Tree Physiology 24, 745752 2004 Heron PublishingVictoria, Canada

Size dependency of photosynthetic water- and nitrogen-use efficiency and hydraulic limitation in Acer mono
ERI NABESHIMA1,2 and TSUTOM HIURA1
1 2

Tomakomai Research Station, Field Science Center for Northern Biosphere, Hokkaido University, Tomakomai, 053-0035, Japan Corresponding author (enabe@exfor.agr.hokudai.ac.jp)

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Received April 28, 2003; accepted January 2, 2004; published online May 3, 2004

Summary We examined open-grown Acer mono Maxim. trees of different sizes to test the hypotheses that (1) hydraulic limitation increases with tree size, thereby reducing photosynthesis, and (2) photosynthetic water- and nitrogen-use efficiencies change with tree size. Maximum net assimilation rate per unit dry mass was significantly lower in large trees than in small trees, whereas leaf nitrogen concentration increased with tree size. As a consequence, photosynthetic nitrogen-use efficiency decreased with increase in tree size. Photosynthetic water-use efficiency, however, increased with tree size, partly as a result of reduced stomatal conductance. Neither root-to-leaf hydraulic conductance nor minimum leaf water potential changed with tree size. Keywords: homeostasis in water status, hydraulic conductance, leaf water potential, nitrogen content, stomatal conductance.

Introduction Functional constraints require that, as an organism increases in size, changes occur in both the relative size of its components and the relative rates of its physiological processes (Brown et al. 2000). Recent studies suggest that, during transpiration, tall trees experience greater hydraulic stress than shorter trees (Ryan and Yoder 1997, West et al. 1997). The hydraulic limitation (HL) hypothesis (Ryan and Yoder 1997) states that the total resistance of the hydraulic pathway increases as trees increase in size. However, other studies suggest that tall trees adjust to increased hydraulic stress by homeostatic processes, such as reducing the leaf area to conducting stem ratio or increasing fine root production (Magnani et al. 2000, McDowell et al. 2002, Mencuccini 2002). The HL hypothesis predicts that increases in hydraulic resistance with increases in tree size reduce sap flow, which in turn limits stomatal conductance (G) and photosynthesis. On the other hand, homeostatic mechanisms that counter the increase in hydraulic stress with increased tree size have carbon costs such as a reduction in leaf area to conducting stem ratio or an increase in fine root production. Therefore, increases in hydraulic stress with increasing tree size are likely, either directly or indirectly, to affect plant productivity.

Several studies emphasize the generality and importance of age-related declines in the photosynthetic productivity of trees (Ryan et al. 1997, Bond 2000, Thomas and Winner 2002, Niinemets 2002), although it is unclear what causes these declines. According to the HL hypothesis, the increase in hydraulic resistance decreases G. Reducing whole-plant hydraulic conductance by notching (Sperry and Pockman 1993), injecting air into xylem conduits (Sperry et al. 1993), or root pruning (Teskey et al. 1983) results in immediate stomatal closure. However, studies on age- or size-related changes in total hydraulic conductance per unit leaf area (KL) have not yielded consistent results (e.g., West et al. 1999, Mencuccini 2002). It thus remains unclear to what extent an increase in tree size decreases hydraulic conductance, and to what extent this impacts G and hence limits photosynthesis. If changes in KL with tree size limit water availability for photosynthesis, photosynthetic water-use efficiency (WUE) should change with tree size. However, an increase in the use efficiency of one resource can lead to a reduction in the use efficiency of other resources. For example, Hirose and Bazzaz (1998) suggested that a trade-off between light- and nitrogen-use efficiency (NUE) exists in canopy photosynthesis. Nitrogen (N) is generally a limiting factor for photosynthetic capacity because a large amount of N is invested in photosynthetic enzymes (Evans 1989). But if the supply of water, not N, decreases as trees grow, photosynthetic WUE should increase as photosynthetic NUE decreases. We used open-grown Acer mono Maxim. trees of different size classes (canopy trees, small trees and saplings) to test the following hypotheses: (1) photosynthetic WUE increases, whereas NUE decreases with increasing tree size; (2) photosynthetic capacity or in situ diurnal photosynthesis decreases with tree size; and (3) hydraulic conductance from soil to leaf decreases with increasing tree size, leading to decreases in G and photosynthesis.

Materials and methods Study site, plant materials and canopy access We studied a deciduous broad-leaved forest stand in the Tomakomai Experimental Forest (TOEF, 4240 N, 14136 E). An-

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nual precipitation at TOEF is 1304 mm, most of which occurs in summer, and the summer mean temperature is 18 C. The dominant species are Acer mono, Acer palmatum Thunb. var. amoenum Ohwi, Cercidiphyllum japonicum Siebold & Zucc., Ostrya japonica Sarg., Prunus ssiori Friedr. Schmidt and Quercus crispula Blume (Hiura et al. 1998). The study species, A. mono, is a shade-tolerant late-successional species (Koike 1988), which regenerates successfully in a wide range of deciduous forest types (Ishizuka and Sugawara 1989, Seiwa and Kikuzawa 1996). Saplings are generally more abundant under closed canopies than in gaps (Abe et al. 1995). Reproductive onset starts from 3 cm in DBH (Koike et al. 1992). The estimated asymptotic height of A. mono in TOEF is about 23 m (height = 23.04(1 exp (0.114DBH 0.748)); r 2 = 0.99; Equation 2 in Thomas 1996). We selected canopy trees of A. mono at the canopy crane site in TOEF. The canopy crane, which is 25 m tall with a 41.5 m jib, can access 183 trees (DBH > 10 cm) of 21 species. The canopy crane site is located in a mature forest stand and A. mono trees at this site had reached their maximum height. Because this forest is mature with a disturbance regime of gap dynamics (Hiura et al. 1998), we can access various sizes of A. mono from the canopy crane. We selected three canopy trees that were close to the maximum height (2022.5 m tall, at 4770 cm DBH) and four intermediate trees that were less than the maximum height, but in full sunlight in canopy gaps (1418.5 m tall, 1731 cm DBH). Because A. mono saplings are seldom observed in the forest understory, or in forest gaps, we selected saplings (1.52 m tall, DBH < 1 cm) from an open site 500 m from the canopy crane site. The open site (approximately 10 ha) was clear-cut in 1981. The soil at both the canopy crane site and the open site was derived from the deep volcanic deposits of Mt. Tarumae (Igarashi 1987). Soil volumetric water content was not significantly different between the sites. Measurements Gas exchange was measured in August and September 2002. To determine the photosynthetic capacity of each tree, we measured maximum net assimilation rate (Aarea ), stomatal conductance to water vapor (Garea ) and transpiration rate (Earea ) in saturating light (1000 mol m 2 s 1) with a portable gas exchange system (Li-6400, Li-Cor, Lincoln, NE) equipped with an LED light source. Light curves verified that saturating photosynthetic photon flux (PPF) was supplied (Shimizu et al., Hokkaido University, Japan, unpublished data). Measurements were conducted between 0700 and 1100 h when the leaf-to-air saturation deficit (VPD) was small (< 1 kPa). During measurements, cuvette air temperature was 20 C (20 1.5 C), CO2 concentration was 370 mol mol 1 and air flow was 500 mol s 1. We selected three canopy leaves from each canopy and intermediate tree, and one leaf from each sapling tree. Leaf mass per area (LMA) and mass-based leaf N concentration (Nmass ) were calculated for each leaf. Dry mass was determined after oven-drying at 60 C for more than 3 days, and N concentration was determined with a C/N analyzer (SUMITOMO NC-900, Osaka, Japan).

To determine the response of leaf gas exchange to VPD, we conducted diurnal measurements of net assimilation rate (in situ Aarea ), stomatal conductance to water vapor (in situ Garea ) and transpiration rate (in situ Earea ) at PPF > 1000 mol m 2 s 1 with the LI-6400 portable gas exchange system. We began each set of measurements at about 0700 h and measured gas exchange hourly until about 1600 h, unless cloudy conditions prevailed. Measurements for canopy and intermediate trees were made on August 16 and 26 and September 8 and 9, and the measurements for saplings were made on September 11. On each measurement day, we selected three trees, a combination of one to two trees each from the canopy and intermediate classes. For each tree, one to three leaves were selected and measured hourly under cuvette conditions of 370 mol mol 1 CO2 concentration and 500 mol s 1 flow rate. To estimate leaf-specific hydraulic conductance of the flow path from soil to leaf (K L ), we determined leaf water potential (leaf) and transpiration rate on a leaf area basis (E; mmol m 2 s 1) in the summer of 2003 (from mid-July to August). Leaf-specific hydraulic conductance from soil to leaf was calculated as: KL = F soil hg leaf (1)

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where F is leaf-area specific liquid water flux within the xylem transport system, soil is soil water potential and hg is the gravitational pull on a column of water of height h and density . Under steady-state conditions, F is identical to E. Soil water potential, minus hg, can be assumed to approximate predawn leaf water potential (predawn): predawn = soil hg Thus, KL can be estimated as: KL = E predawn leaf (3) (2)

We measured G with steady-state porometers (LI-1600, Li-Cor) to determine E (Ishida et al. 1992). The LI-1600 porometer maintains a steady state humidity in the chamber similar to the ambient humidity. All G values were recalculated based on the flow rate of dry air and leaf temperature obtained with an infrared thermometer (IR-TE, Chino, Tokyo, Japan). Air temperature and relative humidity were measured with temperature and humidity sensors connected to a data logger (RTR-53L/53, T&D, Matsumoto, Japan) installed at each measurement point. Air temperature and relative humidity were recorded at 5-min intervals. Transpiration rate was calculated as: GG b E = W G + Gb (4)

where W is the absolute leaf-to-air vapor pressure difference divided by the atmospheric pressure and Gb is the boundary

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where u is wind speed (m s 1), d is leaf length (m), Tleaf is leaf temperature and P is atmospheric pressure (kPa). Wind speeds were measured with an anemometer (Wind Messe561, Empex, Tokyo, Japan). Leaf lengths for each tree were determined by measuring 20 leaves per tree. We measured leaf and predawn with a pressure chamber (Model 1003, PMS Instrument, Corvallis, OR). Immediately after measurement of G, the twigs were cut just below the current-year shoot and used to determine leaf. In addition to predawn, leaf and G were concurrently measured at mid-morning (0730 to 1030 h), noon (1030 to 1230 h) and afternoon (1230 to 1500 h), permitting multiple determinations of KL (Meinzer et al. 1999). We measured KL of each tree throughout an entire day (July 14 and August 5 for the canopy class; July 28 and 31 and August 6 for the intermediate class). Saplings were each measured throughout two days because of a change in weather conditions (August 13 and 17). For each measurement, predawn was determined. Data analysis We calculated maximum net assimilation rate per unit leaf dry mass (Amass ), photosynthetic NUE, photosynthetic WUE and leaf nitrogen concentration per unit leaf area (Narea ) for each tree as follows: A mass = A area / LMA NUE = A mass / N mass
Figure 1. Relationships between tree diameter at breast height (DBH) and (a) maximum net assimilation rate per unit dry mass and (b) maximum net assimilation rate per unit leaf area. Bars indicate standard errors (n = 3, sapling measurements have no SE bars because n = 1). See Table 1 for regression coefficients and r values.

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(6) (7) (8) (9)

WUE = A area / G area N area = N mass LMA

layer conductance, which was estimated as (Pearcy et al. 1989, Jones 1992, Ishida et al. 1996):
0. 5 273 P 3 u G b = 0.446 0.715 10 d Tleaf + 273 101.3

(5)

Values of Amass, Aarea, Garea, NUE, WUE, Nmass, Narea and prefor each leaf measurement were averaged for each tree. For each leaf, time course measurements of E and leaf (mid-morning, noon and afternoon) were averaged for each time. Values of KL were determined with the values of E, leaf and predawn, according to Equation 3 and then the KL values were averaged for each tree. Minimum leaf (minleaf ) and maximum E (Emax ) during a time course measurement were
dawn

Table 1. Regression coefficients of leaf physiological and structural parameters on tree diameter at breast height (DBH) (linear regressions for all parameters except leaf mass per area (LMA); log-linear regression for LMA). Statistical analysis: * = P < 0.05; ** = P < 0.01; and *** = P < 0.001. Parameter Maximum net assimilation rate per unit dry mass (Amass; nmol g 1 s1) Leaf nitrogen content (Nmass; mg g 1) Leaf nitrogen content (Narea; g m 2) Nitrogen-use efficiency (NUE; mol CO2 g 1 N s 1) Water-use efficiency (WUE; mol CO2 mmol 1 H2O) Stomatal conductance (Gmass; mol g 1 s 1) Stomatal conductance (Garea; mmol m 2 s 1) Leaf mass per area (LMA; g m 2) Leaf internal CO2 concentration (Ci; mol mol 1) Slope 1.479 0.041 0.020 0.071 0.235 0.063 0.002 23.359 0.379 Intercept 191.24 23.22 1.53 8.25 34.40 5.76 0.36 60.96 291.73 r 0.908 *** 0.642 * 0.851 ** 0.887 ** 0.733 * 0.801 ** 0.643 * 0.993 *** 0.693 *

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Figure 2. Relationships between tree diameter at breast height (DBH) and (a) nitrogen-use efficiency and (b) water-use efficiency. Bars indicate standard errors (n = 3, sapling measurements have no SE bars because n = 1). See Table 1 for regression coefficients and r values.

determined for each tree. The validation of minleaf was confirmed (E. Nabeshima and T. Hiura, unpublished data) by pressurevolume (PV ) measurements (Tyree and Hammel 1972, Maruyama and Morikawa 1983). To test our hypothesis, we performed linear regression analyses for Amass, Aarea, Garea, Gmass, NUE, WUE, Nmass, Narea, KL, minleaf, Emax and predawn against tree DBH and a log-linear regression analysis for LMA. From leaf measurements, we examined size-dependency of in situ gas exchange responses (Aarea, Amass, Garea, Earea, NUE, WUE) against VPD by multiple regression analysis. Vapor pressure deficit was not significantly dependent on DBH (linear regression analysis, P = 0.073, r = 0.188).

Figure 3. Relationships between tree diameter at breast height (DBH) and (a) leaf mass per area, (b) maximum stomatal conductance per unit leaf area and (c) area-based leaf nitrogen concentration. Bars indicate standard errors (n = 3, sapling measurements have no SE bars because n = 1). See Table 1 for regression coefficients and r values.

Results Light-saturated photosynthetic parameters and leaf traits Maximum net assimilation rates per unit leaf dry mass were significantly lower in large trees than in small trees (Figure 1a, Table 1). In addition, with increasing DBH, NUE significantly decreased and WUE significantly increased (Figure 2, Ta-

ble 1). Leaf Nmass and Narea both increased with increasing tree size (Figure 3c, Table 1); however, Aarea was not significantly correlated with DBH (Figure 1b, P = 0.678). On the other hand, both Garea and Gmass decreased significantly with increasing tree size (Figure 3b, Table 1). Similarly, leaf internal CO2 concentration (Ci ) decreased significantly with increasing DBH (Table 1). Leaf mass per area increased significantly with increasing tree size (Figure 3a, Table 1).

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Figure 4. Relationships between tree diameter at breast height (DBH) and (a) leaf-specific hydraulic conductance (KL ) and (b) predawn ( ) and minimum ( ) leaf water potential. Bars indicate standard errors ((a) during time course, n = 3 to 4; (b) n = 3, but for saplings: n = 2 (minimum leaf water potential) and n = 4 (predawn leaf water potential)). Figure 5. Relationships between vapor pressure deficit (VPD) and diameter at breast height (DBH) with (a) in situ net assimilation rate per unit dry mass and (b) in situ net assimilation rate per unit leaf area. See Table 2 for regression coefficients and r 2 values.

Soil-to-leaf hydraulic conductance and leaf water potential Soil-to-leaf hydraulic conductance per unit leaf area was not significantly correlated with tree size (Figure 4a, P = 0.843). Although predawn significantly decreased with increasing tree size (Figure 4b, P < 0.001), minleaf was not significantly correlated with DBH (Figure 4b, P = 0.868). Maximum transpiration rate decreased significantly with DBH (P = 0.044). Responses of in situ photosynthetic parameters to VPD Values of Amass and Aarea (Figure 5), measured in situ, significantly decreased with increasing VPD and increasing DBH. Similarly, values of Garea and Earea (Figure 6), measured in situ, significantly decreased with increasing VPD and increasing DBH. Multiple regression parameters for these relations are in Table 2. Values of NUE based on in situ measurements significantly decreased with increasing VPD, whereas the corresponding WUE values were not significantly correlated with VPD (Table 2). With increasing size, WUE and NUE calculated from in

situ measurements significantly increased and decreased, respectively (Table 2).

Discussion Thomas and Winner (2002) conducted a meta-analysis comparing the gas exchange characteristics of saplings and adult trees and found that photosynthetic capacity, when expressed on a leaf mass basis, tends to be higher in saplings than in adult trees, but when expressed on a leaf area basis, tends to increase from saplings to mature trees. We found tree-size-dependent declines in mass-based photosynthetic capacity in A. mono (Figure 1). Leaf N content was strongly correlated with photosynthesis (Evans 1989). However, in our study, Nmass increased slightly with increasing tree size, indicating that the decrease

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Figure 6. Relationships between vapor pressure deficit (VPD) and diameter at breast height (DBH) with (a) in situ stomatal conductance (in situ Garea ) and (b) in situ transpiration rate (in situ Earea ). See Table 2 for regression coefficients and r 2 values of (a) and (b).

in mass-based photosynthetic capacity was not the result of N limitation. As tree size increased, photosynthetic NUE decreased and WUE increased (Figure 2). A reduction in G and an increase in Narea contributed to this change (Figure 3). When stomata open to allow CO2 diffusion into the leaf, water is lost in transpiration. Wright et al. (2003) theoretically illustrate the use of water through transpiration and nitrogen (Narea ) in photosynthesis as a two-input production process (Aarea NareaGs ). They presented field data showing that species in low rainfall habitats have higher leaf Narea, which permits lower G for a given photosynthetic rate and thus restraint of transpirational water use. Likewise, our observations of a tree-size-related in-

crease in WUE and decrease in NUE without a significant change in Aarea suggest that, unlike N availability, water availability to leaves decreased with increasing tree size. Hubbard et al. (1999) tested the HL hypothesis for old (about 250 years old and 30 m tall) and young (about 40 years old and 10 m tall) Pinus ponderosa Dougl. ex Laws. trees. They found that: (1) hydraulic conductance was 44% lower in the old trees than in the young trees; (2) leaf N content and photosynthetic capacity were similar between the young and old trees; and (3) G and assimilation declined more steeply with air saturation deficit in the old trees than in the young trees. In contrast, we observed that photosynthesis (Figure 5) and G (Figure 6a) decreased with VPD and increasing tree size (see also Table 2); however, Narea increased (Figure 3c) and Amass decreased (Figure 1a) with increasing tree size. The decrease in photosynthesis with increasing tree size in our study may be explained, in part, by the size-related decline in G, which reduced the CO2 supply to the leaf intercellular spaces. It has been suggested that the increase in LMA also contributes to the size-related decline in photosynthesis (Niinemets 2002). It is well known that LMA increases from the bottom to the top of the canopy. A recent study has suggested that SLA, the reciprocal of LMA, decreases as the gravitational component of the water potential falls (Marshall and Monserud 2003). These authors found that SLA decreased with branch height rather than with light availability, which was inferred from branch position relative to the rest of the canopy. Increases in LMA involve an accumulation of both support and assimilative compounds, and may therefore partly counterbalance the decreases in Amass (Aarea = Amass LMA) (Thomas and Winner 2002). This may explain our finding that mass-based photosynthetic capacity decreased with increasing tree size, whereas area-based photosynthetic capacity did not (Figure 1). Therefore, both the decrease in G and the increase in LMA with increasing tree size may have contributed to the size-related decline in photosynthesis that we observed. Our observation that KL did not decrease with increasing tree size in A. mono (Figure 4) is inconsistent with the result of Hubbard et al. (1999). Mencuccini and Magnani (2000) suggested that some compensation is needed if one postulates that homeostasis in KL is maintained during growth. For example, both a reduction in the ratio of leaf area to sapwood area (McDowell et al. 2002, Mencuccini 2002) and an increase in allocation to fine roots (Magnani et al. 2000) compensate for the increased hydraulic resistance aboveground by increasing the hydraulic conductance belowground. Recent studies have suggested that trees partially compensate for the increase in hydraulic resistance that accompanies increases in height by making structural changes (Magnani et al. 2000, McDowell et al. 2002, Mencuccini 2002). The advantage of such structural changes within a life cycle have seldom been tested, although such testing is important because compensation might involve costs such as reduced primary production (Magnani et al. 2000, Mencuccini and Magnani 2000). Although KL did not decrease with increasing tree size, we found that G did (cf. Figures 3 and 4). Does the finding that G decreased without a decrease in KL support the HL hypothesis?

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Table 2. Multiple regression analyses for in situ photosynthetic parameters. Abbreviations: VPD = vapor pressure deficit; DBH = diameter at breast height; Coefficient = partial regression coefficient; and Std coeff. = standardized partial regression coefficient. Variable Coefficient SE Std coeff. P Whole model F Area-based net assimilation rate (mol m VPD 5.218 DBH 0.023 Constant 20.365
2

r2 0.747

P < 0.001

s ) 0.322 0.01 0.822

0.879 0.129 0.000 0.811 0.268 0.000 0.852 0.327 0.000 0.262 0.387 0.000 0.136 0.355 0.000 0.81 0.365 0.000

< 0.001 0.019

131.369

Mass-based net assimilation rate (nmol g 1 s 1) VPD 51.447 4.065 DBH 0.515 0.123 Constant 218.308 10.374 Stomatal conductance (mmol m 2 s 1) VPD 0.076 DBH 0.001 Constant 0.305 Transpiration rate (mmol m 2 s 1) VPD 0.259 DBH 0.012 Constant 3.051 0.005 0 0.013 0.097 0.003 0.247

< 0.001 < 0.001

81.795

0.648

< 0.001

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< 0.001 < 0.001

119.426

0.729

< 0.001

0.009 < 0.001

9.800

0.180

< 0.001

Water-use efficiency (mol CO2 mmol 1 H2O) VPD 3.230 2.353 DBH 0.257 0.071 Constant 73.788 6.005 Nitrogen-use efficiency (mol CO2 g 1 N s 1) VPD 2.109 0.159 DBH 0.029 0.005 Constant 9.204 0.406

0.173 0.001

8.643

0.163

< 0.001

< 0.001 < 0.001

94.075

0.679

< 0.001

It has been suggested that trees regulate G in a way that prevents catastrophic xylem cavitation (Tyree and Ewers 1991, Sperry 1995, Bond and Kavanagh 1999). Sperry (1995) showed that, in the field, the vulnerability of stem xylem to cavitation by water stress correlates with the minimum xylem pressures. Futhermore, it has been shown that plants that develop less negative pressures have a narrow range of midday leaf water potential (for example, the range is between 1.0 and 1.4 MPa in Betula occidentalis Hook.; Saliendra et al. 1995, Sperry 1995). We found that, as tree size increased, minleaf remained in a narrow range (between 0.8 and 1.25 MPa) and predawn and minimum transpiration rate decreased. Therefore, the decrease in G sufficient as to prevent xylem cavitation. The dependency of physiological parameters on size has rarely been explored in plants (Mencuccini 2002). A knowledge of whether physiological parameters decline, remain constant or increase in response to increases in size would help identify the critical factors associated with changes in plant size. We found that photosynthetic WUE increased and G decreased with increasing size in A. mono, indicating that the supply of water to canopy leaves decreases with increasing size. On the other hand, KL and minleaf varied little with tree size, suggesting homeostasis in water status from root to leaf. Our results only partly support the HL hypothesis, but also indicate an adjustment for homeostasis in water transport. We

conclude that size-dependent changes in leaf photosynthetic rate of A. mono accompanied hydraulic limitation in the broad sense; that is, G decreased in such a manner as to maintain leaf constant, but there was no decline in hydraulic conductance.
Acknowledgments We thank K. Hikosaka, Y. Maruyama, T. Saito, A. Ishida, T. Kobayashi, T. Koike, T. Kitahashi, R. Funada, Y. Sano and Y. Fukushima for their valuable comments during this study. This work was partly supported by grants from the Ministry of Education, Science, Sports and Culture of Japan (09NP1501, 11213204, 13304060, 15208014 to T.H.). References Abe, S., T. Masaki and T. Nakashizuka. 1995. Factors influencing sapling composition in canopy gaps of a temperate deciduous forest. Vegetatio 120:2132. Bond, B.J. 2000. Age-related changes in photosynthesis of woody plants. Trends Plant Sci. 5:349353. Bond, B.J. and K.L. Kavanagh. 1999. Stomatal behavior of four woody species in relation to leaf-specific hydraulic conductance and threshold water potential. Tree Physiol. 19:503510. Brown, J.H., G.B. West and B.J. Enquist. 2000. Scaling in biology: patterns and processes, causes and consequences. In Scaling in Biology. Eds. J.H. Brown and G.B. West. Oxford University Press, Oxford, pp 167198.

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TREE PHYSIOLOGY VOLUME 24, 2004