Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol15.1995:

Tree Physiology 15, 1--10
© 1994 Heron Publishing----Victoria, Canada

Climate influences the leaf area/sapwood area ratio in Scots pine
MAURIZIO MENCUCCINI1,2 and JOHN GRACE3
1

University of Florence, Institute of Forest Ecology and Silviculture, Via S. Bonaventura 13, 50145 Firenze, Italy

2

Present address: Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, NY 14853-1801, USA

3

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

Received March 16, 1994

Summary We tested the hypothesis that the leaf area/sapwood area ratio in Scots pine (Pinus sylvestris L.) is influenced
by site differences in water vapor pressure deficit of the air (D).

Two stands of the same provenance were selected, one in
western Scotland and one in eastern England, so that effects
resulting from age, genetic variability, density and fertility
were minimized. Compared with the Scots pine trees at the
cooler and wetter site in Scotland, the trees at the warmer and
drier site in England produced less leaf area per unit of conducting sapwood area both at a stem height of 1.3 m and at the
base of the live crown, whereas stem permeability was similar
at both sites. Also, trees at the drier site had less leaf area per
unit branch cross-sectional area at the branch base than trees at
the wetter site. For each site, the average values for leaf area,
sapwood area and permeability were used, together with values
of transpiration rates at different D, to calculate average stem
water potential gradients. Changes in the leaf area/sapwood
area ratio acted to maintain a similar water potential gradient
in the stems of trees at both sites despite climatic differences
between the sites.
Keywords: hydraulic architecture, Pinus sylvestris, stem permeability, transpiration, xylem water potential.

Introduction
Plant responses to water deficits in the soil and humidity

deficits in the atmosphere vary temporally and spatially (Kozlowski 1983, Kramer 1983). Over short time scales, leaves
can acclimate through osmotic regulation, by changing stomatal behavior or by increasing water use efficiency. Over
longer time scales, structural modifications can be of major
importance and growth patterns can change as a consequence
of plant water stress. For example, leaf area and productivity
are reduced, whereas the depth of the absorbing root system
and the root/shoot ratio are increased.
Whole-tree responses to water deficits have received considerable attention in the last few years (Schulze 1986, Hinckley
and Ceulemans 1989), particularly the role of plant structure
on water absorption and transport processes (Jarvis 1975,
Zimmermann 1983, Tyree and Ewers 1991). However, little is
known about long-term acclimation as a result of which a

functional balance is maintained within the plant through
changes in carbon allocation. Present models are based on
either mechanistic processes of carbon partitioning or the use
of empirically determined partitioning coefficients, which are
generally based on the ‘‘pipe model’’ theory of plant form, i.e.,
on the relationship between leaf area (or leaf biomass) and
stem or branch sapwood area (Valentine 1985, Makela 1986).

Empirically derived coefficients are static; however, many
studies have shown that the leaf area/sapwood area ratio can
be influenced by variations in stand age (Albrektson 1984),
density, thinning practices (Aussenac and Granier 1988, Pothier and Margolis 1991) and site fertility (Espinosa-Bancalari et
al. 1987, Long and Smith 1988).
Thus, the leaf area/sapwood area ratio can only provide
useful insights on plant--environment relationships if the variables that contribute to the observed variation in the ratio are
identified and this information included in models of plant
growth (Grace 1992). Whitehead and Jarvis (1981) proposed
an equation for the prediction of the slope of the leaf area/sapwood area ratio (S) based on a combination of the PenmanMonteith equation (to describe the transpiration rate of a
coniferous canopy) and the Darcy equation (to describe water
flow through tree stems). The final theoretical expression for S
is (Whitehead et al. 1984a):
S=

k(∆Ψ/l)c
,
Dgs

(1)

where k is the average tree permeability, ∆Ψ/l is the water
potential gradient through the system, D is the time-averaged
vapor pressure deficit of the air, and gs is an appropriately
weighted stomatal conductance. The coefficient c is equal to:
c=

ρw γ λ
,
η cp ρa

(2)

where ρw, γ, λ, η, cp and ρa are the density of water, the
psychrometric constant, the latent heat of vaporization of
water, the dynamic water viscosity, the specific heat of air at
constant pressure and the density of air, respectively, all of
which are, apart from water viscosity, only weakly dependent
on temperature.

2

MENCUCCINI AND GRACE

Edwards and Jarvis (1982) and Whitehead et al. (1984a,
1984b) used this equation to study Sitka spruce (Picea sitchensis (Bong.) Carr.) and lodgepole pine (Pinus contorta Dougl.)
and found that variations in S among different species under
the same climatic conditions were best accounted for by considering variations in permeability. Coyea and Margolis (1992)
used the same equation to compare S in 24 balsam fir (Abies
balsamea (L.) Mill.) stands in Quebec and found that variations in S were directly proportional to permeability and
inversely proportional to tree height.
No systematic attempt has been made to evaluate the behavior of Equation 1 with respect to the Dgs term, i.e., to explore
whether the leaf area/sapwood area ratio is influenced by
variations in climate. In coniferous canopies, stomatal and
surface conductances are reduced by increases in D (e.g., Tan
and Black 1976, Jarvis 1981, Stewart 1988, Kelliher et al.
1993), but both field-based porometer and laboratory assimilation chamber studies have shown that an increase in transpiration rates with D still occurs (e.g., Whitehead et al. 1984b,
Sandford and Jarvis 1986).
We hypothesized that a constant water potential gradient
within tree stems at sites with different average vapor pressure

deficits (and hence transpiration rates) is maintained through
proportional changes in the leaf area/sapwood area ratio (see
Equation 1). Alternatively, changes in gradients of stem water
potential could occur. We tested these two hypotheses in a
study of two matched stands in different climatic regions of the
U.K., in which variability resulting from age and tree provenance was excluded.
The existence of feedback mechanisms in tree hydraulic
architecture in response to drought may have considerable
interest for modeling studies focused on the prediction of
long-term effects in response to global warming and increases
in atmospheric CO2.
Materials and methods
Site description
Two sites of Scots pine (Pinus sylvestris L.) in different climatic regions were selected: Thetford Forest in East Anglia,
southeastern England, and Aberfoyle Forest in southwestern
Scotland (Table 1a). Thetford Forest consists of over 200 km2
of mixed Scots and Corsican pine (Pinus nigra var. maritima
(Ait.) Melv.). Average summer precipitation is 170 mm and
average July temperature is 17.0 °C. During summer, D varies
from 0.5 to 3 kPa, but seldom exceeds 1.5 kPa (Beadle et al.

1985b). The soil is sandy, easily drained, and with a deep
chalky bedrock; details of soil characteristics are given by
Corbett (1973). Aberfoyle Forest is located in a large forest
district in southwestern Scotland. Most plantations comprise
Sitka spruce and lodgepole pine. Average July temperature is
14.4 °C and summer precipitation is 400 mm. Typically, D is
less than 1.0 kPa (G.E. Jackson, J. Irvine and J. Grace, personal communication). Moreover, for much of the summer, the
canopies are wet and transpiration from dry canopies is probably limited to about 50% of the daylight period (e.g., Jarvis
and Stewart 1979). Soils are gley-podsol and waterlogging is

locally frequent depending on the microtopography. Windthrows are frequent and the stand does not have complete
cover. Average wind speed is similar for the two sites.
In this study, Scots pine was the only species present. Forestry Commission archives were used to select the stands on
the basis of age and origin. They were planted in 1954 and
derive from the same seed lot of German origin. Because a seed
lot is made up of the seed crop of a single year from a single
seed collection area, genetic variability was uniform across
sites.
Table 1. Geographic, climatic, structural and nutritional characteristics
of the Thetford and Aberfoyle stands.1

Thetford

Aberfoyle

Site characteristics
Latitude
Longitude
Elevation (m)
Average January temperature (°C)
Average July temperature (°C)
Average annual precipitation (mm)
Average summer precipitation (mm)
Sunshine in summer (hr week − 1)
Average wind speed (m s − 1)

52°25′ N
0°40′ E
50
3.9
17.0

650
170
46
12.1

56°14′ N
4°16′ W
150
2.9
14.4
1500
400
35
13.2

Sample trees characteristics
Average db (cm)
Average height (m)
Crown depth (m)
Leaf area (m2)

SVI (m3 tree −1 year −1)
SVI / LA (× 10 − 4 m3 year −1 m − 2)

23.1 (4.2)
18.3 (1.1)
6.8 (1.15)
25.4 (3.6)
0.027 (0.005)
13.3 (2.2)

17.0 (3.9)
10.1 (1.9)
5.7 (1.77)
22.7 (3.1)
0.011 (0.002)
4.2 (0.6)

Stand structure
Leaf area index (m2 m−2)
Age (winter 1992)

Trees ha − 1
Average db (cm)
Basal area (m2 ha −1)
Sapwood basal area (m2 ha −1)
Stem volume (m3 ha − 1)
Stem sapwood volume (m3 ha − 1)
Yield class (m3 ha −1 year −1)

2.14 (0.44)
38
1146 (208)
21.0 (4.2)
41.59 (7.16)
25.79 (5.13)
310.6 (52.8)
193.3 (32.9)
8

2.59 (0.42)
38
1432 (299)
13.6 (4.2)
22.86 (3.98)
14.51 (2.53)
97.4 (16.6)
62.5 (10.7)
3

Stand nutrition
N (%)
P (%)
K (%)
Ca (%)
Mg (%)

1.0 (0.4)
0.1 (0.0)
0.4 (0.1)
0.4 (0.1)
0.1 (0.0)

1.3 (0.2)
0.1 (0.0)
0.4 (0.1)
0.3 (0.1)
0.1 (0.0)

1

Climate data from nearby meteorological stations in Aberfoyle and
Honington representing the Aberfoyle and Thetford sites, respectively. Sample tree characteristics are based on the mean of 10 sample trees for each study area. Stand structure data are based on the
mean of four replicated plots (area about 300 m2 each), with one
standard deviation given in parenthesis. SVI = average annual stem
volume increment per tree (1992 stem volume − 1989 stem volume)/3; SVI/LA = mean annual stem volume increment per unit of
leaf area. Yield class = mean annual stem volume increment per
hectare. Elemental composition was calculated from 25 samples for
each site, representing all age-classes and canopy positions.

CLIMATE INFLUENCE ON LEAF AREA/SAPWOOD AREA RATIO

Sampling protocol
At each site, a study area of about 0.2 ha was defined and,
within it, 10 trees were selected to represent all the diameter
size classes. The largest size class was represented by a larger
fraction compared to its real frequency (see later and Table 1b),
to increase the accuracy of the estimation of large leaf area
values. On each tree, total height, crown depth and diameter at
breast height (db) were measured. The 10 trees on each site
were cut down at the end of August 1992, i.e., during the period
of maximum needle area and before the beginning of autumn
needle fall (Beadle et al. 1982). All the needles were collected
with the attached twigs, brought to the laboratory in black
plastic bags and stored in a cold, constant temperature (2-4 °C) room until they were processed. The twigs were collected separately from each tree and whorl so that calculations
of individual leaf biomass and area, and vertical leaf area
distribution could be made. The heights of the whorls on the
stem were measured to the nearest cm and the number of
branches per whorl was recorded. The diameter at the base of
each branch was also recorded (branch swelling excluded) and
the sum of branch basal areas calculated. For each tree, two
0.5--0.6 m long stem sections were cut at heights of 1.3 m
(BH) and at the base of live crown (BLC) and used for permeability measurements and estimation of sapwood and heartwood cross-sectional areas.
To scale up from single trees to stand values, we selected
four plots of approximately 300 m2 within each study area.
Within each plot, db of all the trees was measured (Table 1c).
Basal area was calculated by summing over the diameter
distribution within each plot, and standing volume estimates
were made from forest mensuration handbooks (Hamilton
1975). Estimates of stem and stem sapwood volumes for each
plot were obtained from the intensively sampled trees and the
values were adjusted for the difference between the sample
basal area and the plot mean basal area (Cochran 1977).
Leaf area
In the laboratory, the twigs were sampled for each whorl by
removing and drying a fraction of the total fresh mass (48 h at
80 °C). Total needle dry mass for each whorl was the product
of total fresh mass and the ratio of needle dry mass to fresh
mass of the sample. The proportion of needle mass for each
needle age class was estimated based on a sample of six
complete whorls per site, taken randomly from the 10 trees and
representing three layers of the canopy (upper, middle and
lower levels). The division of the canopy was based on the
ecophysiological responses of needles to different light regimes (Beadle et al. 1985a). Specific leaf area was determined
on 100 randomly selected needles for each age class (current,
1- and 2-year-old needles) and each canopy layer. Projected
needle areas were measured with a Li-Cor area meter. For each
canopy layer, values of projected needle area were obtained
from needle dry mass based on the percentages of needle mass
for each age class and the appropriate values of specific leaf
area.
Leaf area for each tree in the four plots was calculated from
its basal area using the relationships between sapwood basal

3

area and total basal area and between leaf area and sapwood
area. The relationship between stem over-bark and sapwood
diameter was determined for each study area, following the
procedure of Whitehead (1978). Twenty cores from 10 trees
were sampled and the corresponding stem over-bark diameter
measured. Each core was immersed in a solution of o-toluidine, hydrochloric acid, distilled water and sodium nitrite
(Shain 1967). This solution is known to react with free phenols
which are more frequent in the heartwood. Values of leaf area
index (LAI) were computed by summing the individual leaf
areas of all trees within the four plots.
Vertical leaf area distribution was calculated assuming that
leaf area for each whorl was evenly distributed in 10-cm
intervals over a height of 1 m above the whorl and averaging
leaf area for each interval over all the sample trees. Leaf area
was then normalized with respect to the average sample needle
area and then to the plot leaf area index. The mean height of
the leaf area and the standard deviation of the leaf area with
respect to height were calculated following Stephens (1969),
and tests for significant skewness and kurtosis were made by
means of standard statistical procedures (Snedecor and Cochran 1967).
Permeability and conducting sapwood area
Stem water permeability was determined by the method described by Edwards and Jarvis (1982). Wood disks were stored
in humid plastic bags at 2 °C. Before measurement, they were
prepared by recutting about 15--20 cm from each end with a
band saw, to give a sample of about 20 cm in length. The two
surfaces were then chiseled to eliminate sawdust residues. The
water used was freshly distilled, filtered through 0.3 and
0.1 µm filters, and then degassed using an ultrasonic pump
under vacuum. The water was stored in 10 dm3 flasks and used
within 2 days. The stem section was sandwiched between two
Plexiglas plates, and the water was forced through the section
under a constant head of water. The outflow of water was
collected in a flask and weighed (± 0.01 g) every 3 min and,
concurrently, the hydrostatic pressure difference and temperature were recorded.
Water temperature was measured to 0.5 °C at the outflow
port and values of dynamic water viscosity were obtained from
tables. The sample length was measured to 1 mm on four sides
and the average taken. The values of water flow (q, m3 s −1),
length (l, m), sapwood area (As, m2), water viscosity (η, Pa s)
and pressure drop (∆P, Pa) were used to calculate permeability
following Darcy’s law (Siau 1984):
ki =

qηl
,
As ∆P

(3)

where ki (m2) is the permeability of the ith sample.
Generally a rapid increase in permeability was observed
until a plateau was reached. The samples were considered
saturated when, after three consecutive measurements, permeability values did not increase further.
Sapwood cross-sectional area was determined by injecting
sufficient toluidine blue into the flow path at the end of the

4

MENCUCCINI AND GRACE

measurement session. The sample was then recut and the area
measured on a new inner section close to the inflow port. An
estimate of stem sapwood volume was obtained from measurements of stem volume assuming a constant proportion of
sapwood area in relation to total basal area, as it was measured
at BH and BLC. After recutting, two wood samples (about
30 cm3 each) were taken from the outer and the inner sapwood
and from the heartwood for determination of relative water
content (RWC). These were used as an independent check of
wood saturation after the session. The same samples were also
used to determine sapwood basic density (WD, dry mass/fresh
volume, kg m −3). Fresh volume was determined by volume
displacement.
Needle nutrient analysis
In February 1993, random samples of needles were taken from
each age class and canopy layer to test for differences in
fertility between study areas. The needles were dried, ground
and analyzed for nitrogen, magnesium, calcium, phosphorus
and potassium concentrations (Allen 1974). Altogether, about
25 samples representing different canopy positions and ageclasses were taken for each study area.

m −1). Canopy transpiration was calculated using the PenmanMonteith equation (Monteith and Unsworth 1990), as in
Whitehead et al. (1984b).
Also, assuming that transpiration rate from an average individual in a stand where there are n stems per hectare is equal
to Et /(ρwn), we calculated the resistance to water flow for an
individual tree, Ri (MPa s m −3), as (Whitehead et al. 1984b):
Ri = nRp.

(5)

Statistical analysis
Linear regression was used to relate leaf mass and area to
sapwood area, permeability and sapwood area × permeability.
Leaf area was also related to the sum of branch cross-sectional
areas. We used analysis of covariance to determine if the
regression coefficients between leaf area and sapwood area (or
sapwood area × permeability) differed between the two sites.
Results
Vertical leaf area distribution

Basal area increments
Increments over the last 3 years were calculated from the
average of four measurements (± 0.1 mm) made with a binocular microscope along two diameters on the BH sample sections
of all 10 trees harvested at the two study areas. The calculated
1989 diameters together with those of 1992 were used to
estimate annual individual tree volume growth rates (SVI).
Volume growth was then compared with leaf area and an index
of needle efficiency in stem volume growth was obtained
(SVI/LA).

There were large differences in average tree height between
sites, but crown depth and leaf area index were similar (Table 1). At both sites, the vertical distribution of leaf area resembled a normal curve, with the center of the needle area
distributions above midcrown canopy height (Figure 1). The
parameters used to describe the foliage distributions are given

Physiological measurements
In a parallel investigation from May 1992 to June 1993,
monthly measurements were taken of shoot stomatal conductance, needle water potential and stem sapwood relative water
content (G.E. Jackson, J. Irvine and J. Grace, personal communication). Needle water potential (MPa) was measured at midday (Ψl). During summer 1992, it was also measured before
dawn (Ψpd). On the same days, wind speed, incoming radiation
and vapor pressure were measured above the canopy. Average
weekly vapor pressure deficits were also obtained from the
British Meteorological Office (British Meteorological Office,
Bracknell) from two nearby stations (Aberfoyle and Honington).
For summer days when field measurements were available,
we calculated the resistance of the entire pathway from soil to
leaves, Rp (MPa s m −1), as (Jarvis 1975):
Rp =

Ψpd − Ψl − h ρw g
,
Et

(4)

where Et (m s −1) is transpiration from the canopy and hρwg is
the gravitational potential of a column of water of height h and
density ρw under the acceleration due to gravity g (0.01 MPa

Figure 1. Vertical distribution of leaf area (leaf area density, LAD, m2
m − 3) at Thetford (j) and Aberfoyle (h). Projected leaf area indices
are 2.1 and 2.6 at Thetford and Aberfoyle, respectively.

CLIMATE INFLUENCE ON LEAF AREA/SAPWOOD AREA RATIO

in Table 2. The mean height was 40 and 46% of crown depth
and the standard deviation of leaf area with respect to height
was 27 and 37% of crown depth at the Thetford and Aberfoyle
sites, respectively. No asymmetry was found in the trees at
Aberfoyle, but the distribution was significantly skewed in the
trees at Thetford, where a larger proportion of leaf area was
above the mean canopy height than below it.

5

Permeability
Permeability at BLC was always greater than at BH. Variations
in permeability were associated with sapwood basic density
(Figure 5, P < 0.01, r2 = 0.46). Average BH and BLC permeability and sapwood basic density of the sample trees at Thetford did not differ significantly from those at Aberfoyle.
Comparison of stand properties

Comparison of tree properties between sites
The parameters for the regression equations between leaf mass
(kg) or leaf area (m2) and sapwood cross-sectional area at BH
and BLC, sum of branch cross-sectional area (CSA), permeability and sapwood area × permeability are given in Table 3.
The relationships between leaf area and sapwood area at BH
and BLC were always linear. For trees at the Aberfoyle site, the
regressions of leaf area on branch CSA and BH and BLC
sapwood area × permeability gave significant positive intercepts.
Covariance analysis showed a significant difference between sites in the slope of the relationship between leaf area
and sapwood area both at BH (P < 0.01, Figure 2a) and at BLC
(P < 0.01, Figure 2b). Also, a significant difference (P < 0.01)
was found when branch CSA was regressed against leaf area
(Figure 2c). When the straight lines were forced through the
origin, the slopes for BH and branch base for trees at Aberfoyle
were almost twice as large as those for trees at Thetford
(Figure 3). Covariance analysis did not show a significant
difference in the slopes between leaf area and sapwood area ×
permeability at BH and BLC (P > 0.05), whereas the intercepts
were significantly different in both cases (P < 0.01, Figures 2d
and 2e). Leaf-specific conductance values (LSC, sapwood area
× permeability/leaf area) were significantly higher in trees at
Thetford than in trees at Aberfoyle (P < 0.01), both at BH and
BLC (Table 4).
At Thetford, individual Huber values (sapwood area/leaf
area ratios, i.e., 1/S) decreased with tree size, both at BH
(Figure 4) and at BLC. At Aberfoyle, no differences among
trees were apparent.
Table 2. Parameters of the normal distribution of leaf area with height
for the two stands.
Parameter

Thetford

Aberfoyle

Crown depth (m)
Mean height of needle area distribution (m)
Midcrown height
Relative mean height (%)1
Standard deviation (m)
Relative standard deviation (%)2
Skewness
Kurtosis

6.8
15.6
14.9
40.4
1.9
27
0.98 *3
2.06 ns4

5.7
7.5
7.3
45.9
2.1
37
0.02
1.81 ns

1
2
3
4

Distance from top of canopy to mean canopy height/canopy depth ×
100.
Standard deviation/canopy depth × 100.
* = Significantly different from zero (P < 0.01).
ns = Not significantly different from 3.0.

We used Equation 4 to calculate Rp for the two stands during
2 days in summer; the average values were 0.700 × 107 and
1.090 × 107 MPa s m −1 for Thetford and Aberfoyle, respectively.
Table 5 summarizes the main hydraulic properties for the
average tree and for the stand in terms of a ratio between
Thetford and Aberfoyle values. For the tree of average leaf
area, leaf area and permeability were unchanged, whereas
sapwood basal area (and probably branch conducting tissue)
doubled; this corresponded to a 50% reduction in average
individual resistance, as calculated from Equation 5. Average
stand resistance at Thetford was reduced to 64% of the value
at Aberfoyle, a slightly higher ratio than for individual resistance.

Discussion
Tree properties
The trees at Thetford were much larger than those at Aberfoyle
(Tables 1b and 1c), with a larger increment of stem volume per
unit of leaf area. This faster growth rate was most likely a result
of the higher temperatures (mean July temperature was 2.6 °C
higher) and higher irradiances (number of sunshine hours per
week was about 30% higher) at Thetford compared with Aberfoyle.
The close relationships between leaf mass or area and sapwood area for Scots pine were similar to those found for many
other coniferous and broad-leaved species (Grier and Waring
1974, Waring et al. 1977, Whitehead 1978, Robichaud and
Methven 1992). Regressions of sapwood areas from below the
leaf canopy gave a better fit than those based on breast height;
for trees at Thetford, the regression was further improved when
CSA was used. This might be the result of a slower response
of stem growth to changes in needle and branch dynamics as
has been found when controlled pruning is performed (Margolis et al. 1988, Långström and Hellqvist 1991).
Significant differences in S were found between sites. The
slopes for trees at Thetford and Aberfoyle (Table 3) compared
well with those reported elsewhere for Scots pine. For BH, the
slope at Thetford (0.09) was similar to values (0.10 and 0.11)
reported previously for similar stands in the same forest
(Whitehead 1978). At Aberfoyle, the slope was 0.15, which is
intermediate between that at Roseisle, northeastern Scotland
(0.14) and that at Devilla, central Scotland (0.24, Whitehead
1978). When leaf area was plotted against the product of
sapwood area and permeability, separate regression lines were
necessary, because trees at Aberfoyle had larger leaf areas per
unit of conductive capacity than trees at Thetford.

6

MENCUCCINI AND GRACE

Table 3. Linear regression equations for the prediction of leaf dry mass (kg) and projected leaf area (m2) on the basis of BH and BLC sapwood
area, sum of branch cross-sectional area (CSA), permeability and sapwood area × permeability (standard errors are given in parenthesis).1
Y

X

Position

a

b

r2

Thetford
Leaf mass

Sapwood area

BH
BLC
Branch
BH
BLC
BH
BLC
BH
BLC
Branch
BH
BLC
BH
BLC

−0.38 (1.44)
−0.19 (1.30)
−0.07 (0.68)
0.08 (3.96)
−0.99 (2.29)
0.72 (1.15)
1.32 (0.99)
−1.86 (6.11)
−8.35 (5.41)
−0.31 (2.85)
0.52 (16.85)
−3.91 (9.87)
2.92 (4.92)
5.47 (4.28)

0.02 (0.01)
0.07 (0.01)
0.02 (0.00)
4.04 × 1012 (2.94)
2.22 × 1012 (0.76)
1.30 × 1014 (0.30)
1.29 × 1014 (0.28)
0.09 (0.02)
0.29 (0.05)
0.09 (0.01)
16.78 × 1012 (12)
9.20 × 1012 (3.32)
5.48 × 1014 (1.28)
5.42 × 1014 (1.21)

0.69
0.81
0.90
0.19 ns
0.51*
0.71
0.72
0.69
0.82
0.90
0.18 ns
0.49*
0.70
0.71

1.35
1.06
0.74
2.17
1.69
1.31
1.28
5.7
4.4
3.1
9.3
7.3
5.6
5.5

BH
BLC
Branch
BH
BLC
BH
BLC
BH
BLC
Branch
BH
BLC
BH
BLC

0.95 (1.04)
1.29 (0.78)
1.62 (0.68)*
2.02 (2.34)
−3.78 (1.84)
2.67 (0.95)*
2.35 (0.58)**
2.43 (4.15)
4.14 (2.52)
6.23 (2.46)**
5.65 (10.84)
−19.96 (8.91)
10.66 (3.70)*
10.10 (2.20)**

0.03 (0.01)
0.05 (0.01)
0.02 (0.00)
2.06 × 1012 (1.40)
3.02 × 1012 (0.60)
1.03 × 1014 (0.32)
1.10 × 1014 (1.82)
0.15 (0.03)
0.26 (0.03)
0.12 (0.01)
12.42 × 1012 (6.5)
15.05 × 1012 (2.9)
5.76 × 1014 (1.22)
5.75 × 1014 (0.68)

0.72
0.80
0.83
0.21 ns
0.76
0.58
0.82
0.82
0.92
0.91
0.31 ns
0.77
0.74
0.90

1.28
1.08
1.02
2.17
1.19
1.59
1.03
5.1
3.5
3.7
10.0
5.8
6.2
3.9

CSA
Permeability
Sapwood area × permeability
Leaf area

Sapwood area
CSA
Permeability
Sapwood area × permeability

Aberfoyle
Leaf mass

Sapwood area
CSA
Permeability
Sapwood area × permeability

Leaf area

Sapwood area
CSA
Permeability
Sapwood area × permeability

1

SEE

Equations are of the form Y = a + b X. Sapwood area measured in cm2. CSA = sum of branch cross-sectional areas measured in cm2; permeability
in m2; sapwood area × permeability in m4; BH = breast height (1.3 m); BLC = base of live crown; R2 = coefficient of determination; SEE =
standard error of the estimate. Intercepts not significantly different from zero (P > 0.05), unless indicated. Slopes always significant (P < 0.01),
unless indicated; ns = not significant; * = P < 0.05; ** = P < 0.01.

Figure 2. Relation between leaf area (m2)
and (a) BH sapwood area (cm2), (b) BLC
sapwood area (cm2), (c) sum of branch
cross-sectional areas (cm2), (d) BH sapwood area × permeability (m4), and (e)
BLC sapwood area × permeability (m4) at
Thetford (j, thin line) and Aberfoyle (h,
thick line). Parameters of the regression
equations are given in Table 4.

CLIMATE INFLUENCE ON LEAF AREA/SAPWOOD AREA RATIO

Figure 3. Slope S of the leaf area/sapwood area ratio at BH, BLC and
branch base for the two sites. Slopes refer to straight lines forced
through the origin. At branch base, total cross-sectional area (CSA)
was measured (heartwood within 10% of total CSA). Numbers in the
figure refer to the ratio of Aberfoyle/Thetford slopes. Asterisks refer
to the significance level of the differences between slopes (covariance
analysis).

Figure 5. Relation between natural logarithm of k (permeability, m2)
and logarithm of WD (sapwood basic density, kg m − 3) in Scots pine;
ln ( k × 1013) = 19.69 − 2.77 ln (WD), P < 0.01, R2 = 0.46.

Table 5. Ratio between Thetford and Aberfoyle values for the main
hydraulic properties.
Properties

Table 4. Summary of the hydraulic parameters for the 10 sample trees
(standard errors are given in parenthesis).1
Parameter
Leaf area (m2)

Thetford

Aberfoyle

22.7 (3.1)

25.4 (3.6)

BH
Sapwood area (cm2)
Permeability (× 10 − 12 m2)
S (m2 cm − 2)
LSC (× 10 −3 kg s − 1 m −1 MPa − 1)

268.9 (27.7)
1.3 (0.2)
0.08 (0.01)
1.6 (0.1)

151.9 (21.5)
1.6 (0.1)
0.17 (0.01)
0.9 (0.1)

BLC
Sapwood area (cm2)
Permeability (× 10 − 12 m2)
S (m2 cm − 2)
LSC (× 10 −3 kg s − 1 m − 1 MPa −1)

105.6 (9.4)
2.9 (0.2)
0.21 (0.02)
1.4 (0.1)

81.5 (13.2)
3.0 (0.2)
0.32 (0.02)
0.9 (0.1)

1

S = Leaf area/sapwood area ratio; LSC = leaf specific conductance
(sapwood area × permeability/leaf area).

Figure 4. Individual Huber values (sapwood area/leaf area ratio, cm2
m − 2) at BH for the two sites, Thetford (j) and Aberfoyle (h).

We hypothesized that a constant water potential gradient
within tree stems at sites with different average D (and hence
transpiration rates) can be maintained through proportional
changes in the leaf area/sapwood area ratio. Alternatively,

7

Thetford/Aberfoyle
ratio

Average tree
Leaf area (m2)
BH sapwood area (cm2)
BH permeability (× 10 − 12 m2 )
Individual resistance (MPa s m −3)
Theoretical stem ∆Ψ/l (MPa m −1)

1.04
2.18
0.93
0.52
0.69

Stand
Sapwood area (cm2 ha −1)
Leaf area index (m2 m −2)
Leaf area index/sapwood area (m2 cm −2)
Pathway resistance (MPa s m −1)

1.75
0.83
0.47
0.64

changes in gradients of stem water potential could occur. To
test our hypothesis, we used Equation 1, substituting for the
appropriate values of leaf area, sapwood area and permeability
of the two sites and solving for ∆Ψ/l, the gradient in the stem
water potential; stomatal conductance at different D was estimated using the relationship between the canopy-averaged
stomatal conductance and D given by Whitehead et al. (1984b)
for the Roseisle forest, which has an intermediate climate
between Aberfoyle and Thetford. Checks made with data
available for our stands showed that such a relationship adequately described average canopy behavior at both sites.
Trees at Thetford had a hydraulic advantage over trees at
Aberfoyle under the same climatic conditions, especially at
high D, i.e., at high transpiration rates (Figure 6). During
summer 1992, D ranged between 1.0--1.5 kPa and 0.5--1.0 kPa
at Thetford and Aberfoyle, respectively (G.E. Jackson, J. Irvine
and J. Grace, personal communication, British Meteorological
Office). As a consequence, trees at Thetford could develop a
theoretical gradient between 0.007 and 0.010 MPa m −1 compared with a range between 0.009 and 0.017 MPa m −1 (thicker
part of the straight lines) for trees at Aberfoyle. Values of water
viscosity were calculated assuming an average water temperature of 15 and 20 °C for Aberfoyle and Thetford, respectively.
Different combinations of temperatures did not change the
results.

8

MENCUCCINI AND GRACE

Figure 6. Relation between calculated water potential gradient (∆Ψ/l,
MPa m − 1) in the stem and water vapor pressure deficit of the air (D,
kPa) for an average tree at Aberfoyle and Thetford. The thicker parts
of the two lines indicate the range of D values commonly found at the
two sites. Water potential gradients were calculated using Equation 1
and assuming a water temperature of 15 and 20 °C for trees at
Aberfoyle and Thetford, respectively. See text for further details.

Thus, changes in the leaf area/sapwood area ratio effectively
acted to reduce the gradient in stem water potential of trees at
Thetford. Although the trees were the same age at the two sites,
there were large differences in tree size between sites which
might explain why the range in ∆Ψ/l at Thetford was, on
average, slightly lower than at Aberfoyle.
Measured values of stem water potential gradients for Scots
pine at Thetford based on a tree-cutting technique and water
potential measurements, i.e., including the gravitational component, are in the range 0.02 to 0.06 MPa m −1 (Roberts 1977).
These values were about 1--3 times higher than those found in
our study. This difference may be attributed to the use of
saturated sapwood permeability and median, rather than maximum, transpiration rates for our estimates of water potential
gradients. Stem sapwood permeability is probably reduced in
summer as a result of embolism, as shown by measurements of
seasonal variations in sapwood relative water content at our
sites (G.E. Jackson, J. Irvine and J. Grace, personal communication). Also, our values of stem permeability correspond to
the below-crown portion of the stems; if the conductive capacity of stem internodes within the crown had been considered,
lower permeability values would have been found (Pothier et
al. 1989).
Scaling up to the stand
The main resistance to water transport in Scots pine is in the
soil--root compartment (Roberts 1977), but both the stem and
the branches can contribute a significant resistance. Predawn
water potential (Ψpd) averaged −0.5 and −0.6 MPa at Aberfoyle
and Thetford, respectively, with midday values typically
around −1.4 to −1.6 MPa (G.E. Jackson, J. Irvine and J. Grace,
personal communication). Therefore, mean ∆Ψ between the
root surface and the leaves was about 0.9--1.1 MPa at both
sites. In the stems and branches, S was much smaller in trees
at Thetford than in trees at Aberfoyle (Figure 3), and this may
have contributed to the maintenance of the similar ∆Ψ and
prevented the need for lower water potentials in needles at
Thetford.

Also, the consistent reduction in the overall stand resistance
to water flow from the soil to the atmosphere during two days
in summer (Table 5) was probably determined by the development of a larger sapwood area in the stems and branches of
trees at Thetford compared with trees at Aberfoyle.
It is not known how the leaf area/sapwood area ratio is
maintained, i.e., whether xylem development controls leaf area
development or vice versa. Growth regulators (e.g., auxins) in
the leaves may control rates of cell division and maturation of
xylem (Larson 1976, Aloni 1991), and for Scots pine, there is
evidence that exogenous IAA promotes tracheid production in
the stem (Little and Sundberg 1990, Little et al. 1990). However, cambium activity, rather than IAA concentration, may
determine patterns of tracheid production (Sundberg et al.
1993).
Both variations in stand density and fertility are known to
influence S (Brix and Mitchell 1983, Long and Smith 1988).
High stand density and low fertility may indirectly affect the
amount of leaf area sustained by a unit of sapwood area by
increasing sapwood basic density (Keane and Weetman 1987,
Espinosa-Bancalari et al. 1987) and, consequently, by reducing
permeability (see Figure 5). It is unlikely that our results were
influenced by these variables. Although, at Thetford, vertical
leaf area distribution was significantly skewed (Figure 1) and
suppressed trees had higher Huber values (Figure 4), neither
sapwood basic density nor permeability differed between sites.
Moreover, needle elemental analysis showed no difference or
only small differences in nutrient concentration between the
two study areas (Table 1d), percent nitrogen concentration
being slightly higher in needles at Aberfoyle than at Thetford,
perhaps because of a difference in needle weight per unit leaf
area (Smith et al. 1981). Overall, our values of elemental
concentrations were within the normal range reported for Scots
pine needles (Ovington 1959, Malkonen 1974, Lim and
Cousens 1986, Helmisaari 1990).
The present investigation is the first field test of Whitehead
and Jarvis’s hypothesis with respect to the influence of climate
on the leaf area/sapwood area ratio. Our results suggest that
trees respond to increased transpiration rates determined by
increases in D through a reduction in the leaf area/sapwood
area ratio. The presence of a structural change in response to
increased evaporative demand has important consequences for
our understanding of the effects of water deficit on tree and
stand water relations.

Acknowledgments
We thank Gail Jackson and James Irvine for their help in collecting the
field data and for access to unpublished data. We also acknowledge
Paul Jarvis for useful comments on earlier versions of the manuscript
and Frank Berninger (University of Helsinki) for stimulating discussions. The first author was partly supported by a joint British Council-MURST agreement (Project: Ecological significance of cavitation).
Part of the project was funded by a grant from the Natural Environment Research Council.

CLIMATE INFLUENCE ON LEAF AREA/SAPWOOD AREA RATIO
References
Albrektson, A. 1984. Sapwood basal area and needle mass of Scots
pine (Pinus sylvestris L.) trees in Central Sweden. Forestry 57:35-43.
Allen, S.E. 1974. Chemical analysis of ecological material. Blackwell
Scientific Publ., Oxford, 565 p.
Aloni, R. 1991. Wood formation in deciduous hardwood trees. In
Physiology of Trees. Ed. AS. Raghavendra. John Wiley and Sons,
New York, pp 175--197.
Aussenac, G. and A. Granier. 1988. Effects of thinning on water stress
and growth in Douglas-fir. Can. J. For. Res. 18:100--105.
Beadle, C.L., H. Talbot and P.G. Jarvis. 1982. Canopy structure and
leaf area index in a mature Scots pine forest. Forestry 55:2--19.
Beadle, C.L., R.E. Neilson, H. Talbot and P.G. Jarvis. 1985a. Stomatal
conductance and photosynthesis in a mature Scots pine forest. I.
Diurnal, seasonal and spatial variation in shoots. J. Appl. Ecol.
22:557--571.
Beadle, C.L., R.E. Neilson, H. Talbot and P.G. Jarvis. 1985b. Stomatal
conductance and photosynthesis in a mature Scots pine forest. II.
Dependence on environmental variables of single shoots. J. Appl.
Ecol. 22:573--586.
Brix, H. and A.K. Mitchell. 1983. Thinning and nitrogen fertilization
effects on sapwood development and relationships of foliage quantity to sapwood area and basal area in Douglas-fir. Can. J. For. Res.
13:384--389.
Cochran, W.G. 1977. Sampling techniques. 3rd Edn. John Wiley and
Sons, New York, NY, 381 p.
Corbett, W.M. 1973. Breckland forest soils. The Soil Survey, Rothamsted Experimental Station, Harpenden, Herts, pp 6--13.
Coyea, M.R. and H.A. Margolis. 1992. Factors affecting the relationship between sapwood area and leaf area of balsam fir. Can. J. For.
Res. 22:1684--1693.
Edwards, W.R.N. and P.G. Jarvis. 1982. Relations between water
content, potential and permeability in stems of conifers. Plant Cell
Environ. 5:271--277.
Espinosa-Bancalari, M.A., D.A. Perry and J.D. Marshall. 1987. Leaf
area--sapwood area relationships in adjacent young Douglas-fir
stands with different growth rates. Can. J. For. Res. 17:174--180.
Grace, J. 1992. Incorporating species attributes and environmental
heterogeneity into forest models. In Responses of Forest Ecosystems to Environmental Changes. Eds. A. Teller, P. Mathy and J.N.R.
Jeffers. Elsevier Science Publ. Ltd., London, New York, pp 115-125.
Grier, C.C. and R.H. Waring. 1974. Conifer foliage mass related to
sapwood area. For. Sci. 20:205--206.
Hamilton, G.J. 1975. Forest mensuration handbook. For. Comm.
Lond. Booklet 39, 276 p.
Helmisaari, H.-S. 1990. Temporal variation in nutrient concentrations
in Pinus sylvestris needles. Scand. J. For. Res. 5:177--193.
Hinckley, T.M. and R. Ceulemans. 1989. Current focuses in woody
plant water relations and drought resistance. Ann. Sci. For.
46s:317--324.
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.
Jarvis, P.G. 1981. Stomatal conductance, gaseous exchange and transpiration. In Plants and Their Atmospheric Environment. Eds. J.
Grace, E.D. Ford and P.G. Jarvis. Blackwell, Oxford, pp 175--204.
Jarvis, P.G. and J.B. Stewart. 1979. Evaporation of water from plantation forest. In: The Ecology of Even-aged Plantations. Eds. E.D.
Ford, D.C. Malcolm and J. Atteson. Inst. Terr. Ecol., Cambridge,
pp 327--350.

9

Keane, M.G. and G.F. Weetman. 1987. Leaf area--sapwood cross-sectional area relationships in repressed stands of lodgepole pine. Can.
J. For. Res. 17:205--209.
Kelliher, F.M., R. Leuning and E.-D. Schulze. 1993. Evaporation and
canopy characteristics of coniferous forests and grasslands. Oecologia 95:153--163.
Kozlowski, T.T. 1983. Water deficits and plant growth. Vol. VII.
Academic Press, New York, 251 p.
Kramer, P.J. 1983. Plant and soil water relationships. Academic Press,
New York, 483 p.
Långström, B. and C. Hellqvist. 1991. Effects of different pruning
regimes on growth and sapwood area of Scots pine. For. Ecol.
Manage. 44:239--254.
Larson, P.R. 1976. The leaf--cambium relation and some prospects for
genetic improvement. In Tree Physiology and Yield Improvement.
Eds. M.G.R. Cannell and F.T. Last. Academic Press, London,
pp 261--282.
Lim, M.T. and J.E. Cousens. 1986. The internal transfer of nutrients in
a Scots pine stand. I. Biomass components, current growth and their
nutrient content. Forestry 59:1--16.
Little, C.H.A. and B. Sundberg. 1990. Tracheid production in response
to indole-3-acetic acid varies with internode age in Pinus sylvestris
stems. Trees 5:101--106.
Little, C.H.A., B. Sundberg and A. Ericsson. 1990. Induction of
acropetal 14C-photosynthate transport and radial growth by indole3-acetic acid in Pinus sylvestris shoots. Tree Physiol. 6:177--189.
Long, J.N. and F.W. Smith. 1988. Leaf area--sapwood area relations of
lodgepole pine as influenced by stand density and site index. Can.
J. For. Res. 18:247--250.
Makela, A. 1986. Implications of the pipe model theory on dry matter
partitioning and height growth in trees. J. Theor. Biol. 123:103-120.
Malkonen, E. 1974. Annual primary production and nutrient cycle in
some Scots pine stands. Comm. Inst. For. Fenn. 84:1--87.
Margolis, H.A., R.R. Gagnon, D. Pothier and M. Pineau. 1988. The
adjustment of growth, sapwood area, heartwood area and saturated
sapwood permeability of balsam fir after different intensities of
pruning. Can. J. For. Res. 18:723--727.
Monteith, J.L. and M.H. Unsworth. 1990. Principles of environmental
physics. Edward Arnold, London, 291 p.
Ovington, J.D. 1959. Mineral content of plantations of Pinus sylvestris
L.. Ann. Bot. 23:75--88.
Pothier, D. and H.A. Margolis. 1991. Analysis of growth and light
interception of balsam fir and white birch saplings following precommercial thinning. Ann. Sci. For. 48:123--132.
Pothier, D., H.A. Margolis, J. Poliquin and R.H. Waring. 1989. Patterns of change of saturated sapwood permeability and sapwood
conductance with stand development. Can. J. For. Res. 19:432--439.
Roberts, J. 1977. The use of tree-cutting technique in the study of the
water relations of mature Pinus sylvestris L. J. Exp. Bot. 28:751-767.
Robichaud, E. and I.R. Methven. 1992. The applicability of the pipe
model theory for the prediction of foliage biomass in trees from
natural, untreated black spruce stands. Can. J. For. Res. 22:1118-1123.
Sandford, A.P. and P.G. Jarvis. 1986. Stomatal responses to humidity
in selected conifers. Tree Physiol. 2:89--103.
Schulze, E.-D. 1986. Whole-plant responses to drought. Aust. J. Plant
Physiol. 13:127--141.
Shain, L. 1967. Resistance of sapwood in stems of loblolly pine to
infection by Fomes annosus. Phytopathology 57:1034--1045.
Siau, J.F. 1984. Transport processes in wood. Springer-Verlag, Berlin,
281 p.

10

MENCUCCINI AND GRACE

Smith, R.B., R.H. Waring and D.A. Perry. 1981. Interpreting foliar
analysis from Douglas-fir as weight per unit leaf area. Can. J. For.
Res. 11:593--598.
Snedecor, G.W. and W.G. Cochran. 1967. Statistical methods. The
Iowa State University Press, Ames, Iowa, 593 p.
Stephens, G.R. 1969. Productivity of red pine. I. Foliage distribution
in tree crowns and stand canopy. Agric. Meteorol. 6:275--282.
Stewart, J.B. 1988. Modelling surface conductance of pine forest.
Agric. For. Meteorol. 43:19--35.
Sundberg, B., A. Ericsson, C.H.A. Little, T. Nasholm and R. Gref.
1993. The relationship between crown size and ring width in Pinus
sylvestris L. stems: dependence on indole-3-acetic acid, carbohydrates and nitrogen in the cambial region. Tree Physiol. 12:347-362.
Tan, C.S. and T.A. Black. 1976. Factors affecting the canopy resistance 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.

Valentine, H.T. 1985. Tree growth models: derivation employing the
pipe-model theory. J. Theor. Biol. 117:579--585.
Waring, R.H., H.L. Gholz, C.C. Grier and M.L. Plummer. 1977.
Evaluating stem conducting tissue as an estimator of leaf area in
four woody angiosperms. Can. J. Bot. 55:1474--1477.
Whitehead, D. 1978. The estimation of foliage area from sapwood
basal area in Scots pine. Forestry 51:35--47.
Whitehead, D. and P.G. Jarvis. 1981. Coniferous forests and plantations. In Water Deficits and Plant Growth. Vol. VI. Ed. T.T. Kozlowski. Academic Press, New York, pp 49--152.
Whitehead, D., W.R.N. Edwards and P.G. Jarvis. 1984a. Conducting
sapwood area, foliage area, and permeability in mature trees of
Picea sitchensis and Pinus contorta. Can. J. For. Res. 14:940--947.
Whitehead, D., P.G. Jarvis and R.H. Waring. 1984b. Stomatal conductance, transpiration and resistance to water uptake in a Pinus
sylvestris spacing experiment. Can. J. For. Res. 14:692--700.
Zimmermann, M.H. 1983. Xylem structure and the ascent of sap.
Springer-Verlag, Berlin, 143 p.