolism at field under normal conditions (>–2.0 MPa). For earlywood, the low capacity storage found for the functioning range of potentials (between 0–1 MPa) suggests that its water uptake would be related linearly to the water loss by the leaves (Table 3; Fig. 5b). The advantage of maintaining this steady-state flow is stressed by the fact that few embolism events occur at less negative than –2.0 MPa (Fig. 5a). Therefore for earlywood, the trade-off associated with low vulnerability to embolism and high ks is low water storage capacity (Goldstein et al., 1998; Stratton et al., 2000). These characteristics might be important in old trees with a higher percentage of latewood, and it can be hypothesized that for the natural range of , earlywood would best serve the tree by conducting water efficiently and safely and latewood by providing an important amount of stored water. On the other hand, under dry conditions (< –2.0 MPa), earlywood would be more likely than latewood to use water storage that could represent an important fraction, but then latewood would keep a minimum level of ks through better resistance to embolism. This hypothesis could explain why there was a bigger difference in RWC in latewood than in earlywood between winter and summer (Table 5). This hypothesis could also explain why trees with higher wood density and higher percentage latewood are related to arid areas (Polge, 1973; Megraw, 1985; Barajas-Morales, 1985) and are more resistant to cavitation (Alder et al., 1996; Hacke et al., 2001).
Trade-off between hydraulic and mechanical properties of latewood and earlywood
Latewood had a density 2.3 times higher than earlywood (Table 4), similar to other findings for the same species (Lutz, 1964; (Takjima, 1967). The overstated controlling factor for wood strength among trees is the varying latewood percentage for most species (Zobel and Van Buijtenen, 1989). Douglas-fir trees grow mostly during the springtime, when there is plenty of rain and sun to support the growth (Waring and Running, 1998). The change from earlywood to latewood is closely related to the availability of soil moisture, because a high moisture stress decreased auxin production (Gilmore et al., 1966). The regulation of cell diameter is hormonal and is mediated by an auxin originating in the buds of growing shoots. High auxin production triggers the production of earlywood (reviewed in Larson, 1994; Aloni, 2001).
For a given amount of carbon stored as sapwood, changing the growth ring latewood/earlywood ratio from 0.5 (ratio found in the trees studied) to 2, for just 1 year, would enhance the overall wood density by 34%, which would also give an increase in Young’s modulus (E or wood stiffness) in the same range (Biblis, 1969; Mott et al., 2002), because wood density and E are correlated by a factor close to 1 (Bodig and Jayne, 1982). Mechanical performance (as judged by structural stiffness) increases greatly as the sample diameter gets larger, but this change is dominated by the increase in the second moment of area (I that scales as a function of stem radius to the fourth power), which almost entirely erases the contribution of E. The key quotient is then ExI (structural stiffness) and a change in latewood/earlywood to 2 would increase ExI by only 26% (with an average growth rate of 8.6 mm year–1, Table 1), because for a given amount of wood stored, a higher latewood/earlywood ratio would also mean a narrower growth ring. On the other hand, ks would be reduced by 46%, but the overall sapwood C0.5–1.0 would be increased by 55%. Therefore, changing the proportion of latewood/earlywood for only 1 year would have more impact on hydraulic parameters than on mechanical resistance of the sapwood. The trade-off and the advantage would be that, because of an increase in capacitance, more stored water would then be available for the trees.
|
Acknowledgements |
|---|
This project was supported by USDA CSREES 97-35103-5052, and by a special USDA grant to Oregon State University for wood utilization research. The authors thank Richard Symons, Andrew Chang, and Duncan Wilson for their assistance with tree felling at McDonald Forest. We also thank Marcel Merk, Jennifer Swenson, Laurent Bouffier, and Randy Johnson for field assistance, and BJ Bond, SJ Christie, M Unsworth, G Howe, and R Leichti for corrections on the manuscript. This is paper 3533 of the Forest Research Laboratory, Oregon State University, Corvallis, OR.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Alder NN, Sperry JS, Pockman WT. 1996. Roots and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia 105, 293–301.
Aloni R. 2001. Foliar and axial aspects of vascular differentiation: hypotheses and evidence. Journal of Plant Growth Regulation 20, 22–34.
Bannan MW. 1967. Anticlinal divisions and cell length in conifers cambium. Forest Products Journal 17, 63–69.
Barajas-Morales J. 1985. Wood structural differences between trees of two tropical forests in Mexico. IAWA Journal 6, 355–364.
Biblis EJ. 1969. Transitional variation and relationships among properties within Loblolly pine growth rings. Wood Science and Technology 3, 14–24.
Bodig J, Jayne BA. 1982. Mechanics of wood and wood composites. New York, NY Van Nostrand Reinhold Company.
Bolton AJ, Petty JA. 1978. A model describing axial flow of liquids through conifer wood. Wood Science and Technology 12, 37–48.
Carlquist S. 1985. Vasicentric tracheid as a drought survival mechanism. Aliso 11, 37–68.
Cochard H, Peiffer M, Le Gall K, Granier A. 1997. Developmental control of xylem hydraulic resistances and vulnerability to embolism in Fraximus excelsior L. impacts on water relation. Journal of Experimental Botany 48, 655–663.[ISI]
Cown DJ. 1975. Variations in tracheid dimensions in the stem of a 26-year-old radiata pine tree. Appita 28, 237–245.
Crombie DS, Hipkins MF, Milburn JA. 1985. Gas penetration of pit membranes in the xylem of Rhododendron as the cause of acoustic detectable sap cavitation. Australian Journal of Plant Physiology 12, 445–453.
De Kort I. 1993. Relationship between sapwood amount, latewood percentage, moisture content and crown vitality of Douglas-fir. IAWA Journal 14, 413–427.
Domec J-C, Gartner BL. 2001. Cavitation and water storage capacity in bole xylem segments of mature and young Douglas-fir trees. Trees 15, 204–214.
Domec J-C, Gartner BL. 2002a. Age- and position-related changes in hydraulic versus mechanical dysfunction of xylem: inferring the design criteria for Douglas-fir wood structure. Tree Physiology 22, 91–104.[ISI][Medline]
Domec J-C, Gartner BL. 2002b. Effects of change in Douglas-fir bordered pit structure and functioning on tree hydraulics. Proceedings of the 2001 SAF National Convention. Denver, Co, 351–356.
Edwards WRN, Jarvis PG. 1982. Relation between water content, water potential and permeability in stems of conifers. Plant, Cell and Environment 5, 271–277.
Ellmore GS, Ewers FW. 1986. Fluid flow in the outermost xylem increment of a ring-porous tree, Ulmus americana. American Journal of Botany 73, 1771–1774.[ISI]
Ewers FW, Carlton MR, Fisher JB, Tyree MT. 1997. Vessel diameters in roots versus stems of tropical lianas and other growth forms. IAWA Journal 18, 261–279.
Fengel D. 1972. Structure and function of the membrane in softwoods bordered pits. Holzforschung 26, 1–9.
Gibson AC, HW Calkin, Nobel PS. 1985. Hydraulic conductance and xylem structure in tracheid-bearing plants. IAWA Bulletin 6, 293–302.
Gilmore AR, Boyce SG, Ryker RA. 1966. The relationship of specific gravity of loblolly pine to environmental factors in southern Illinois. Forest Science 12, 399–405.
Goldstein G, Andrade JL, Meinzer FC, Holbrook NM, Cavelier J, Jackson P, Celis A. 1998. Stem water storage and diurnal patterns of water use in tropical forest canopy trees. Plant, Cell and Environment 21, 397–406.
Gregory SG, Petty JA. 1973. Valve action of bordered pits in conifers. Journal of Experimental Botany 24, 763–767.
Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA. 2001. Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126, 457–461.
Hargrave KR, Kolb KJ, Ewers FW, Davis SD. 1994. Conduit diameter and drought-induced embolism in Salvia mellifera Green (Labiatae). New Phytologist 126, 695–705.[ISI]
Holbrook NM. 1995. Stem water storage. In: Gartner BL, ed. Plant stems: physiology and functional morphology. San Diego: Academic Press, 105–124.
Kellog RM, Sastry CBR, Wellwood RW. 1975. Relation between cell wall composition and cell wall density. Wood Fiber 7, 170–177.
Kennedy RW. 1961. Variation and periodicity of summerwood in some second-growth Douglas-fir. Tappi Journal 44, 161–165.
Kennedy RW, Warren WG. 1969. Within-tree variation in physical and chemical properties of Douglas-fir. In: Second World Consultation on Forestry Tree Breeding, Vol. 1. Washington, DC: International Union of Forest Research Organization, 393–417.
Larson PR. 1962. A biological approach to wood quality. Tappi Journal 45, 443–448.
Larson PR. 1994. The vascular cambium: development and structure. New York: Springer-Verlag.
Lebourgeois F. 2000. Climatic signals in earlywood and total ring width of Corsican pine from western France. Annals of Forest Science 57, 155–164.
Lo Gullo MA, Salleo S, Piaceri EC, Rosso R. 1995. Relations between vulnerability to xylem embolism and xylem conduit dimensions in young trees of Quercus cerris. Plant, Cell and Environment 18, 661–670.
Lutz J. 1964. How growth rate affects properties of softwood veneer. Forest Products Journal 24, 94–102.
Megraw RA. 1985. Wood quality factors in loblolly pine. Atlanta, Georgia: TAPPI Press.
Matzner SL, Rice KJ, Richards JH. 2001. Intra-specific variations in xylem cavitation in interior live oak (Quercus wislizenii A. DC.). Journal of Experimental Botany 52, 783–789.
McMillan CW. 1968. Morphological characteristics of loblolly pine wood as related to specific gravity, growth rate and distance from pith. Wood Science and Technology 2, 166–176.
Mott L, Les G, Shaler S. 2002. Mechanical properties of individual southern pines fibers. Part II. Comparison of earlywood and latewood fibers with respect to height and juvenility. Wood and Fiber Science 34, 212–220.
Panshin AJ, de Zeeuw C. 1980. Textbook of wood technology, 4th edn. New York: McGraw-Hill.
Park S. 1984. Structure of ‘opposite wood’. II. Variability in the diameter and wall thickness of the tracheid, ring width, and late-wood percentage. Mokuzai Gakkaishi 30, 110–116.
Petty TA. 1972. The aspiration of bordered pits in conifer wood. Proceedings of the Royal Society, Series B 181, 395–406.
Petty JA, Puritch GS. 1970. the effects of drying on the structure and permeability of the wood Abies grandis. Wood Science and Technology 4, 140–154.
Pockman WT, Sperry JS. 2000. Vulnerability of xylem cavitation and the distribution of Sonoran desert vegetation. American Journal of Botany 87, 1287–1299.
Polge H. 1973. Facteurs écologiques et qualité du bois. Annals of Forest Science 30, 307–328.
Rasband W. 1996. NIH Image. Version 1.60. National Institutes of Health, Bethesda, MD.
Richter H. 1976. The water status in the plant—experimental evidence. In: Lange OL, Kappen, Schulze ED, eds. Water and plant life. Berlin: Springer, 42–58.
Salleo S, Hinckley TM, Kikuta SB, Lo Gullo MA, Weilgony P, Yoonand TM, Richter H. 1992. A method for inducing xylem emboli in situ: experiments with a field-grow tree. Plant, Cell and Environment 15, 491–497.
SAS Institute Inc. 1997. SAS software release 6.12. SAS Institute Inc.: Cary, NC.
Schulte PJ, Gibson AC. 1988. Hydraulic conductance and tracheid anatomy in six species of extant seed plants. Canadian Journal of Botany 66, 1073–1079.
Siau JF. 1984. Transport processes in wood. Berlin: Springer-Verlag.
Sperry JS, Saliendra NZ. 1994. Intra-and inter-plant variation in xylem cavitation in Betula occidentalis. Plant, Cell and Environment 17, 1233–1241.
Sperry JS, Tyree MT. 1988. Mechanism of water stress-induced xylem embolism. Plant Physiology 88, 581–587.
Sperry JS, Tyree MT. 1990. Water stress-induced xylem embolism in three species of conifers. Plant, Cell and Environment 13, 427–436.
Spicer R, Gartner BL. 1998a. How does a gymnosperm branch assume the hydraulic status of a main stem when it takes over a leader? Plant, Cell and Environment 21, 1063–1070.
Spicer R, Gartner BL. 1998b. Hydraulic properties of Douglas-fir (Pseudotsuga menziesii) branches and branch halves with reference to compression wood. Tree Physiology 18, 777–784.[ISI][Medline]
Stratton L, Goldstein G, Meinzer FC. 2000. Stem water storage capacity and efficiency of water transport: their functional significance in a Hawaiian dry forest. Plant, Cell and Environment 23, 99–106
Takjima T. 1967. Tree growth and wood properties. Tokyo: Faculty of Agriculture of Tokyo University.
Timell TE. 1986. Compression wood in gymnosperms, Vol. 1. Berlin: Springer-Verlag.
Tyree MT, Davis ST, Cochard H. 1994. Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? IAWA Journal 15, 335–360
Tyree MT, Ewers FW. 1991. Tansley Review No. 34. The hydraulic architecture of trees and other woody plants. New Phytologist 119, 345–360.[ISI]
Tyree MT, Sperry JS. 1988. Do woody plants operate near the point of catastrophic xylem dysfunction caused by dynamic water stress: answer from a model. Plant Physiology 88, 574–580.
Tyree MT, Yang S. 1990. Water storage capacity of Thuja, Tsuga, and Acer stems measured by dehydration isotherms. Planta 182, 420–426.
Waring RH, Running SW. 1998. Ecosystems analysis at a multiple scale. San Diego Press.
Westing AH. 1968. Formation and function of compression wood in gymnosperms. II. Botanical Review 34, 51–78.
Yoshizawa N, Kiyomiya M, Idei T. 1987. Variations in tracheid length and morphological changes in tracheid tips associated with the development of compression wood. Wood Science and Technology 21, 1–10.
Zimmermann MH. 1983. Xylem structure and the ascent of sap. Berlin: Springer-Verlag.
Zobel BH, Van Buijtenen JP. 1989. Variation among and within trees. In: Wood variation: its causes and control. New York: Springer-Verlag.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. Nadler, E. Raveh, U. Yermiyahu, M. Lado, A. Nasser, M. Barak, and S. Green Detecting Water Stress in Trees Using Stem Electrical Conductivity Measurements Soil Sci. Soc. Am. J., June 18, 2008; 72(4): 1014 - 1024. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J.-C. Domec, B. Lachenbruch, and F. C. Meinzer Bordered pit structure and function determine spatial patterns of air-seeding thresholds in xylem of Douglas-fir (Pseudotsuga menziesii; Pinaceae) trees Am. J. Botany, November 1, 2006; 93(11): 1588 - 1600. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. S. Sperry, U. G. Hacke, and J. Pittermann Size and function in conifer tracheids and angiosperm vessels Am. J. Botany, October 1, 2006; 93(10): 1490 - 1500. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. M. Chapotin, J. H. Razanameharizaka, and N. M. Holbrook A biomechanical perspective on the role of large stem volume and high water content in baobab trees (Adansonia spp.; Bombacaceae) Am. J. Botany, September 1, 2006; 93(9): 1251 - 1264. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Pittermann, J. S. Sperry, U. G. Hacke, J. K. Wheeler, and E. H. Sikkema Inter-tracheid pitting and the hydraulic efficiency of conifer wood: the role of tracheid allometry and cavitation protection Am. J. Botany, September 1, 2006; 93(9): 1265 - 1273. [Abstract] [Full Text] [PDF] |