Summary Aboveground xylem hydraulic conductance was determined in Scots pine (Pinus sylvestris L.) trees and stands from 7 to about 60 years of age. At the stand scale, leaf area index and net primary productivity (NPP, above- plus below-ground) increased and reached a plateau at about 25--30 and 15--20 years, respectively; both parameters declined in mature stands. Stand hydraulic conductance followed a similar trend to NPP, with a maximum at about 15--20 years and a pro-nounced reduction in old stands. At the tree scale, annual biomass growth per unit of leaf area (growth efficiency) de-clined with tree age, whereas aboveground sapwood volume per unit leaf area, which is linearly related to maintenance respiration costs, steadily increased. Radiation interception per unit leaf area increased significantly with reduced leaf area index of mature stands, despite increased foliage clumping in the canopies of mature trees. Needle nutrient concentration did not change in the chronosequence. Tree hydraulic conductance per unit leaf area was strongly and positively correlated with growth efficiency. We discuss our findings in the context of growth reductions in mature and old trees, and suggest that increased hydraulic resistance and maintenance respiration costs may be the main causes of reduced carbon gain in mature and old trees.
Keywords: hydraulic architecture, Pinus sylvestris, respiration costs, transpiration.
Introduction
The pattern of variation in net primary productivity (NPP) of forest stands over the life cycle of the forest is well established (Waring and Schlesinger 1985). In a young stand, NPP first increases until canopy closure when a plateau is reached. Later, there is a steady decline in NPP with the progressive opening of the canopy. Part of the decline in NPP is attributable to reductions in stand density and leaf area index; however, large variations in growth efficiency of trees, Eg (i.e., biomass or volume growth per unit leaf area; Waring 1983) also occur with age (Kaufmann and Ryan 1986, Kuuluvainen 1991).
Traditionally, declines in stand NPP and Eg have been re-lated to the progressive increase in growth and maintenance respiration associated with nonphotosynthetic tissues in ma-ture and old stands (Yoda et al. 1965, Kira and Shidei 1967), but alternative explanations have also been proposed including a reduction in the efficiency of radiation interception (Kuulu-vainen 1991), a change in the allocation patterns (Long and Smith 1992), or a reduction in the needle photosynthetic ca-pacity of old trees (Kull and Koppel 1987).
When a tree ages, the pathway for water transport from the soil to the top of the canopy increases greatly. According to a simple Ohm’s Law analogy of water flow (Richter 1973), if height growth is not exactly matched by a steady increase in transport capacities per unit of tree leaf area, the difference in water potential between the soil and leaves, ∆Ψ, will have to increase to maintain a constant transpiration rate (Jarvis 1975, Zimmermann 1983). Increases in ∆Ψ during the tree life cycle may be detrimental, particularly if tissue water potentials fall below species-specific cavitation thresholds (Tyree and Sperry 1989, Tyree and Ewers 1991). As a consequence of this trade-off, old trees might have a lower time-averaged transpiration rate than young trees. However, few experiments have been performed to test whether the hydraulic conductance over the whole pathway changes with tree age (Yang and Tyree 1994, Saliendra et al. 1995, Mencuccini and Grace 1996). A lower transpiration rate may represent a constraint for tree growth because of stomatal limitations to photosynthesis (Jones 1992).
Recently, Mencuccini and Grace (unpublished observa-tions) estimated aboveground xylem hydraulic conductance for Scots pine (Pinus sylvestris L.) trees ranging from 7 to about 60 years of age. We now use those results to estimate: (a) at the stand scale, the hydraulic conductance for the same stands; and (b) at the tree scale, the relationship between tree hydraulic conductance per unit of leaf area and growth effi-ciency, Eg. Parameters related to sapwood maintenance respi-ration (i.e., tree sapwood volume), photosynthetic capacity (needle nitrogen concentration) and radiation interception (light extinction coefficients) are also presented.
Hydraulic conductance, light interception and needle nutrient
concentration in Scots pine stands and their relations with net primary
productivity
MAURIZIO MENCUCCINI
1,2and JOHN GRACE
31
Istituto di Ecologia Forestale e Selvicoltura, Università degli studi di Firenze, Via S. Bonaventura, 13, 50145 Firenze, Italy 2
Present address: Boyce Thompson Institute for Plant Research, Cornell University, Tower Road, Ithaca, NY 14853-1801, USA 3
Institute of Ecology and Resource Management, University of Edinburgh, Darwin Building, Mayfield Road, EH9 3JU Edinburgh, U.K.
Received June 8, 1995
Materials and methods
Site description
The study area is an extensive plantation of Scots pine and Corsican pine (Pinus nigra var. maritima (Ait.) Melv.) in Thetford Forest, East Anglia, U.K. Climatic data for the forest have already been presented (Mencuccini and Grace 1995). Average summer precipitation is 170 mm, and average July temperature is 17.0 °C. A soil description is given by Corbett (1973). Although there are some subtle differences among areas, linked to the average depth of the alkaline chalky bed-rock, that affect the patterns of understory vegetation and tree growth rates, soil nutrition is not considered to be a limiting factor for tree growth in Thetford Forest (Corbett 1973, S. Malone, personal communication). Ten study sites were se-lected in even-aged stands of Scots pine, with tree age (meas-ured from the year of planting) ranging from 7 to 59 years (Table 1). The selected stands are located at sites with a deep--medium deep chalky bedrock, and are considered homo-geneous with respect to site class and growth rate.
Genetic variability among stands was standardized by using Forestry Commission archives to select the stands according to age and origin. Eight stands were derived from seed collected locally in the seed orchards of the forest. The two youngest stands were naturally regenerated from nearby seed sources. No thinning had been performed during the last 10 years. The two sapling stands and stands 5016, 4086, 4078 and 3047 had never been thinned.
Sampling strategy
For each site, two 20-m diameter plots were selected in the 7-, 14- and 18-year-old stands and two 40-m diameter plots were selected in the other stands. The diameters of all the trees were measured to the nearest centimeter. At each site, three domi-nant trees (30 trees total) were felled during late September 1993, i.e., after summer needle fall. The 30 felled trees were
used to obtain information about tree leaf area, stem sapwood volume, conductive capacities of stem and branches, and needle nutrient concentration.
Tree leaf area
Ten to 15 branches of different sizes and in different crown positions were sampled per tree. Altogether, 279 branches were sampled in the 24 oldest trees, and the six saplings were completely harvested. For each branch, whorl number from the top was recorded, and branch diameter and length were meas-ured. The leafy shoots were cut, transported to the laboratory in black plastic bags, dried for 48 h at 80 °C and weighed to the nearest 0.1 g. Total needle mass was estimated from the total dry mass times the proportion of needle to total dry mass, which had been determined in separate samples for each whorl.
We developed a regression model for predicting branch needle mass based on branch size and whorl position within the crown (Mencuccini and Grace 1996). For each whorl, branch needle mass values were transformed to projected (flat) needle area by using values of specific leaf area appropriate for each canopy layer. Total tree projected needle area, Al (m2), was obtained from the sum of the predicted branch leaf areas.
Tree hydraulic conductance
Stemwood hydraulic conductivity, kh (i.e., water flow rate per unit of pressure × length, g m MPa−1 s−1), was measured on two stem disks per sample tree. The 60 samples were then used to find a relationship between hydraulic conductivity and over-bark stem diameter, so that the hydraulic conductance, Gs (i.e., water flow rate per unit of pressure, g MPa−1 s−1), of all the crown internodes could be estimated based on their diameters and lengths. Whole-branch conductance, Gb (i.e., flow rate from the branch base to all the tips per unit of pressure, g MPa−1 s−1), was measured on 39 sample branches selected to represent the whole range of diameters and whorl positions in
Table 1. Structural characteristics of the Scots pine stands before sampling.1
Site Stand Age Trees ha−1 Basal area D H Asba Gt
code (years) (m2 ha−1) (cm) (m) (m2 ha−1) (g MPa−1 s−1)
Lynford 4087 7 3280 7.01 6.8 (3.1) 1.6 (0.2) 2.32 0.776 (0.994)
Hockham 9036 7 3285 7.03 6.9 (3.2) 2.2 (0.3) 3.16 0.792 (0.980)
Santon 5016 14 3133 40.34 12.8 (3.4) 7.7 (0.7) 38.31 2.130 (0.810)
Lynford 4086 18 3883 30.48 10.0 (3.9) 9.9 (0.2) 29.45 1.168 (0.802)
Lynford 4078 32 1560 48.63 19.9 (5.8) 16.9 (1.2) 44.04 2.283 (0.698)
Santon 3047 33 1783 48.58 18.6 (4.0) 18.4 (0.6) 44.46 1.677 (0.698)
Harling 8029 43 796 41.12 25.6 (5.3) 19.5 (1.3) 36.42 2.672 (0.722)
Hockham 9047 46 732 38.32 25.8 (4.8) 19.1 (0.8) 33.94 2.858 (0.720)
Croxton 5036 58 430 34.95 32.2 (4.2) 24.2 (0.1) 30.31 2.056 (0.830)
Harling 8033 59 398 38.05 34.8 (5.2) 21.7 (1.3) 32.71 3.520 (0.815)
1 Age was calculated from date of planting. Values for number of trees ha−1, stem basal area (at 1.3 m) ha−1, stem diameter at breast height (D) (base of crown for the saplings) and sapwood basal area (at 1.3 m) ha−1 (Asba ), are the average from two 40-m diameter plots (20 m diameter in the four youngest stands) established in each stand before sample trees were felled; H is the average height of the three sampled dominant trees per stand; Gt (average tree hydraulic conductance, g MPa−1 s−1) is calculated as the hydraulic conductance of the tree of average basal area of each plot, estimated on the basis of diameter and height (see text for further details). Numbers in parenthesis are standard deviations for D
the crown. A regression model based on branch basal diameter and position in the crown was used to estimate branch conduc-tance for all the other branches (Mencuccini and Grace 1996). Tree aboveground hydraulic conductance, Gt (i.e., total tree flow rate from ground base to all the tips per unit of pressure, g MPa−1 s−1), for the 30 sample trees was then calculated by summing, either in series or in parallel, the conductances of all the branches and stem internodes (Mencuccini and Grace 1996). Tree Gt values were used to calculate leaf specific hydraulic conductances, GLS (i.e., the ratios of Gt to the tree leaf area (Al) values, g MPa−1 m−2 s−1). The GLS measures the capacity of the aboveground xylem to hydraulically supply the canopy.
Aboveground sapwood volume
Because sapwood maintenance respiration is linearly related to sapwood volume (Ryan 1990, Sprugel 1990), we used above-ground sapwood volume, Vs (m3), as an index of maintenance respiratory costs. For each of the 30 sample trees, sapwood area was measured at three positions along the stem (breast height, crown base and base of the top third of the crown) using either cores or entire sections. Stem diameter was measured at 1-m intervals along the bole and in the middle of every crown internode thereafter. Sapwood area, As (m2), was closely corre-lated with under-bark stem diameter, D (lnAs = −0.534 + 2.06lnD, R2 = 0.99, P < 0.0001); therefore, sapwood area at the base of each 1-m segment was estimated from the calculated regression and the measured stem diameter corrected for bark thickness. Stem sapwood volume was calculated assuming the trunk to be a cylinder in the basal 1 m, a frustum of a paraboloid along the stem and a cone in the top meter. Stem sapwood volume was obtained by summing the segment sapwood vol-umes. Branch biomass was calculated using the data set given in Ovington (1957) and converted to sapwood volume using measured wood specific gravity (0.44 g cm−3, Mencuccini and Grace 1995). Branches were assumed to be 100% sapwood. Tree biomass growth and growth efficiency
Tree biomass (above- plus belowground, excluding fine roots) was estimated using Ovington’s data set (1957), which was obtained in the same forest by a similar sampling protocol. We estimated tree biomass growth as the difference between 1993 and 1988 biomass values divided by five. Biomass values for both years were obtained from a regression model of tree biomass on breast height diameter (cf. Ovington 1957). A correction for logarithmic transformation bias was introduced (Baskerville 1972, Sprugel 1983).
The 1988 diameter of each tree was estimated by measuring the radial increments of the last 5 years on two cores taken at right angles at breast height. Growth efficiency, Eg (g m−2 year−1) (Waring 1983), was calculated as the ratio of the average annual tree biomass growth divided by the leaf area sustained at the end of the period.
Stand leaf area index
Winter leaf area for each tree in the stand plots was calculated from its basal area using site-specific nonlinear relationships
between total basal area and sapwood basal area, and between sapwood area and leaf area (Dean et al. 1988). Projected leaf area indices (Lp) were computed by summing the individual leaf areas of all the trees within each stand plot. Summer Lp values were estimated by assuming that the fraction of fallen 2-year-old needles represented about 30% of the total. This assumption was supported by two findings: first, in a previous investigation in which Scots pine trees at Thetford were cut before the summer needle fall (Mencuccini and Grace 1995), 2-year-old needles were found to represent about 30% of the total leaf area; and second, when the slope of the relationship between sapwood area and leaf area for the trees reported in this study was compared with the value given in Mencuccini and Grace (1995), which was determined during the summer, a difference of about 30% was found.
Light interception
During four cloudless days (August 14--17, 1993), PAR light interception was determined for each stand between 1100 and 1400 h. Two PAR sensors were used, one located outside the stand plots, in an open area of more than 50-m radius, and the second located inside one of the two plots of each stand. The two sensors were connected to microvolt integrators, so that cumulative radiation interception during a 10-min period could be determined (Saffell et al. 1979). The sensor inside the stand was held in a vertical position above the operator’s head and moved along fixed transects inside the plot area. Three or four measurement sessions were made for each stand. Stand PAR interception was calculated as the proportion of incoming (direct plus diffuse) radiation, Q0, that did not penetrate the canopies.
Light extinction coefficients for the stands (saplings ex-cluded) were calculated as:
Γ=−ln(Qi/Q0) 0.5Lt
cosθ, (1)
where Qi is the light measured beneath the canopies and Qi/Q0 is the fraction transmitted; Γ is the light extinction coefficient of the canopies, i.e., the mean projection of the unit leaf area (expressed as one half the total surface area) in the direction of the beam on a plane normal to the solar beam (Lang 1991, Chen and Black 1992, Stenberg et al. 1994); Lt is the total-sur-face-area leaf area index (at the summer level); and cosθ, the cosine of the solar zenith angle, accounts for the beam path length within the canopy. In Equation 1, Lt is used instead of Lp because this parameter is more closely related to radiation interception for nonflat objects (Chen and Black 1992). We calculated 0.5Lt by multiplying Lp by 1.35 (cf. Flower-Ellis and Olsson 1993).
ori-entation both inside and outside the stands was used to mask the operator.
For each ring of the LAI-2000, the average transmittance of isotropic diffuse radiation through the canopy,trd, was calcu-lated as a weighted average of the ring transmittance (weights = 0.066, 0.189, 0.247, 0.249 and 0.249, respectively). The extinction coefficient for diffuse isotropic radiation, kd, was obtained as (Stenberg et al. 1994):
kd =−ln(trd) 0.5Lt
. (2)
The effective leaf area index, as estimated by the LAI-2000 (LLi-Cor ), was then calculated according to Li-Cor (1991) and is related to the true L as (Smith et al. 1993):
LLi−Cor= 0.5LtΩ, (3)
where 0.5Lt is the true allometric leaf area index calculated as one half the total surface area (Chen and Black 1992), and Ω is the foliage clumping factor, which accounts for the nonran-domness of needle distribution in the canopy (Nilson 1971). The clumping factor varies between 0 for a completely aggre-gated foliage distribution and 1 for a random distribution. Therefore, the comparison between Lt and LLi-Cor gives infor-mation about foliage randomness in the canopy. An analogous expression for Ω was similarly derived from the summer PAR transmittance data, assuming Γ = 0.5.
For both the summer and winter measurement sets, average radiation interception per unit of leaf area, IL (m−2), was calcu-lated as:
IL =1 − tr 0.5Lt
, (4)
where tr is the average stand transmittance. Stand hydraulic conductance
Tree aboveground hydraulic conductance, Gt (g MPa−1 s−1), was closely correlated with stem diameter at breast height, D, and tree height, H (lnGt = −3.8892 + 1.9012lnD− 0.0034H2, R2 = 0.78, n = 30). This relationship was used to estimate hydraulic conductance for all the trees in the stand plots based on the measured breast height diameters and the average tree height of the sample trees of each stand.
Stand aboveground hydraulic conductance, Gst (g MPa−1 m−2 s−1), was calculated as:
The approach used to estimate individual tree biomass growth rates was extended to estimate stand NPP. To estimate diameter growth from 1988 to 1993 for all the trees in the plots, we used a calculated regression of basal area increment ∆Ab, on 1993 basal area values, Ab, and on tree height, H (ln∆Ab = 0.4617 − 0.0978H + 0.9587lnAb, Radj2 = 0.63, P < 0.0001, SEE = 0.375), based on the data from the 30 sample trees plus 50 additional trees from the same stands. Stand NPP was calculated as the sum of individual biomass growth rates.
Needle nutrient concentration
Needle nutrient concentrations were determined for the three sample trees of each stand. Three random samples (avoiding the terminal shoot) were taken from current-year needles on branches of different crown positions (top and middle crown), giving a total of six samples per tree. The needles were dried, ground and analyzed for total nitrogen, calcium and magne-sium as described by Allen (1974).
Statistical analyses
Differences in needle nutrient concentrations with stand age were evaluated (after angular transformation) with a one-factor analysis of variance, by grouping the 30 trees in five age-classes (i.e., 7, 15, 30, 45 and 60 years). Because tree age was a continuous variable, orthogonal polynomial contrasts, rather than means tests, were used to describe the response to treat-ment (Steel and Torrie 1980).
Results
Stand scale parameters
In winter, projected Lp increased from about 0.7 at 7 years to 4 at 14 years (Figure 1a) and then remained constant for about 15--20 years. Thereafter Lp declined to between 2 and 3.
Percent diffuse interceptance (from winter LAI-2000 meas-urements; Norman and Welles 1983) and percent intercepted light (from summer PAR sensor measurements) followed a similar pattern (Figure 1b), with a pronounced increase in transmittance in the two oldest stands. Values of radiation interception were generally high (sometimes close to 95%) in the young stands. Light extinction coefficients Γ and kd varied between 0.21 and 0.40 (average = 0.32) and between 0.40 and 0.65 (average = 0.54), respectively (Table 2). Both coefficients were inversely related to stand age (r = −0.73 and −0.78, respectively, P < 0.05).
were significantly correlated with each other (r = 0.91, P < 0.01) and the slope was not significantly different from 1 (P > 0.05). Both summer and winter Ω values significantly declined with stand age (R2 = 0.62, P < 0.01, n = 16), indicating an increase in foliage clumping or self-shading in mature trees. Average radiation interception per unit leaf area, IL, varied
between 0.17 and 0.26 m−2 and between 0.13 and 0.20 m−2 for the winter and summer data sets, respectively (Table 2). Radia-tion intercepRadia-tion per unit leaf area declined with increasing L (r = −0.93, P < 0.001, and r = −0.89, P < 0.01, for winter and summer, respectively).
Stand aboveground hydraulic conductance to water flow paralleled the age-related trend for NPP (cf. Figures 1c and 1d); Gst had maximum values of about 0.5--0.6 g MPa−1 m−2 s−1 for the 14- and 18-year-old stands and was markedly reduced in the older stands; the two 60-year-old stands had values that were similar to those of the two sapling stands (about 0.15 g MPa−1 m−2 s−1). Sapwood area per hectare (measured at breast height) steadily increased with stand age up to about 30--35 years and then declined (Table 1). Stand NPP peaked at about 15 years and then steadily declined in old stands (Figure 1d).
Needle nitrogen, calcium and magnesium concentrations did not differ among different tree age classes (Table 3, P > 0.05).
Tree scale parameters
Tree growth rate increased with stem diameter, but at a lower rate in large trees than in saplings. Therefore, Eg was lower for large trees than for small trees (Figure 2a). Tree Eg was also negatively related to Gt (Figure 2b) and linearly related to GLS (Figure 2c, r = 0.81, P < 0.0001). Aboveground sapwood volume increased with tree size so that sapwood volume per unit leaf area was larger for large diameter trees than for small diameter trees (Figure 3).
Discussion
Stand scale parameters
Variations in stand leaf area indices or leaf biomass with stand age have frequently been reported (e.g., for Scots pine, Ov-ington 1957, Albrektson 1980, Miller and Miller 1987, Kuulu-vainen 1991). In our stands, L reached a plateau at about 15 years of age. The subsequent reduction in L in the four oldest stands is attributed to a decrease in tree density that was accelerated by thinning. Light interception measurements in-dicated that foliage density in the 15- and 30-year-old (un-thinned) stands was close to the maximum that can be sustained at these sites. Under the canopies of the 15- and 30-year-old stands, almost no understory species were found, and the transmitted radiation was occasionally lower than 5%. The decline in light extinction coefficients with stand age may indicate an increase in foliage clumping in the canopies. Reductions in light extinction coefficients with increasing tree size or tree leaf area have been reported by Smith et al. (1991) and Sampson and Smith (1993) for unmanaged lodgepole pine stands and by Brown and Parker (1994) for mixed deciduous stands. In mature stands, foliage is concentrated in fewer trees and branches, with larger between- and within-crown gaps (Long and Smith 1992). Moreover, vertical needle area distri-bution and needle area density (needle area per unit of canopy volume) change with stand age (Mencuccini 1995). All of these age-related variations in branch geometry and shoot Figure 1. Variation of some stand parameters with tree age in 10 Scots
pine stands at Thetford, U.K. (a) Winter leaf area index (based on projected leaf area), Lp. (b) Percent of intercepted PAR radiation (+) and percent canopy diffuse interceptance from the LAI-2000 (j). (c)
arrangement can lead to an increase in foliage aggregation, thereby potentially reducing radiation interception (Sampson and Smith 1993, Sampson and Allen 1995). Our mean Ω value (0.65) corresponds to a canopy-averaged ratio of shoot silhou-ette area to total needle area of 0.162, which is close to the average value of 0.147 reported by Smolander et al. (1994) for spherically projected Scots pine shoots. This may imply that needle aggregation at the shoot level accounts for much of the discrepancy between the allometric and LAI-2000 measure-ments of leaf area index for Scots pine.
The age-related changes in stand hydraulic conductance paralleled the pattern observed for NPP with a maximum occurring at a stand age of 15--20 years. The finding that stand hydraulic conductance to water flow was strongly dependent on stand age, as a result of the age-related variation in individ-ual hydraulic conductance and stand density (see Table 1), suggests that stand age may significantly affect the compo-nents of the hydrological balance. We note that the reduction in stand hydraulic conductance was not paralleled by variation in stand sapwood area per hectare, which increased for 30--35 years before declining.
Stands of about 60 years of age (about the rotation age for this forest) had an aboveground hydraulic conductance that was about 25--30% of the maximum at 15--20 years of age. Based on the finding that understory vegetation was com-pletely absent in the stands between 14 and 33 years of age and
canopy radiation interception was around 95%, we speculate that the plateau value of hydraulic conductance for these stands (about 0.55 g MPa−1 m−2 s−1, see Figure 1c) represents the community value of aboveground hydraulic conductance. In the sapling stands, a dense community of graminoids, and in the older stands, a thick understory of bracken (Pteridium aquilinum L.) contribute to the pathway for water transport from soil to atmosphere. A comparison of the values of above-ground hydraulic conductance of the old stands with the com-munity value of 0.55 g MPa−1 m−2 s−1 suggests that the graminoids in the young stands and the bracken understory in the old stands influence the water flow from the soil to the atmosphere at least as much as the Scots pine canopy. This conclusion agrees with the finding that bracken L is generally inversely proportional to Scots pine L (Roberts et al. 1980, 1984). Similar results have also been obtained for different species and environmental conditions (Tan and Black 1976, Kelliher et al. 1990, Whitehead et al. 1994).
Tree scale parameters
Declining Eg with tree age has been reported for lodgepole pine (Pinus contorta var. latifolia Engelm.), Engelmann spruce (Picea engelmanii Parry ex. Engelm.), subalpine fir (Abies lasiocarpa (Hook.) Nutt.) (Kaufmann and Ryan 1986) and Scots pine (Kuuluvainen 1991); however, the mechanism un-derlying the reduction has not been elucidated.
Kuuluvainen (1991) proposed that age-related declines in NPP and Eg were related to reductions in radiation interception efficiency. However, in old stands, L generally declines; there-fore, all other factors being equal, intracrown competition for light should become less, not more intense in old trees. In our stands, despite increased foliage clumping, average radiation interception per unit leaf area, IL, was negatively related to L, indicating that intracrown competition for light decreased with tree age. We calculated that, with a decrease in L from 4 to 2.5 (about the range shown from 30 to 60 years of age, see Figure 1a), IL would increase by more than 30%, both for the PAR and LAI-2000 sets of measurements, thus invalidating Kuuluvainen’s (1991) proposal that a reduction in the effi-ciency of conversion of solar radiation in old trees accounts for the age-related declines in NPP and Eg.
Table 2. Light interception parameters during winter for Scots pine stands of different ages (summer values in parenthesis).1
Site Stand code Age (years) 0.5Lt IL kd(Γ) Ω
Santon 5016 14 5.3 (6.9) 0.18 (0.14) 0.65 (0.41) 0.83 (0.83)
Lynford 4086 18 4.3 (5.6) 0.22 (0.17) 0.63 (0.36) 0.78 (0.72)
Lynford 4078 32 5.3 (6.9) 0.18 (0.14) 0.61 (0.39) 0.73 (0.79)
Santon 3047 33 5.6 (7.2) 0.17 (0.13) 0.55 (0.28) 0.66 (0.56)
Harling 8029 43 4.1 (5.3) 0.20 (0.16) 0.41 (0.29) 0.52 (0.58)
Hockham 9047 46 3.8 (4.9) 0.22 (0.17) 0.49 (0.30) 0.59 (0.59)
Croxton 5036 58 3.1 (4.1) 0.26 (0.20) 0.55 (0.33) 0.66 (0.66)
Harling 8033 59 3.2 (4.2) 0.22 (0.16) 0.40 (0.21) 0.48 (0.42)
1 Symbols: L
t, total-surface-area leaf area index; IL, intercepted radiation (measured with PAR sensors in summer and with LAI-2000 in winter) per unit of leaf area; kd and Γ, light extinction coefficients calculated according to Equations 2 and 1, respectively; and Ω, foliage randomness factor for the canopy (0 < Ω < 1).
Table 3. Needle nutrient concentrations in Scots pine needles from stands of different age.1
Stand age class % N % Ca % Mg
7 1.51 0.42 0.11
15 1.32 0.61 0.11
30 1.56 0.51 0.09
45 1.60 0.42 0.08
60 1.69 0.54 0.09
1 Differences within columns are not significantly different (P < 0.05)
Long and Smith (1992) suggested that the age-related de-clines in NPP and Eg could be attributed to a change in allocation patterns; however, our total tree biomass growth (fine roots excluded) data rule out this possibility.
Another possible explanation for the large age-related
re-ductions in stand NPP and tree Eg is that reductions in needle nitrogen concentration, due to the accumulation of undecom-posed litter on the forest floor (Nommik 1966), result in re-duced photosynthetic capacity; however, this explanation is not supported by our data. Thus, although nitrogen require-ments for conifer plantations peak at the time of canopy clo-sure and then gradually decline (Beets and Pollock 1987, Miller 1995, but see also Binckley et al. 1995), needle nitrogen concentrations did not vary among age classes (Table 2). Simi-larly, in lodgepole pine and ponderosa pine, foliar nitrogen concentrations did not differ among different tree age classes (Schoettle 1994, Yoder et al. 1994, but see also Vapaavuori et al. 1995).
The most commonly accepted explanation of the age-related declines in NPP and Eg is based on maintenance respiration costs (Yoda et al. 1965, Kira and Shidei 1967) and assumes that respiration rates increase substantially and that photosynthetic rates remain constant with tree age; however, both of these assumptions have recently been queried (Ryan and Waring 1992, Yoder et al. 1994). Thus, in a subalpine lodgepole pine stand, growth respiration declined steadily with stand age, and although maintenance respiration increased, the increase was not sufficient to account for the observed reduction in NPP of the old stands (Ryan and Waring 1992). Yoder et al. (1994) observed reduced photosynthetic rates and stomatal conduc-tances and an increased effect of stomatal limitation in old trees of both P. contorta and P. ponderosa and speculated that reduced hydraulic conductance could account for the decline in Eg with tree age. Similar reductions in stomatal conductance of old trees have also been reported for Scots pine (Hellqvist et al. 1980, Mattson-Djos 1981) and giant sequoia ( Se-quoiadendron giganteum Bucholz, Grulke and Miller 1994).
We observed an age-related increase in aboveground sap-wood volume per unit leaf area (Figure 3); however, it seems unlikely that increases in maintenance respiration alone can account for the large reductions in NPP and Eg. To assess the potential effect of the age-related increase in sapwood volume per unit of leaf area, we estimated maintenance respiration from sapwood volume and mean yearly temperature as de-Figure 2. (a) Variation of growth efficiency, Eg(tree annual biomass
growth per unit of leaf area, g dry matter m−2 year−1), with leaf area for 30 dominant trees sampled from the 10 study sites (three trees per site) (Eg = exp(6.271 − 0.0219Al), R2 = 0.881, P < 0.00001, SEE = 0.228). Leaf area values estimated as in Mencuccini and Grace (1996). Annual biomass growth rates estimated on the basis of measured radial growth rates and Ovington’s (1957) allometric equations. (b) Relation between Eg and tree aboveground hydraulic conductance, Gt (g MPa−1 s−1), for the 30 dominant sample trees (lnEg = 6.0477 − 0.6801 lnGt,
R2 = 0.683, P < 0.00001, SEE = 0.372). (c) Relation between Eg and hydraulic conductance per unit of leaf area, GLS (g MPa m−2 s−1), for the 30 dominant sample trees from the 10 stands (Eg = 51.711 + 1708.06 GLS, R2 = 0.652, P < 0.00001, SEE = 101.89). h, 7 years old;
s, 14--18 years old; j, 32--33 years old; r, 44--48 years old; d, 58--59 years old. Large values of Eg, an index of biomass production efficiency, were significantly associated with large values of GLS, a parameter of tree hydraulic capacity.
scribed by Ryan et al. (1995). The values for the parameters Q10 (= 2) and respiration rate at 10 °C, R10 (= 7.8 µmol m−3 s−1), were taken from Linder and Troeng (1981) and Ryan et al. (1995), respectively. Respiration rates were adjusted to ac-count for daily and yearly temperature amplitudes (Ryan 1991a, 1991b). To correct tree biomass growth rates for both construction and maintenance respiration costs (in C units, foliage and belowground maintenance respiration excluded), we assumed construction respiration costs to be 28% of the C in the new growth (Chung and Barnes 1977). Based on the mean annual temperature at Thetford Forest of 10.0 °C, above-ground sapwood maintenance respiration was, on average, only 6.1% of total tree yearly production, which is close to the estimate of 7.6% in Figure 4 of Ryan et al. (1995). Growth efficiency corrected for construction and maintenance respira-tion costs, Eg∗ (g C m−2 year−1), was still negatively related to tree diameter, D (Figure 4, in relative units).
For the stands of this study, Mencuccini and Grace (1996) showed that aboveground xylem hydraulic conductance per unit leaf area, GLS, decreased about fourfold for mature trees (Figure 4). Assuming that the water potential difference be-tween soil and leaves (gravitational component excluded) in-creases by 50% from young to mature trees and that belowground conductance is similar among age classes, the greater resistance to water flow should reduce the transpiration rate in mature trees to around 70% of the rate in saplings. Reductions in stomatal conductance to about 20% of the value in young saplings have been measured in old (> 100 years old) Scots pine trees (Mattson-Djos 1981). Therefore, we conclude that hydraulic factors probably underlie the age-related reduc-tions in NPP and Eg. We consistently found a positive linear relationship between GLS and Eg. Although the presence of such a correlation does not imply the existence of a causal relationship (it might have simply been the result of the al-lometric scaling of structural and functional properties), it supports the suggestion that hydraulic factors, through their influence on stomatal behavior and photosynthetic rates, are associated with reduced growth rates of mature and old trees (Ryan and Waring 1992, Yoder et al. 1994).
Acknowledgments
Federico Magnani, James Irvine and Gail Jackson significantly con-tributed to the development of this project. Graham Russell and Paul Van Gardingen kindly provided the PAR sensors and the LAI-2000. Mike Brockington helped in collecting field data and in measuring dry needle mass. Jonathan Comstock critically reviewed a previous draft of the manuscript.
References
Albrektson, A. 1980. Total tree production as compared to conven-tional forestry production. In Structure and Function of Northern Coniferous Forests----An Ecosystem Study. Ed. T. Persson. Ecol. Bull. 32:315--328.
Allen, S.E. 1974. Chemical analysis of ecological material. Blackwell Scientific Publications, Oxford, U.K., 565 p.
Baskerville, G.L. 1972. Use of logarithmic regression in the estima-tion of plant biomass. Can. J. For. Res. 2:49--53.
Beets, P.N. and D.S. Pollock. 1987. Uptake and accumulation of nitrogen in Pinus radiata stands as related to age and thinning. N.Z. J. For. Res. 17:353--371.
Binckley, D., F.W. Smith and Y. Son. 1995. Nutrient supply and declines in leaf area and production in lodgepole pine. Can. J. For. Res. 25:621--628.
Brown, M.J. and G.G. Parker. 1994. Canopy light trasmittance in a chronosequence of mixed-species deciduous forests. Can. J. For. Res. 24:1694--1703.
Chen, J.M. and T.A. Black. 1992. Defining leaf area index for non-flat leaves. Plant Cell Environ. 15:421--429.
Chung, H-H. and R.L. Barnes. 1977. Photosynthate allocation in Pinus taeda. I. Substrate requirements for synthesis of shoot biomass. Can. J. For. Res. 7:106--111.
Corbett, W.M. 1973. Breckland forest soils. The Soil Survey, Rotham-sted Experimental Station, Harpenden, Herts, U.K., pp 6--13. Dean, T.J., J.N. Long and F.W. Smith. 1988. Bias in the leaf
area--sap-wood area ratios and its impact on growth analysis in Pinus con-torta. Trees 2:104--109.
Flower-Ellis, J.G.K. and L. Olsson. 1993. Estimation of volume, total and projected area of Scots pine needles from their regression on length. Stud. For. Suec. 190:1--19.
Grulke, N.E. and P.R. Miller. 1994. Changes in gas exchange charac-teristics during the life span of giant sequoia: implications for response to current and future concentrations of atmospheric ozone. Tree Physiol. 14:659--668.
Hellqvist, J., K. Hillerdal-Hagströmer and E. Mattson-Djos. 1980. Field studies of water relations and photosynthesis in Scots pine using manual techniques. In Structure and Function of Northern Coniferous Forests----An Ecosystem Study. Ed. T. Persson. Ecol. Bull. 32:183--204.
Jarvis, P.G. 1975. Water transfer in plants. In Heat and Mass Transfer in the Plant Environment. Part 1. Eds. D.A. de Vries and N.G. Afgan. Scripta Book Co., Washington, D.C., pp 369--394. Jones, H.G. 1992. Plants and microclimate. Cambridge Univ. Press,
Cambridge, U.K., 428 p.
Kaufmann, M.R. and M.G. Ryan. 1986. Physiographic, stand, and environmental effects on individual tree growth and growth effi-ciency in subalpine forests. Tree Physiol. 2:47--59.
Kelliher, F.M., D. Whitehead, K.J. McAneney and M.J. Judd. 1990. Partitioning evapotranspiration into tree and understory compo-nents in two young Pinus radiata D. Don stands. Agric. For. Me-teorol. 50:211--227.
Figure 4. Relation between Eg∗ (growth efficiency corrected for con-struction and maintenance respiration, in g C m−2 year−1, in relative units) and breast height diameter, D. The curve superimposed is not fitted to the data but represents the variation in GLS with D (also in relative units), taken from Mencuccini and Grace (1996). h, 7 years old; s, 14--18 years old; j, 32--33 years old; r, 44--48 years old; d,
Kira, T. and T. Shidei. 1967. Primary production and turnover of organic matter in different forest ecosystems of the western Pacific. Jpn. J. Ecol. 17:70--87.
Kull, O. and A. Koppel. 1987. Net photosynthetic response to light intensity of shoots from different crown positions and age in Picea abies (L.) Karst. Scand. J. For. Res. 2:157--166.
Kuuluvainen, T. 1991. Long-term development of needle mass, radia-tion intercepradia-tion and stemwood producradia-tion in naturally regenerated
Pinus sylvestris stands on Empetrum-Vaccinium site type in the northern boreal zone in Finland: an analysis based on an empirical study and simulation. For. Ecol. Manage. 46:103--122.
Lang, A.R.G. 1991. Application of some of Cauchy’s theorems to estimation of surface area of leaves, needles, and branches of plants and light trasmittance. Agric. For. Meteorol. 55:191--212. Li-Cor, Inc. 1991. LAI-2000 Plant canopy analyzer operating manual.
Li-Cor, Lincoln, NE, 180 p.
Linder, S. and E. Troeng. 1981. The seasonal variation in stem and course root respiration of a 20-year-old Scots pine (Pinus sylvestris
L.). Mittl. Forstl. Bundesvers. Wien 142:125--139.
Long, J.N. and F.W. Smith. 1992. Volume increments in Pinus con-torta var. latifolia: the influence of stand development and crown dynamics. For. Ecol. Manage. 53:53--64.
Mattson-Djos, E. 1981. The use of pressure bomb and porometer for describing plant water stress in tree seedlings. In Proc. Nordic Symp. on Vitality and Quality of Nursery Stock. Ed. P. Puttonen. Dept. Silviculture, Univ. Helsinki, Finland, pp 45--57.
Mencuccini, M. 1995. Hydraulic architecture parameters in a Scots pine chronosequence (Thetford, East Anglia, U.K.). Ph.D. Disser-tation. University of Padova, Italy, 150 p.
Mencuccini, M. and J. Grace. 1995. Climate influences the leaf area/sapwood area ratio in Scots pine. Tree Physiol. 15:1--10. Mencuccini, M. and J. Grace. 1996. Developmental patterns of
above-ground hydraulic conductance in a Scots pine (Pinus sylvestris L.) age sequence. Plant Cell Environ. In press.
Miller, H.G. 1995. The influence of stand development on nutrient demand, growth and allocation. Plant Soil 168/169:225--232. Miller, H.G. and J.D. Miller. 1987. Nutritional requirements of Sitka
spruce. Proc. R. Soc. Edinb. 93B:75--83.
Nilson, T. 1971. A theoretical analysis of the frequency of gaps in plant stands. Agric. Meteorol. 8:25--38.
Nommik, H. 1966. The uptake and translocation of fertiliser 15N in young trees of Scots pine and Norway spruce. Stud. For. Suec. 35:1--18.
Norman, J.M. and J.M. Welles. 1983. Radiative transfer in an array of canopies. Agron. J. 75:481--488.
Ovington, J.D. 1957. Dry matter production by Pinus sylvestris. Ann. Bot. 21:287--314.
Richter, H. 1973. Frictional potential losses and total water potential in plants: a re-evaluation. J. Exp. Bot. 24:983--994.
Roberts, J., J.S. Wallace and R.M. Pitman. 1984. Factors affecting stomatal conductance of bracken below a forest canopy. J. Appl. Ecol. 21:643--656.
Roberts, J., C.F. Pymar, J.S. Wallace and R.M. Pitman. 1980. Seasonal changes in leaf area, stomatal and canopy conductances and transpi-ration from bracken below a forest canopy. J. Appl. Ecol. 17:409--422.
Ryan, M.G. 1990. Growth and maintenance respiration in stems of
Pinus contorta and Picea engelmannii. Can. J. For. Res. 20:48--57. Ryan, M.G. 1991a. Effects of climate change on plant respiration.
Ecol. Appl. 1:157--167.
Ryan, M.G. 1991b. A simple method for estimating gross carbon budgets for vegetation in forest ecosystems. Tree Physiol. 9:255--266.
Ryan, M.G. and R.H. Waring. 1992. Maintenance respiration and stand development in a subalpine lodgepole pine forest. Ecology 73:2100--2108.
Ryan, M.G., S.T. Gower, R.M. Hubbard, R.H. Waring, H.L. Gholz, W.P. Cropper, Jr. and S.W. Running. 1995. Woody tissue mainte-nance respiration of four conifers in contrasting climates. Oecolo-gia 101:133--140.
Saffell, R.A., G.S. Campbell and E.C. Campbell. 1979. An improved micropower counting integrator. Agric. Meteorol. 20:393--396. Saliendra, N.Z., J.S. Sperry and J. Comstock. 1995. Influence of leaf
water status on stomatal response to humidity, hydraulic conduc-tance, and soil drought in Betula occidentalis. Planta 196:357--366. Sampson, D.A. and H.L. Allen. 1995. Direct and indirect estimates of leaf area index (LAI) for lodgepole and loblolly pine stands. Trees 9:119--122.
Sampson, D.A. and F.W. Smith. 1993. Influence of canopy architec-ture on light penetration in lodgepole pine (Pinus contorta var. latifolia) forests. Agric. For. Meteorol. 64:63--79.
Schoettle, A.W. 1994. Influence of tree size on shoot structure and physiology of Pinus contorta and Pinus aristata. Tree Physiol. 14:1055--1068.
Smith, N.J., J.M. Chen and T.A. Black. 1993. Effects of clumping on estimates of stand leaf area index using the Li-Cor LAI-2000. Can. J. For. Res. 23:1940--1943.
Smith, F.W., D.A. Sampson and J.N. Long. 1991. Comparison of leaf area index estimates from tree allometrics and measured light inter-ception. For. Sci. 37:1682--1688.
Smolander, H., P. Stenberg and S. Linder. 1994. Dependence of light interception efficiency of Scots pine shoots on structural parame-ters. Tree Physiol. 14:971--980.
Sprugel, D.G. 1983. Correcting for bias in log-transformed allometric equations. Ecology 64:209--210.
Sprugel, D.G. 1990. Components of wood-tissue respiration in young
Abies amabilis trees. Trees 4:88--98.
Steel, R.G.D. and J.H. Torrie. 1980. Principles and procedures of statistics. A biometrical approach. 2nd Edn. McGraw-Hill, New York, 663 p.
Stenberg, P., S. Linder, H. Smolander and J. Flower-Ellis. 1994. Performance of the LAI-2000 plant canopy analyzer in estimating leaf area index of some Scots pine stands. Tree Physiol. 14:981--995.
Tan, C.S. and T.A. Black. 1976. Factors affecting the canopy resis-tance of a Douglas-fir forest. Boundary-Layer Meteorol. 10:475--488.
Tyree, M.T. and F.W. Ewers. 1991. The hydraulic architecture of trees and other woody plants. New Phytol. 119:345--360.
Tyree, M.T. and J.S. Sperry. 1989. Vulnerability of xylem to cavitation and embolism. Annu. Rev. Plant Physiol. Mol. Biol. 40:19--38. Vapaavuori, E.M., A.H. Vuorinen, P.J. Aphalo and H. Smolander.
1995. Relationship between net photosynthesis and nitrogen in Scots pine: seasonal variation in seedlings and shoots. Plant Soil 168/169:263--270.
Waring, R.H. 1983. Estimating forest growth and efficiency in relation to canopy leaf area. Adv. Ecol. Res. 13:327--354.
Waring, R.H. and W.H. Schlesinger. 1985. Forest ecosystems: con-cepts and management. Academic Press, Orlando, FL, 340 p. Whitehead, D., F.M. Kelliher, P.M. Lane and D.S. Pollock. 1994.
Yoda, K., K. Shinozaki, H. Ogawa, K. Hozumi and T. Kira. 1965. Estimation of the total amount of respiration in woody organs in trees and forest communities. J. Biol. Osaka City Univ. 16:15--26.
Yoder, B.J., M.G. Ryan, R.H. Waring, A.W. Schoettle and M.R. Kauf-mann. 1994. Evidence of reduced photosynthetic rates in old trees. For. Sci. 40:513--527.
