Quercus Robur): the Impact of Crown and Hydraulic Architecture

Reduced photosynthesis in old oak (Quercus robur): the impact of crown and hydraulic architecture

STEFFEN RUST1,2 and ANDREAS ROLOFF1 1 Technische Universität Dresden, Institut für Forstbotanik und Forstzoologie, Postfach 10, D-01735 Tharandt, Germany 2 Author to whom correspondence should be addressed ([email protected]) Downloaded from https://academic.oup.com/treephys/article/22/8/597/1648401 by guest on 30 September 2021

Received February 26, 2001; accepted November 2, 2001; published online May 1, 2002

Summary We tested the hypothesis that changes in crown ground, the largest hydraulic resistance along this pathway re- architecture of old pedunculate oak trees (Quercus robur L. sides in the smallest shoots of the crown (Yang and Tyree ssp. robur Kl. et Kr. et Rol.) reduce leaf specific hydraulic con- 1993). In old and declining trees, the smallest shoots are char- ductance of shoots, thereby limiting stomatal conductance and acterized by short internodes and a high frequency of nodes, assimilation of affected shoots. At the end of summer 1999, hy- and a decrease in shoot growth increment in these shoots is the draulic conductance and leaf specific hydraulic conductance, first sign of reduced vigor (Roloff 1993). The formation of measured with a high-pressure flow meter in 0.5- to 1.5-m long short shoot internodes reduces leaf specific conductance of shoots, were 27 and 39% lower, respectively, in shoots of low these shoots (Rust and Hüttl 1999). Tausend et al. (2000) ob- vigor compared with vigorously growing shoots in a 165-year- served a pronounced impact of differences in crown architec- old stand in southeastern Germany. Two types of bottlenecks ture on gas exchange. Therefore, in addition to path length, to water transport can be identified in shoots of old oak trees, developmental changes in crown architecture may also influ- namely nodes and abscission zones. The reduction in hydraulic ence whole-plant conductance (Becker et al. 2000). conductance was especially severe in shoots with diameters of In pedunculate oak, the architecture of the crown is strongly less than 2 mm. Maximum stomatal conductance and maxi- influenced by the age and vigor of the tree (Roloff 1993, mum net assimilation rate increased significantly with hydrau- Sonesson 1999, Rust et al. 2000). In vigorous trees, the periph- lic conductance and leaf specific hydraulic conductance. Our eral crown consists of a dense network of long shoots. De- data support the hypothesis that changes in shoot and conse- creasing vigor results in reduced shoot growth increments and quently crown architecture observed in aging trees can limit a characteristic modification of the branching pattern. Even- photosynthesis by reducing shoot hydraulic conductance. tually, the declining crown can be described as consisting of Thus, in addition to increasing pathway length and lower con- brush-like leaf clusters. In old oak trees (more than 80– ductivity of xylem in old trees, structural changes in shoot and 100 years old), cladoptosis (the active shedding of shoots) crown architecture need to be considered when analyzing wa- seems to be the main mechanism responsible for the transfor- ter relations and photosynthesis in mature and declining trees. mation of crown architecture. It is enabled by a special abscission zone formed at branch junctions. These abscission Keywords: assimilation, hydraulic conductance, hydraulic zones, which are characterized by small conduits (Rust et al. limitation, stomatal conductance. 2000), may have an even larger impact on hydraulic conductance than the high frequency of nodes. Our hypothesis was that modifications in crown architec- Introduction ture of old oak trees reduce leaf specific hydraulic conduc- As trees age, height growth and wood production decline. The tance of shoots, thereby limiting stomatal conductance and hydraulic limitation hypothesis attributes this reduction in assimilation of affected shoots. To test the hypothesis, we in- productivity to hydraulic limitation of photosynthesis caused vestigated gas exchange and hydraulic conductance of shoots by increased resistance in the vascular systems of old trees differing in vigor. (Yoder et al. 1994, Ryan and Yoder 1997, Hubbard et al. 1999). Yoder et al. (1994) postulated that increasing path length and the reduction in hydraulic conductance of the con- Materials and methods ducting tissue limit stomatal conductance in large old trees. There is substantial experimental evidence that stomatal Field site and plant material conductance is positively correlated with hydraulic conduc- In August 1999, we conducted experiments on Quercus ro- tance of the soil–root–leaf pathway in a wide range of plant bur L. ssp. robur Kl. et Kr. et Rol. trees growing in a stand species (Meinzer and Grantz 1990, Sperry and Pockman 1993, planted in 1835. The site was located near Dresden, south- Bond and Kavanagh 1999, Meinzer et al. 1999). Above eastern Germany at 124 m a.s.l. 598 RUST AND ROLOFF

Thirty-five shoots were selected from four trees to cover a Results range of shoot structures. The investigated branches were Shoot leaf area was not correlated with vigor class but in- classified on the basis of vigor classes (VC) as: VC 0 = mean –1 creased significantly with basal diameter. Mean leaf area of shoot increment over the last 3 years exceeds 20 cm year ; the shoots was 0.17 ± 0.05 m2. VC 1 = mean shoot increment over the last 3 years does not ex- Shoots of VC 0 and 1 (most vigorous shoots) had signifi- ceed 15 cm year–1; VC 2 = mean shoot increment over the last –1 cantly higher (P < 0.01) KS than shoots of VC 2 and 3 (least 3 years does not exceed 10 cm year ; and VC 3 = mean shoot vigorous shoots) (Figure 1A). Shoots of VC 0 had a signifi- increment over the last 3 years does not exceed 5 cm year–1 cantly (P < 0.01) higher KLS than shoots in all other vigor (Roloff 1993). classes (Figure 1B). Eight to nine branches per tree were selected in the south- Sapwood specific conductivity of excised segments, KW, facing upper canopy (about 15 m above ground). One leaf per was reduced significantly (P < 0.001) when a segment con- Downloaded from https://academic.oup.com/treephys/article/22/8/597/1648401 by guest on 30 September 2021 branch was labeled and gas exchange was measured several tained nodes (Figure 2); however, this effect was limited to times throughout the day between 1000 and 1600 h. Stomatal segments with diameters of less than 2 mm. The smaller the di- conductance (gs) and net carbon assimilation rate (A) were ameter of the nodal segment, the larger the deviation in KW measured with a portable gas analyzer (HCM-1000, Walz, from the value attained by internodes of similar diameter. Effeltrich, Germany). Over the range of 1 to 5 mm in sapwood diameter, segments –6 –6 –1 –1 without nodes had a KW of 7.13 × 10 ±0.2×10 kg s m Hydraulic architecture MPa–1, compared with a value of 4.54 × 10–6 ±0.3×10–6 kg All the branches used for gas exchange measurements were s–1 m–1 MPa–1 for segments with nodes. enclosed in dark plastic bags with wet paper towels and imme- Variation in gs was closely associated with variation in KLS. diately transported to the laboratory for further analysis. Peak values of gs initially rose sharply, then more gradually –1 –1 Whole-shoot hydraulic conductance (KS;kgs MPa ) was with increasing KLS (Figure 3). The response of gs to vapor measured with a custom-built, high-pressure flow meter pressure deficit did not differ significantly among vigor (HPFM) as described by Tyree et al. (1993, 1994, 1995). In the classes. Peak transpiration (Emax) increased linearly with KLS laboratory, the bases of the shoots were recut under water to a (data not shown). basal diameter of 4–9 mm and connected to the HPFM. Peak net assimilation rates of individual shoots were signifi- Branch temperatures were measured to account for changes in cantly correlated with KS and KLS. Net assimilation rate ap- water viscosity and values were standardized to 20 °C. For the peared to rise to a maximum (Amax) when plotted against KS perfusion, we used degassed, filtered (pore size 0.2 µm) and (Figure 4), and was linearly correlated with KLS (Figure 5). acidified demineralized water. Leaves and petioles were re- The most vigorous shoots (VC 0) had significantly higher (P < moved by stripping them from current-year shoots. Shoots were infiltrated at a pressure of 0.1 MPa until water was drip- ping from the cut ends and water flow entering the shoot be- came constant.

We determined KS by dividing the rate of water flow through the shoot measured with the HPFM (F;kgs–1)bythe pressure drop (P; MPa) from the base of the shoot to the apices with leaves removed (Yang and Tyree 1993). Leaf specific shoot conductance (KLS) was calculated as KS/AL, where AL is leaf area, which was measured with a leaf area meter (Delta-T Devices, Cambridge, U.K.).

On another set of branches, hydraulic conductivity (KH;kg –1 –1 s mMPa ) and sapwood specific conductivity (KW)ofex- cised segments with or without nodes were measured as described by Sperry et al. (1988). Briefly, a 5- to 10-cm long segment was excised under water to prevent air from entering the xylem. The segment was then connected to plastic tubing supplied with degassed, filtered and acidified demineralized water under a pressure of 0.006 MPa. Flow rates through segments were measured gravimetrically to determine KH.

Statistical analysis

Effects of vigor class on KS, AL and KLS were subjected to analysis of variance with the branch basal diameter as covariate. Figure 1. Effects of vigor class on shoot conductance KS (A) and leaf All analyses were conducted with the general linear model in specific shoot conductance KLS (B). Error bars indicate one standard the SPSS software package (SPSS, Chicago, IL). error.

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Figure 2. Sapwood specific hydraulic conductivity (KW) of segments Figure 4. Relationship between maximum measured net assimilation less than 2 mm in diameter and with (᭺) or without (᭹) nodes. Values rate (Amax) and hydraulic shoot conductance (KS) measured in the of r 2 are 0.73 and 0.90, respectively. same shoot (line represents hyperbolic equation).

0.001) Amax than shoots in the other vigor classes (0.55 versus (Figure 1B). Two types of bottlenecks to water transport can 5.97 ± 0.28 µmol m–2 s–1). be identified in shoots of old oak trees, namely nodes and

abscission zones. The reduction in KW was especially severe in shoots with diameters of less than 2 mm (Figure 2). Nodal con- Discussion striction zones, which have been reported previously (Zim- With increasing age, crown and consequently hydraulic archi- mermann 1978, Salleo et al. 1982, Tyree et al. 1983, Salleo tecture of trees undergo fundamental changes (Roloff 1993). and LoGullo 1986), are characterized by low vessel diameter In pedunculate oak, cladoptosis is the main mechanism re- and a high frequency of vessel ends (Zimmermann 1983). Be- sponsible for the transformation of crown architecture. In stem cause older segments tend to be wider than younger segments junctions of juvenile oaks, the formation of regular xylem dis- (regression r = 0.57, P < 0.001), our data indicate that, within a ables the abscission zone immediately after flushing, whereas nodal zone, anatomical differences between nodal and inter- in mature trees the frequency of active abscission zones in- nodal wood decrease as the branch ages. creases with age and declining vigor. In addition, more and There is substantial evidence from modeling studies (Jones

longer chains of short shoots are formed in aging trees. Be- and Sutherland 1992) and experimental data that gs is at least cause nodes (Figure 2; Rust and Hüttl 1999) and abscission partially limited by the hydraulic conductance of the soil– zones (Rust et al. 2000) reduce hydraulic conductance, their root–leaf pathway in a wide range of plant species (Meinzer occurrence may partially explain the results of Tyree et al. and Grantz 1990, Sperry and Pockman 1993, Bond and Kava- (1993), who found a 1.5- to 2-fold higher resistance in shoots nagh 1999, Meinzer et al. 1999). In contrast to other studies of of pedunculate oak than in sessile oak (Quercus robur L. ssp. the hydraulic limitation hypothesis, where reduced hydraulic petraea Kl. et Kr. et Rol.), which has a lower rate of abscis- conductance of shoots in old trees was deduced from leaf gas sion. exchange data, xylem sap flow and leaf water potentials

In shoots of VC 3, KS was 27% lower than in shoots of VC 0 (Yoder et al. 1994, Ryan and Yoder 1997, Hubbard et al. 1999, (Figure 1A). Because lower KS is not offset by lower leaf ar- Tausend et al. 2000), we measured conductance with an eas, KLS was 39% lower in VC 3 shoots than in VC 0 shoots HPFM, a technique that is independent of gas exchange data.

Figure 3. Maximum measured stomatal conductance (gs) increases Figure 5. Relationship between maximum measured net assimilation with leaf specific hydraulic conductance (KLS) measured in the same rate (Amax) and leaf specific hydraulic shoot conductance (KLS) mea- shoot. The r 2 value of the hyperbolic fit is 0.64. sured in the same shoot.

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We found that maximum gs and A increased significantly Bond, B. and K.L. Kavanagh. 1999. Stomatal behavior of four woody species in relation to leaf-specific hydraulic conductance and with KL and KLS (Figures 3–5). Compared with other oak species, shoots of pedunculate oak contain a higher proportion of threshold water potential. Tree Physiol. 19:503–510. total aboveground resistance (Tyree et al. 1993). In addition, Cochard, H., N. Breda, A. Granier and G. Aussenac. 1992. Vulnera- bility to air embolism of three European oak species (Quercus pet- this species is more vulnerable to embolism than other oak raea (Matt) Liebl., Q. pubescens Willd., Q. robur L.). Ann. Sci. species (Cochard et al. 1992). It seems likely that gs is adjusted For. 49:225–233. to maintain xylem water potential above the critical point Flückiger, W., S. Braun, S. Leonardi, L. Förderer and U. Bühler. where runaway embolism (Tyree and Sperry 1988) would oc- 1989. Untersuchungen an Buchen in festen Waldbeobachtungs- cur. Similar relationships between hydraulic conductance and flächen des Kantons Zürich. Schweiz. Z. Forstwes. 140: 536–549. gas exchange have been reported for intact plants by Meinzer Hubbard, R.M., B.J. Bond and M.G. Ryan. 1999. Evidence that hydraulic conductance limits photosynthesis in old Pinus ponderosa

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