Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol16.1996:

Tree Physiology 16, 459--468
© 1996 Heron Publishing----Victoria, Canada

Hydraulic conductance, light interception and needle nutrient
concentration in Scots pine stands and their relations with net primary
productivity
MAURIZIO MENCUCCINI1,2 and JOHN GRACE3
1

Istituto di Ecologia Forestale e Selvicoltura, Università degli studi di Firenze, Via S. Bonaventur
a, 13, 50145 Firenze, Italy

2

Present address: Boyce Thompson Institute for Plant Research, Cornell University, Tower Road, Ithac
a, NY 14853-1801, USA

3

Institute of Ecology and Resource Management, University of Edinburgh, Darwin Building, Mayfield Ro
ad, EH9 3JU Edinburgh, U.K.

Received June 8, 1995

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 belowground) 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 pronounced reduction in old stands. At the tree scale, annual
biomass growth per unit of leaf area (growth efficiency) declined 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 related to the progressive increase in growth and maintenance
respiration associated with nonphotosynthetic tissues in mature 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 (Kuuluvainen 1991), a change in the allocation patterns (Long and
Smith 1992), or a reduction in the needle photosynthetic capacity 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 tradeoff, 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 observations) 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 efficiency, Eg. Parameters related to sapwood maintenance respiration (i.e., tree sapwood volume), photosynthetic capacity
(needle nitrogen concentration) and radiation interception
(light extinction coefficients) are also presented.

460

MENCUCCINI AND GRACE

Materials and methods

used to obtain information about tree leaf area, stem sapwood
volume, conductive capacities of stem and branches, and
needle nutrient concentration.

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 bedrock, 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 selected in even-aged stands of Scots pine, with tree age (measured 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 homogeneous 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 dominant trees (30 trees total) were felled during late September
1993, i.e., after summer needle fall. The 30 felled trees were

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 measured. 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 overbark 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
code

Age
(years)

Lynford
Hockham
Santon
Lynford
Lynford
Santon
Harling
Hockham
Croxton
Harling

4087

9036
5016
4086
4078
3047
8029
9047
5036
8033

7
7
14
18
32
33
43
46
58
59

1

Trees ha −1
3280
3285
3133
3883
1560
1783
796
732
430
398

Basal area
(m2 ha −1)

D
(cm)

H
(m)

Asba
(m2 ha −1)

Gt
(g MPa −1 s −1)

7.01
7.03
40.34
30.48
48.63
48.58
41.12
38.32
34.95
38.05

6.8 (3.1)
6.9 (3.2)
12.8 (3.4)
10.0 (3.9)
19.9 (5.8)
18.6 (4.0)
25.6 (5.3)
25.8 (4.8)
32.2 (4.2)
34.8 (5.2)

1.6 (0.2)
2.2 (0.3)
7.7 (0.7)
9.9 (0.2)
16.9 (1.2)
18.4 (0.6)
19.5 (1.3)
19.1 (0.8)
24.2 (0.1)
21.7 (1.3)

2.32
3.16
38.31
29.45
44.04
44.46
36.42
33.94
30.31
32.71

0.776 (0.994)
0.792 (0.980)
2.130 (0.810)
1.168 (0.802)
2.283 (0.698)
1.677 (0.698)
2.672 (0.722)
2.858 (0.720)
2.056 (0.830)
3.520 (0.815)

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
and H, and 95% confidence limits for Gt (calculated from the regression).

NET PRIMARY PRODUCTIVITY IN SCOTS PINE STANDS

the crown. A regression model based on branch basal diameter
and position in the crown was used to estimate branch conductance 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 aboveground 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 correlated 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 volumes. 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.

461

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 excluded) were calculated as:
Γ=−

ln(Q i/Q 0)
cos θ,
0.5 Lt

(1)

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

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-surface-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).
During the early morning on two uniformly overcast winter
days (March 15--16, 1994), light interception measurements
were repeated with an LAI-2000 plant canopy analyzer (LiCor, Inc., Lincoln, NE). Ten to 12 readings were made inside
each stand (saplings excluded), and two readings were made
outside in a large open area (before and after the below-canopy
readings). A 90° view restrictor with the same azimuthal ori-

462

MENCUCCINI AND GRACE

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 calculated 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 )
.
0.5 Lt

(2)

Stand NPP
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, R2adj = 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

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 nonrandomness of needle distribution in the canopy (Nilson 1971).
The clumping factor varies between 0 for a completely aggregated foliage distribution and 1 for a random distribution.
Therefore, the comparison between Lt and LLi-Cor gives information 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 calculated as:
IL =

1 − tr
0.5Lt

,

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
−2 −1
m s ), was calculated as:
n

(5)

∑ Gt

i

i=1

Ap

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 ageclasses (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 treatment (Steel and Torrie 1980).
Results
Stand scale parameters

(4)

where tr is the average stand transmittance.

G st =

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 magnesium as described by Allen (1974).

,

where Ap is the plot area (m2), and Gt is the tree aboveground
hydraulic conductance.

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 measurements; 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).
The LAI-2000 always underestimated the allometrically
determined L, calculated as one half the total leaf area. On
average, values of LLi-Cor were 34% smaller than values of
0.5Lt. Estimates based on a reduced area of view (four rings of
the LAI-2000) increased the values of LLi-Cor by 9--15%, especially in the most dense stands (cf. Stenberg et al. 1994). Values
of Ω calculated for each stand varied between 0.48 and 0.83
(average = 0.66) and between 0.42 and 0.83 (average = 0.64)
for the winter LAI-2000 and summer PAR sensor measurements, respectively (Table 2). Winter and summer Ω values

NET PRIMARY PRODUCTIVITY IN SCOTS PINE STANDS

463

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). Radiation interception 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

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)
Aboveground stand hydraulic conductance, Gst (g MPa −1 m −2 s −1). (d)
Annual net primary production, NPP (above- plus belowground, fine
roots excluded, g dry matter m −2 year −1), averaged for the period
1988--1993. Each point represents the average of the values from two
plots for each stand. Age is determined from the year of planting. The
values of Lp and Gst were calculated using the equations given in the
text and Mencuccini and Grace (1996). The NPP was calculated using
Ovington’s (1957) data set and measured growth rates. Radiation
interception was determined with PAR sensors over 4 days in summer
(August 14--17, 1993) and with a Li-Cor LAI-2000 over 2 days in
winter (March 15--16, 1994).

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

Variations in stand leaf area indices or leaf biomass with stand
age have frequently been reported (e.g., for Scots pine, Ovington 1957, Albrektson 1980, Miller and Miller 1987, Kuuluvainen 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 indicated that foliage density in the 15- and 30-year-old (unthinned) 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 distribution 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

464

MENCUCCINI AND GRACE

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
Lynford
Lynford
Santon
Harling
Hockham
Croxton
Harling

5016
4086
4078
3047
8029
9047
5036
8033

14
18
32
33
43
46
58
59

5.3 (6.9)
4.3 (5.6)
5.3 (6.9)
5.6 (7.2)
4.1 (5.3)
3.8 (4.9)
3.1 (4.1)
3.2 (4.2)

0.18 (0.14)
0.22 (0.17)
0.18 (0.14)
0.17 (0.13)
0.20 (0.16)
0.22 (0.17)
0.26 (0.20)
0.22 (0.16)

0.65 (0.41)
0.63 (0.36)
0.61 (0.39)
0.55 (0.28)
0.41 (0.29)
0.49 (0.30)
0.55 (0.33)
0.40 (0.21)

0.83 (0.83)
0.78 (0.72)
0.73 (0.79)
0.66 (0.56)
0.52 (0.58)
0.59 (0.59)
0.66 (0.66)
0.48 (0.42)

1

Symbols: Lt, 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
15
30
45
60

1.51
1.32
1.56
1.60
1.69

0.42
0.61
0.51
0.42
0.54

0.11
0.11
0.09
0.08
0.09

1

Differences within columns are not significantly different (P < 0.05)
according to an orthogonal polynomial contrast test (n = 10), following ANOVA.

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 silhouette 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 measurements 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 individual hydraulic conductance and stand density (see Table 1),
suggests that stand age may significantly affect the components 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 completely 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 aboveground hydraulic conductance of the old stands with the community 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 underlying 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; therefore, 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 efficiency of conversion of solar radiation in old trees accounts for
the age-related declines in NPP and Eg.

NET PRIMARY PRODUCTIVITY IN SCOTS PINE STANDS

465

Figure 3. Relation between aboveground sapwood volume per unit of
leaf area, Vs /Al (m3 m −2), and over-bark breast height diameter, D
(cm), for the 30 sample trees (Vs/Al = exp(−7.4390 + 0.0809D), R2 =
0.784, P < 0.00001, SEE = 0.505). The ratio Vs/Al is linearly related to
aboveground sapwood maintenance respiration for the unit of leaf
area. h, 7 years old; s, 14--18 years old; j, 32--33 years old; r,
44--48 years old; d, 58--59 years old.

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 (lnE g = 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.

Long and Smith (1992) suggested that the age-related declines 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 undecomposed litter on the forest floor (Nommik 1966), result in reduced photosynthetic capacity; however, this explanation is
not supported by our data. Thus, although nitrogen requirements for conifer plantations peak at the time of canopy closure 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). Similarly, 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 conductances 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 (Sequoiadendron giganteum Bucholz, Grulke and Miller 1994).
We observed an age-related increase in aboveground sapwood 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-

466

MENCUCCINI AND GRACE

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 account 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, aboveground 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 respiration costs, E∗g (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 between soil and leaves (gravitational component excluded) increases 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 reductions 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 allometric 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).

Figure 4. Relation between E ∗g (growth efficiency corrected for construction 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,
58--59 years old.

Acknowledgments
Federico Magnani, James Irvine and Gail Jackson significantly contributed 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.

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