Tree Physiology Advance Access published May 22, 2016

Tree Physiology 00, 113

doi:10.1093/treephys/tpw041

Research paper

Branch age and light conditions determine leaf-area-specific

conductivity in current shoots of Scots pine
Leila Grnlund1,2, Teemu Hltt1 and Annikki Mkel1
1Department

of Forest Sciences, University of Helsinki, Post Office Box 27, Helsinki FI-00014, Finland; 2Corresponding author (leila.gronlund@helsinki.fi)

Shoot size and other shoot properties more or less follow the availability of light, but there is also evidence that the topological
position in a tree crown has an influence on shoot development. Whether the hydraulic properties of new shoots are more regulated by the light or the position affects the shoot acclimation to changing light conditions and thereby to changing evaporative
demand. We investigated the leaf-area-specific conductivity (and its components sapwood-specific conductivity and Huber value)
of the current-year shoots of Scots pine (Pinus sylvestris L.) in relation to light environment and topological position in three
different tree classes. The light environment was quantified in terms of simulated transpiration and the topological position was
quantified by parent branch age. Sample shoot measurements included length, basal and tip diameter, hydraulic conductivity of
the shoot, tracheid area and density, and specific leaf area. In our results, the leaf-area-specific conductivity of new shoots
declined with parent branch age and increased with simulated transpiration rate of the shoot. The relation to transpiration
demand seemed more decisive, since it gave higher R2 values than branch age and explained the differences between the tree
classes. The trend of leaf-area-specific conductivity with simulated transpiration was closely related to Huber value, whereas the
trend of leaf-area-specific conductivity with parent branch age was related to a similar trend in sapwood-specific conductivity.
Keywords: leaf area, sapwood, shoot structure, tree structure.

Introduction
In the adaptive geometry of trees, the size and properties of
new shoots are crucial for the acclimation of the crown, not only
to the prevailing environment but also for the expected future
conditions modified by neighbours. While shoot size and many
shoot properties, such as specific leaf area (SLA), stomatal size
and density, nitrogen content, and shoot and leaf angle, have
been demonstrated to follow the availability of light to the shoot
(Ishii etal. 2007), the allocation of growth between new buds
has also been shown to depend on the topological position of
the bud in the crown (Perttunen etal. 1996, Prusinkiewicz etal.
1996, de Reffye etal. 1997, Kurth and Sloboda 1997). Goulet
etal. (2000) suggested that the effect of position could be
explained by a vigour index that quantifies the relative reduction of branch cross-sectional area along the branch axes from

the stem base to the shoot. Nikinmaa etal. (2003) showed

through simulations with a three-dimensional structuralfunctional model that not light alone, but light and vigour index
together predicted shoot size distributions that led to realistic
crown shapes in Scots pine (Pinus sylvestris L.).
Shoot size may have further implications on shoot properties
through allometric relationships and morphological constraints
(Takenaka 1997, 2000, Osada 2006). For example, the allocation of shoot biomass to foliage and wood has been found to
depend strongly on the age of the parent branch (Suzuki 2003).
Mkel etal. (1980) found that while 45% of leader shoot biomass in young Scots pine trees consisted of wood, the woody
mass of shoots in 20-year-old branches was only 2% of the
total shoot mass. The larger proportion of wood in the shoots
near the top may be an adaptation that increases the mechanical

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Received October 19, 2015; accepted April 17, 2016; handling Editor Frederick Meinzer

2 Grnlund etal.

Q = K L AL

P
= EL AL
L

(1)

where AL (m2) is leaf area and P/L (Pam1) is the pressure

wers 1991). Because the
gradient of the shoot (Tyree and E
pressure gradient must likely have an upper limit to maintain the
hydraulic balance of the shoot, a means for a shoot to acclimate
to an increasing evaporative demand would be to increase KL
when the demand for EL increases with increasing exposure to
light. Leaf-area-specific conductivity can be expressed in terms
of sapwood-area-specific conductivity KS (m2Pa1s1) and the
Huber value Hv as follows:
Tree Physiology Volume 00, 2016

KL = K S

AS
= K S Hv
AL

(2)

where AS (m2) is xylem cross-sectional area. This shows that the

leaf-area-specific conductivity will increase if either the sapwood-specific conductivity increases or the Huber value
increases. The former is related to the tracheid lumen area, tracheid density and pit structure in the shoot, while the latter is
determined by shoot allometry.
Sapwood-specific conductivity of the shoot can be calculated
based on water flow measurements through the shoot. According to Darcys law (Siau 1984), the hydraulic conductivity of a
porous medium can be estimated from the measured water flow
rate, the cross-sectional area of the sample and the pressure
drop over a given distance. Sapwood-specific conductivity can
also be estimated by utilizing the information about the tracheid
properties of the shoot. An equation has been derived from the
HagenPoiseuille law that gives the conductivity as a function of
tracheid number and diameter (Tyree and Ewers 1991). However, this theoretical value of hydraulic conductivity does not
take into account the effect of pit membrane resistance or possible embolism (Tyree and Ewers 1991, Domec etal. 2006,
Renninger etal. 2006). The predicted values for hydraulic conductivity can thus be expected to be higher than those based on
hydraulic conductivity measurements. Especially, the contribution of pit membranes to hydraulic conductivity is large and also
variable since pit membrane resistance has been found to vary
between 20 and 90% in conifers (Choat etal. 2008, Schulte
etal. 2015).
The objective of this study is to analyse the hydraulic properties of the current-year shoots at the tips of the branches in
Scots pine (Pinus sylvestris L.) in relation to local environment,
quantified in terms of simulated transpiration, and topological
position in the crown, quantified by branch age. Transpiration
drives the water flow in the shoot (Eq. 1) and is also closely
related to irradiance through its effect on stomatal control (Hari
etal. 2000, Medlyn etal. 2011). Branch age reflects the number of bifurcations along the water transport pathway, which is
an important factor in the vigour index found to characterize
the distribution of shoot growth (Nikinmaa et al. 2003). In
order to separate environmental variation from branch age, we
consider dominant and suppressed trees in a homogenous
part of a stand, as well as trees growing next to a large gap in
the same stand. We hypothesize that KL decreases with the age
of the branch axis regardless of the light exposure of the
crown, and that it increases as a function of increasing evaporative demand created by light availability. In particular, we will
investigate how these dependences, if detected, can be attributed to either sapwood-specific conductivity, KS, or Huber
value, Hv. Measuring sapwood-specific conductivity in two
ways also enables us to compare the theoretical against the
actual values.

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strength of the shoots that will support the future branch axes,
but such allometric variation may also be of significance for the
physiological functioning of the shoots. Particularly, the woodto-foliage ratio is important for the hydraulic properties of the
shoots (Tyree and Ewers 1991).
Hydraulic properties of branches vary within the crown so that
the conductivity of the branch axes decreases from the top down
at least in relatively young individuals (Zimmermann 1983, Tyree
and Ewers 1991, Protz etal. 2000, Sellin and Kupper 2004).
The same trend has been observed also in broadleaved species,
both in smaller and taller trees (Clearwater and Meinzer 2001,
Lemoine etal. 2002, Sellin etal. 2013). Zimmermann (1983)
suggested that this pattern could contribute to the apical control
in trees: as the hydraulic conductivity of branch axes decreases
with the age of the branch, this directs the water transport
upwards, thus allowing for more water and sugars to be used in
the growth of the upper shoots. This would also suggest that in
older trees where apical control is weakened, hydraulic conductivity of branch axes and shoots would no longer follow the same
pattern. Indeed, results from the tallest giant redwoods provide
evidence that growth as well as the hydraulic conductivity of new
shoots increases in the opposite direction, i.e., from top down
(Koch etal. 2004), although it is not clear whether this is caused
by hormonal changes in apical control or more directly by heightrelated problems of water transport.
If the hydraulic properties of new shoots were related to
crown structure, we would expect a dependence of hydraulic
conductivity on the topological position of the shoot in the
crown, regardless of the local environment of the shoot. On the
other hand, if the hydraulics were more directly regulated by
thelocal environment, then the light conditions of the shoot and
its immediate evaporative demand would explain shoot hydraulic
properties more readily than shoot position.
In order to analyse the hydraulic properties and their relationship to the environment quantitatively, we consider the water flux
through a shoot (Q, m3s1) in relation to the leaf-area-specific
conductivity (KL, m2Pa1s1) of the shoot on one hand, and the
leaf-area-specific transpiration rate (EL, m3m2s1), on the other
hand:

Leaf-area-specific conductivity in current shoots3

Materials and methods

Sampling protocol

Hydraulic conductivity measurements

First the hydraulic conductivity of the sample shoots was estimated by measuring the water flow rate through the shoot sample by applying constant head of water (e.g., Melcher etal.
2012). We used a solution of distilled water and KCl
(0.1moll1) and the movement of water was driven by gravity.
An approximately 35cm long piece was cut from the base
of the sample shoot and covered by Teflon tape while the sample was under water to prevent air entry into the sample. Next
the shoot sample was placed tightly into the head of the rubber
tube, which was connected to a water reservoir 1m above the

Table2. Measured tracheid properties of the sample trees (meanstandard deviation). Tree status: S, suppressed trees; D, dominant trees; O,
open-grown trees. Significance test is from one-way analysis of variance
(ANOVA).
Tree number and status

Tracheid lumen
area (m2)

Tracheid density
(103m2)

1S
3S
5S
Group average
2D
4D
6D
Group average
7O
8O
Group average
Significance of the group
average at P=0.05

80.536.2
89.734.8
90.434.3
87.735.2
79.838.9
94.141.9
79.731.0
84.638.0
101.841.8
103.441.1
102.541.5
No

6.11.2
5.60.8
5.30.9
5.61.0
6.31.8
5.61.6
5.91.2
6.01.6
4.71.0
5.00.9
4.90.9
Yes

Table1. Sample tree measurements, sampling of the current-year shoots (minimum and maximum height and parent branch age of sample shoots)
and sample shoot measurements (meanstandard deviation). Tree status: S, suppressed trees; D, dominant trees; O, open-grown trees. DBH, diameter at breast height.
Tree
number
and status

DBH
(cm)

Height
(m)

Crown
ratio (%)

Tree age
(years)

Shoot
height
(m)

Branch
age
(years)

Shoot length
(mm)

Shoot tip
diameter (mm,
with bark)

Shoot basal
diameter (mm,
with bark)

Shoot basal
diameter (mm,
without bark)

1S
3S
5S
2D
4D
6D
7O
8O

8.5
7.6
8.1
14.9
14.6
14.5
14.6
11.3

10.0
9.5
11.0
14.5
14.0
14.0
10.0
9.8

40.0
36.8
40.9
58.6
50.0
50.0
77.5
66.7

28
28
31
33
34
34
29
27

6.09.0
6.09.0
6.59.0
6.011.0
7.011.0
7.511.0
2.58.5
4.08.5

412
312
612
817
816
1118
418
414

59.330.8
57.521.1
71.127.1
55.232.4
95.842.9
50.623.1
132.9104.5
131.078.9

2.70.5
2.30.3
2.30.5
2.70.9
3.80.7
3.00.6
3.81.4
3.41.2

2.90.8
2.80.7
2.70.4
3.01.0
4.10.8
3.30.7
4.31.7
4.11.4

1.10.4
1.00.3
1.30.3
1.20.4
1.60.8
1.30.3
2.31.1
2.31.0

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The measurements were taken in a 30-year-old even-aged

P. sylvestris stand with stocking density 2100ha1 in southwest
Finland, Hyytil, Juupajoki (6150N, 2418 E) in August
2012. A 1010m2 plot was formed and all the trees were tallied for breast height diameter. Three dominant and suppressed
trees as well as two trees growing on stand edge (subsequently
called open-grown) were chosen as sample trees. Dominant
trees were defined as trees growing in a normal wooded light
environment, and suppressed trees were defined as trees growing in a shady environment with tree tops clearly below the
dominant tree tops. All eight sample trees were measured for
diameter at breast height, height, age, and crown width and
length (Table1).
Five to six current-year shoots were cut from different heights
from the south side of each sample tree using pruning shears
(Table1). The compass angle was selected to coincide with the
gap direction of the open-grown trees. Each measurement day,
the sample shoots of one sample tree were cut in the morning.
A half-metre long piece was cut from the branch and placed
immediately in a water bucket. The branch parts were taken to
the laboratory, and shoots at the tips of the branches were measured for length, basal and tip diameter (Table1), SLA, tracheid
area and density (Table2), and hydraulic conductivity.

shoot sample. The Teflon tape prevented water from flowing

between the tube and the sample. The tape also minimized the
water flow through dwarf shoots. The water, drained through the
sample, was collected into an Erlenmeyer bottle and weighed
every 15min over 2h. A piece of cling film was used to cover
the mouth of the Erlenmeyer between the weighings to minimize
evaporation. The correlation between time and the amount of
water in the Erlenmeyer was almost perfectly linear, suggesting
that no plugging of the xylem conduits was occurring during the
measurements (see Figure S1 available as Supplementary Data
at Tree Physiology Online). We varied the measurement order of
shoots to avoid possible systematic error related to the time
between cutting and hydraulic conductivity measurement, such
that the measurements were done from top to bottom at least in
one sample tree and the opposite direction at least in one tree.
To minimize the time spent in the bucket, the hydraulic conductivity measurements were done partly simultaneously.
Finally, the results from the hydraulic conductivity measurements were used to estimate measured sapwood-specific

4 Grnlund etal.
hydraulic conductivity KS (m2Pa1s1, where Pa=kgm1s2) of
the sample shoots (Siau 1984):
KS =

Ql
gha

(3)
(m3s1),

where Q is the measured water flow rate

l is length of
the sample (m), is the density of water (1000kgm3), g is
the standard gravity (9.81ms2), h is the height of the water
column (m) and a is the xylem cross-sectional area of the base
of the sample (m2). Water flow rate Q was the average of eight
measurements at 15-min intervals over 2h.

Measurement of tracheid properties for

theoreticalhydraulic conductivity

1
4

j =1

Aij2 /

1
i
A j 8 0.001

Tree Physiology Volume 00, 2016

Five needles of each sample shoot were randomly chosen for

SLA measurements. Length, width and thickness of the selected
needles were measured by caliper, and the needles were dried
in the oven (105C, 24h). The dry mass of each needle was
determined. For SLA calculations, the surface area of the sample
needles, aL (cm2), was estimated using the half-cylinder method
(Lin etal. 2002):

(4)

aL = (2rn + rn )ln

(5)

where r n (cm) is the needle radius (radius is the average of the

measured thickness and width divided by two) and ln (cm) is the
measured needle length. When the summed needle area of
thefive needles was divided by the summed dry mass, we got
the SLA (cm2g1) of the sample shoot. Shoot needle area
wasthen calculated from needle mass and SLA.
Because we did not measure needle mass in the shoots sampled in 2012, these traits were estimated using a model derived
from the measurements in 2013. A new sample of shoots was
collected in August 2013 in the same site for determining shoot
allometry. Eight new sample trees were chosen. These trees also
represented three different tree classes and were comparable to
the first set of sample trees by their diameter. Five to six currentyear shoots per tree were chosen. From each shoot, all of the
needles were plucked out and needle mass was weighed both
fresh and dry (105C, 24h). The same procedure was carried
out for the woody part of the shoot.
We estimated an allometric model between needle mass (Wn)
and woody mass (Ww) in the shoots separately for each dominance class:

Wn = Ww

(6)

where and are parameters. This model gave good fits to data
(see Figure S2 available as Supplementary Data at Tree Physiology
Online). The foliage mass of the 2012 shoots was estimated
using this equation, where the independent variable, Ww, was
estimated from shoot volume and density. Shoot volume was
calculated as a cut cone defined by its basal and tip diameters
and length, and density was retrieved from the literature
(K rkkinen 1976; dry-fresh density: 424kgm3).
The estimated AL allows us to view the calculated conductivity
values as leaf-area specific:

KL = K S

AS
AL

(7)

where K S is the sapwood-specific conductivity value

(m2Pa1s1), AS is the xylem cross-sectional area of the sample

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K S =

Leaf-area measurements

Next the theoretical hydraulic conductivity of the sample shoots

was calculated from the measured tracheid properties. For calculating tracheid area and density, a 1-cm-long piece was cut from
each sample shoot (the base of the hydraulic conductivity measurement sample) and stored in the freezer. Later, microscopic
sections were prepared from each of these small pieces by using
ice microtome Leica CM 3050 S (Leica Biosystems, Wetzlar, Germany). This device freezes the piece of wood on the adapter.
Water is dripped on to the sample in cold environment until it is
totally covered by ice. The adapter is then mounted on the microtome and the desired thickness of the sections (here 20m) is
set. When a couple of unbroken sections have been successfully
transferred on the object glass, those are dried by using an alcohol
series and finally coloured with Safranin. Preparations were made
permanent using Canadian balsam. After a few days of drying, all
the sections were checked with a microscope and the best one
from each sample shoot was selected for detailed calculations.
Each section was photographed with an Olympus ALTRA 20
colour camera attached to an Olympus CX 31 microscope (Olympus Optical Co., Tokyo, Japan). One overall photo was taken with
40 magnification. The section was divided into four 90 sectors
and one sample image was taken of each sector with 400 magnification. Sample images covered 5% of the total sector area.
Average tracheid density and area values were calculated from
these sample images. From each image, every single tracheid
was digitized to get the lumen area and the number of tracheids
in the picture frame. The cross section values of density and area
were calculated as averages over these four sample images. All
the calculations were made using the image manipulation program ImagePro (Media Cybernetics, Inc., Rockville, MD, USA).
The theoretical value of the sapwood-area-specific hydraulic
conductivity, denoted as K S (m2Pa1s1), was estimated from
the sample measurements of tracheid area and sample area
(Tyree and Ewers 1991):
4

where Aj (m2) is the area of sample j and Aij (m2) is the lumen area
of the ith tracheid in the sample and 0.001 is the dynamic viscosity of water (Pas). All tracheids were counted as conducting.

Leaf-area-specific conductivity in current shoots5

shoot (m2) and AL is the estimated needle area of the shoot
(m2). Xylem cross-sectional area was calculated from the measured shoot basal diameter without bark.

Simulated transpiration

Statistical methods
We tested the hypotheses of the study by examining the variability
of KL and its components KS and Hv with whorl age and estimated

y i = axi + b + i

y i = axi + b + b1d1i + b2d2i + i

(8)

(9)

y i = axi + b + a1d1i xi + a2d2i xi + b1d1i + b2d2i + i (10)

where i denotes measurement; y and x are the dependent and

independent variables, respectively; a, a1 and a2 are slope
parameters; b, b1 and b2 are intercept parameters; d1 and d2 are
dummy variables; and i is residual error. The dummy variable d1
takes values d1i=1 for measurements i from the dominant tree
class, while d1i=0 otherwise. Similarly, d2i=1 for measurements
from the suppressed tree class and d2i=0 otherwise.
Equation (8) tested the strength of the linear regression
between the two variables without separating the tree classes.
Equation (9) tested whether the intercept parameter of suppressed or dominant trees differed from that of the open-grown
trees. In Eq. (10), both the intercept and slope parameters were
tested against those of the open-grown trees.
All statistical analyses were made using the stats package of R
software (R Development Core Team 2014). The significance of
the regressions was assessed using the F-test and the goodness
of fit is reported in terms of R2. The significance of the components of the regression equation was analysed with the t-test. We
took P<0.001 to indicate highly significant, P<0.01 significant
and P<0.05 almost significant regressions and parameters. All
three regression equations were formed for each variable and the
one with the best fit was selected for further analysis.

Results
Shoot position and environment
Photosynthetically active radiation (molm2s1) and transpiration (molm2s1) values were estimated in five different relative canopy heights for each tree class (see Figure S3 available
as Supplementary Data at Tree Physiology Online). The displayed results were calculated as an average of the half hourly
values between 1.45 and 3.15 p.m. on 31 August. At the bottom of the living canopy, the simulated PAR values were
8molm2s1 in suppressed trees, 46molm2s1 in dominant trees and 192molm2s1 in open-grown trees. The corresponding values at the top of the canopy were 302, 621 and
619. Measured PAR values under the canopy of the suppressed
and dominant trees were 52molm2s1 and in the open
place next to the open-grown trees 178molm2s1. Date
and time were the same as in SPP simulations. The vertical

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We used a process model, SPP (Stand Photosynthesis Program)

(Mkel etal. 2006), to estimate the vertical distribution of photosynthetically active radiation (PAR) and the leaf-area-specific
evapotranspiration rate, EL, in model stands defined by the measurements. In SPP, the tree stand consists of different tree size
classes and ground vegetation. Within one size class, all the trees
are identical and distributed randomly. The information needed to
describe size classes (crown size, tree height, stem number and
SLA) was obtained from the field measurements. Crown shape is
assumed to be ellipsoid and crowns are filled with randomly distributed and spherically orientated shoots. Weather data were
obtained from the SMEAR II station approximately half a kilometre
away. Based on weather data, SPP calculates sun elevation and
the attenuation of direct and diffuse radiation through the canopy
(Oker-Blom etal. 1989). Direct radiation arrives at a given zenith
angle and diffuse radiation is assumed to come equally from all
directions. Momentary attenuated radiation at a certain point
inside a crown is used as an input for shoot level photosynthesis.
Transpiration is calculated as a function of stomatal conductance,
saturation deficit of water vapour and the ratio of diffusivity of
water relative to carbon dioxide. Stomatal conductance is based
on the so-called optimality model (Hari etal. 2000) and, in
accordance with empirical evidence (Medlyn etal. 2011), is
strongly controlled by PAR. The calculations are done at a half
hourly time step. Shoot level results can be integrated over the
whole crown and canopy.
We simulated two stand configurations with SPP. One consisted
of three size classes including the dominant, suppressed and an
intermediate class from the measured stand, while the other
included only one size class at a low density (700ha1) to imitate
the open-grown trees of the study. We used SPP for calculating
the vertical distribution of PAR and EL (both in molm2s1 per
all-sided leaf area) averaged over August 2012, including day
and night hours. Use of mean daily maximum values would have
resulted in approximately fivefold higher values.
For comparison, the light conditions under the tree canopy
were also evaluated by LI-190 Quantum sensor (LI-COR, Lincoln, Nebraska, USA), which measures PAR. Photosynthetically
active radiation was measured on the last day of August during
a heavily overcast afternoon. A total of 25 under-canopy measurements were taken across a grid covering the main measurement plot, and five measurements were made in the gap next to
the open-grown trees.

transpiration using linear regression analysis. We similarly

analysed the structural traits underlying the dependence of KS and
Hv on the explanatory variables, including tracheid lumen area and
density, and SLA. We tested for differences between tree classes
by means of dummy variables for the intercept and slope of the
regressions. We formed regression equations of the form

6 Grnlund etal.
istribution of simulated transpiration was similar to simulated
d
PAR. These calculated curves were used to estimate the transpiration rate at the relative height of each tree, relative to the total
height of the canopy of the corresponding tree class.
Because our objective was to analyse the dependence of
shoot conductivity in relation to the simulated transpiration
demand as well as branch age, it is interesting to see how these
are related to each other in the sample trees. In each tree class,
there was a strong linear relationship between the simulated
transpiration and the age of the branch the measured shoot was
attached to, but the levels of transpiration clearly differed

between the tree classes. As expected, the simulated transpiration

was largest in the open-grown trees and smallest in the suppressed trees, while the shoots of the dominant trees ranged
from relatively high transpiration levels at the top to low levels at
the bottom of the canopy (Figure1).

Figure1. Relationship between age of the branch the shoot is attached

to and simulated shoot transpiration (molm2s1). Transpiration values
are averaged over August, including day and night hours. See Table3 for
statistics.

Huber value and SLA

Tracheid properties and sapwood-specific conductivity

The Huber value showed no dependence on branch age, but the

mean value (intercept) of the suppressed trees differed significantly

Table3. Summary of the statistical tests. The symbols are as in Eqs (810): the slope parameters a, a1 and a2 and the intercept parameters b, b1 and
b2 are for open-grown, dominant and suppressed trees, respectively. The regression with the lowest P-value of the three alternatives is reported, and
the significance of the coefficients being non-zero are given (***P<0.001, **P<0.01, *P<0.05). There were total of 15 sample shoots in suppressed, 16 in dominant and 10 in open-grown trees. K S (sapwood specific) and K L (leaf-area specific) are the theoretical conductivity values (based
on tracheid properties). KS and KL are the measured conductivity values (based on hydraulic conductivity measurements).
y

a1

a2

b1

b2

R2

Transpiration
Tracheid lumen area
Tracheid lumen area
Tracheid density
Tracheid density

Branch age
Branch age
Transpiration
Branch age
Transpiration
Branch age
Transpiration
Branch age
Transpiration
Branch age
Transpiration
Branch age
Transpiration
Branch age
Transpiration
Branch age
Transpiration

3.59
5.02
0.99
0.13
0.05
1.31010
2.411011
1.641011
3.901012
4.691007
7.751007
1.16
0.68
1.071014
2.311015
1.391015
4.411016

102.15
154.10
38.08
3.53
8.34
3.531009
6.161010
3.491010
7.421011
1.091004
5.241005
105.50
162.05
3.391013
8.331014
3.341014
9.521015

1.91*

0.29***

4.61***

1.78*

0.08

2.47

7.55
7.41
5.59
2.81**
0.12
8.081011
2.161010
2.461010**
3.061010**
1.241005

50.92**
6.54
2.281014

1.871014**
2.641014***

72.86***
24.75***
35.38***
0.36
1.92**
5.561010***
9.281010**
2.161010*
4.451010**
4.901005***

35.26**
18.67*
1.341013***

3.061015
2.791014**

0.92
0.72
0.57
0.70
0.56
0.64
0.44
0.22
0.23
0.39
0.38
0.85
0.78
0.43
0.47
0.17
0.27

K S
K S
KS
KS
Huber value
Huber value
SLA
SLA
KL
KL
KL
KL

Tree Physiology Volume 00, 2016

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The mean tracheid lumen area of the sample trees varied from
79.7 to 103.4m2 and mean tracheid density varied from 4.7 to
6.3103m2 (Table2). The average lumen area was largest
and average cell density was lowest in the open-grown trees, but
differences between suppressed and dominant trees were small.
Since tracheid lumen area and tracheid density were correlating with branch age and simulated transpiration (Table3), it was
expected that also theoretical sapwood-specific conductivity
( K S , m2Pa1s1) would correlate with those variables (Figure2,
Table3). Especially tracheid lumen area has a big influence, and
the correlation was stronger with branch age than with simulated
transpiration.
When the sapwood-specific conductivity values based on water
flux measurements (KS, m2Pa1s1) were plotted against branch
age and simulated transpiration, there was only a weak correlation
(P<0.05) in both cases (Figure2c and d, Table3). There were
differences between tree classes caused by the varying mean
value. Divergent sapwood-specific conductivity values were also
compared by using average values of tree classes (Table4).

Leaf-area-specific conductivity in current shoots7

from that of the open-grown trees (Table3). The values for the
dominant trees seemed to decline somewhat with branch age, but
the dependence was not statistically significant. On the other hand,
there was a weak but statistically significant correlation between
Huber value and simulated transpiration, which did not differ
between tree classes (Figure3a, Table3).
The fit between SLA and branch age was statistically significant, but only when all tree classes had separate coefficients
(Table3). In contrast, all tree classes fell tightly on the same
curve when SLA was plotted against simulated transpiration.
However, this curve appeared to be non-linear, such that the
linear statistical fit rendered the suppressed tree intercept statistically significantly different from the rest (Figure3b, Table3).

Leaf-area-specific conductivity
Leaf-area-specific conductivity calculated from the K S values
decreased with branch age, but the pattern was dependent on

the tree class. The values in the suppressed class were smaller
than and statistically significantly different from the dominant
and open-grown classes, and the dominant class showed a
steeper decline with age than the others, although it did not differ statistically significantly from the open-grown class
(Figure4a, Table3). On the other hand, the dependence of the
leaf-area-specific conductivity on simulated transpiration seemed
more decisive, since it gave higher R2 values than branch age
(Table3). Simulated transpiration also explained those differences between the suppressed, dominant and open-grown trees
that branch age did not (Figure4b).
Leaf-area-specific conductivity values were also calculated
from the measured sapwood-specific conductivity (KS) values.
There was no correlation with branch age, but the mean value
of dominant trees differed significantly from that of the opengrown trees (Figure4c, Table3). However, a moderate correlation was found between conductivity and simulated

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Figure2. Theoretical and measured sapwood-specific conductivity (m2Pa1s1) as a function of branch age (a and c) and simulated transpiration
(molm2s1) (b and d). Transpiration values are averaged over August, including day and night hours. Statistically significant regression lines are
shown (P<0.05). See Table3 for statistics.

5.610051.31005
1.010045.21005
1.110041.11005
Yes
Measured

2.510148.51015
3.510142.21014
1.910148.61015
No
1.110134.01014
1.710138.61014
2.310137.51014
Yes

Theoretical
Measured

4.310101.61010
3.910102.61010
1.810107.61011
Yes

Theoretical

1.910094.81010
1.810095.61010
2.210096.61010
No
Suppressed trees
Dominant trees
Open-grown trees
Significance of the tree class average at P=0.05

Huber value
Leaf-area-specific conductivity (m2Pa1s1)
Sapwood-specific conductivity (m2Pa1s1)

transpiration when the mean values were allowed to differ

between tree classes (Figure4d, Table3). Note that the ratio
of the transpiration rate to leaf-area-specific hydraulic conductivity represents the pressure loss gradient of the shoot (see
Eq. 1). The increase in hydraulic conductivity with increasing
transpiration rate thus restrains the pressure loss from increasing linearly with increasing transpiration rate. However, the
adaptation of conductivity to transpiration is not complete
since the pressure gradient (calculated from Figure 4, not
shown) increases with increasing transpirational demand. For
example, the pressure gradient calculated from Figure4a is
approximately three times larger at a transpiration rate of
70molm2s1 in comparison with at a transpiration rate of
10molm2s1 (not shown). Also, the open-grown trees have
a lower measured conductivity (Figure4b) for a given transpiration rate indicating a larger pressure loss in comparison with
the dominant and suppressed trees. For example, the calculated
pressure gradient for the open-grown tree is approximately

Tree Physiology Volume 00, 2016

Figure3. Huber value (a) and SLA (b) as a function of simulated transpiration (molm2s1). Transpiration values are averaged over August,
including day and night hours. Statistically significant regression lines are
shown (P<0.05). See Table3 for statistics.

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Table4. Sapwood-specific conductivity, leaf-area-specific conductivity and Huber value of tree classes (meanstandard deviation). Theoretical values are based on tracheid properties and measured values are based on hydraulic conductivity measurements. Significance test is from one-way ANOVA.

8 Grnlund etal.

Leaf-area-specific conductivity in current shoots9

four times larger in comparison with the dominant and suppressed trees at an intermediate transpiration rate of
50molm2s1 (not shown).

Discussion
The study provided support for our hypotheses that leaf-areaspecific conductivity of new shoots declines with parent branch
age and increases with simulated transpiration rate of the shoot,
related to shoot light conditions driving transpiration.
The trend with parent branch age in the leaf-area-specific conductivity of shoots (calculated from theoretical K S values) was
related to a similar trend in sapwood-specific conductivity K S ,
which was strongly correlated with parent branch age and only
showed a weak relationship with the environmentally determined
simulated transpiration (Figure2). Similar trends were found in

tracheid lumen area and tracheid density, which largely

determined the theoretical sapwood-specific conductivity.
However, the mean value of K S in suppressed trees tended to
differ from the other tree classes, and the slope of tracheid
density against parent branch age was steepest in the dominant trees. These properties were, therefore, not totally unaffected by tree class.
It was interesting that a pattern similar to the theoretical sapwood-specific conductivity could be found in shoot length when
plotted against branch age (Figure5a). This was indicative of
the existence of a strong, tree-class-independent relationship
between shoot length and tracheid lumen area (Figure 5b),
which will be further reflected onto a dependence of sapwoodspecific conductivity on shoot length. Also, earlier studies found
that xylem conduit diameter is better explained with stem length
than environmental conditions (e.g., Olson and Rosell 2013,

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Figure4. Theoretical and measured leaf-area-specific conductivity (m2Pa1s1) as a function of branch age (a and c) and simulated transpiration
(molm2s1) (b and d). Transpiration values are averaged over August, including day and night hours. Statistically significant regression lines are
shown (P<0.05). See Table3 for statistics.

10 Grnlund etal.

lson etal. 2014). We could not find any direct comparison of

O
shoot length vs conduit size in the literature. However, in the
longer shoots, the location of tracheids that were examined was
further from shoot apex (i.e., shoot length in our measurements
corresponds to distance from leaf apex), and distance from leaf
apex is known to be a very strong predictor of conduit diameter
(e.g., Petit etal. 2008). As shoot length in a particular parent
branch has been related to both the general availability of
resources to the branch and to the genetically affected topological position of the shoot in the crown (Perttunen etal. 1996,
Kurth and Sloboda 1997, Goulet etal. 2000, Nikinmaa etal.
2003), this suggests that sapwood-specific conductivity is also
affected by these two different factors. Increasing resources,
such as light available to the parent branch, together with position closer to the tree top, would thus improve sapwood-specific
conductivity. This pattern seems to allow for increasing conductivity with increasing transpiration demand in canopy trees. In

Tree Physiology Volume 00, 2016

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Figure5. (a) Shoot length (m) as a function of branch age. R2=0.77.

Suppressed trees: y=0.110.01x. Dominant trees: y=0.200.01x.
Open-grown trees: y=0.300.02x. (b) Tracheid lumen area (m2) as
a function of shoot length (m). R2=0.74 (log-transformed linear regression). All sample trees: y=204.38x0.32. Statistically significant regression lines are shown (P<0.05).

open-grown trees, the trend with branch age is not parallel with
the trend in light conditions. If the trend with branch age was
stronger, this could lead to low sapwood-specific conductance
relative to the transpiration demand in the lower branches of
open-grown trees. Shoot elongation and tracheid growth may be
anatomically and physiologically linked to yield the observed
relationship.
While sapwood-specific conductivity was largely responsible for the parent-branch-age-related trend in the leaf-areaspecific conductivity, the trend in the latter with simulated
transpiration was more closely related to the Huber value,
which did not correlate with parent branch age but had a statistically significant correlation with simulated transpiration. An
even stronger correlation with simulated transpiration was
found in SLA. If sapwood-area-specific conductivity was constrained by shoot size as discussed above, the flexibility of
SLA seemed to provide a means for more complete acclimation of leaf-area-specific conductivity to either within-canopy
or open conditions.
As a conclusion, it seems that when shoots needed to acclimate their structure to an increasing transpiration demand, it
happened by changing specific needle area and Huber value.
Hence photosynthesis could be greater, and water transport still
sufficient, when shoots were growing in good light.
The conductivity values of the lower shoots of open-grown
trees were of the same order of magnitude as those of the
upper shoots of suppressed trees. This suggests that despite
their better light position, open-grown trees were still somewhat controlled by shoot size that was smaller on lower
branches. This may be related to evolutionary adaptation to
inside-canopy rather than open-grown conditions in young
Scots pine trees.
Comparison between theoretical and measured conductivities
revealed that the difference was largest in the open-grown trees.
This was probably due to the fact that the theoretical hydraulic
conductivities did not include the pit resistance, and that pit
resistance was relatively higher in the open-grown trees in comparison with other tree classes. It has been found that shaded
conifers will compensate for small diameter tracheids by
changes in pit membrane structure making pits more conductive
(e.g., Schoonmaker etal. 2010, Schulte 2012, Hacke 2014,
Schulte etal. 2015), which may also make them more vulnerable to cavitation (Cochard etal. 1999, Schoonmaker etal. 2010,
Hltt etal. 2011, Plavcov etal. 2011). However, this functional link is not as clear in gymnosperms as in angiosperms.
Furthermore, shaded conifers are expected to experience less
negative midday water potentials and lower stomatal conductances than light-grown ones (e.g., Cochard etal. 1999), so
they do not need to be so resistant to cavitation. In contrast,
open-grown conifers have lower pit conductance and better
resistance to cavitation (Hacke 2014), which allows shoots in
good light to operate at lower water potentials. Using Eq. (1)

Leaf-area-specific conductivity in current shoots11

c ircular. Lewis (1992) and Mencuccini etal. (1997) have presented the hydraulic diameter of rectangular tracheids:

dh =

2ab
a+b

(11)

where a and b are the sides of the rectangle.

If this hydraulic diameter had been used in Eq. (4), for example, assuming b/a=1.5, theoretical sapwood-specific conductivity values in each tree class would have been approximately
half of the presented ones. Of course, this does not explain the
differences between tree classes.
Average values of tracheid properties and sapwood-specific
and leaf-area-specific conductivity are more or less affected by
the sampling of the shoots in each tree class. For example, in
suppressed trees, the oldest age classes were missing because
of the lack of living branches in the lowest whorls, while in the
dominant and open-grown trees, the younger age classes were
under-represented because of poor reachability. On average, the
open-grown trees had the highest leaf-area-specific conductivity
based on tracheid properties, followed by dominant and suppressed trees (Table4). The order changed when conductivity
values were based on hydraulic conductivity measurements: the
dominant trees had the highest leaf-area-specific conductivity,
followed by suppressed trees. The open-grown trees had the
lowest average. Other studies made with Pinus sp. show similar
results to those based on tracheid properties: leaf-area-specific
values were higher in open-grown trees compared with understorey or closed-canopy trees (Cochard etal. 1999, Protz etal.
2000, Schoonmaker et al. 2010). Similar data have been
published also for Picea abies (Sellin 2001). Leaf-area-specific
conductivities for branches did not differ between the crown
classes, while conductivities for stems did for the benefit of the
trees growing in better light.
Reid etal. (2003) did not detect any differences between tree
classes, when leaf-area-specific values were compared. Then
again they found some significant differences in sapwood-specific conductivity, as did Protz etal. (2000) and Sellin (2001).
Trees growing in higher light conditions had larger sapwoodspecific conductivity values. In our study, the theoretical average
of sapwood-specific conductivity was highest in the open-grown
trees, with little difference between suppressed and dominant
trees (Table4). In line with previous studies (Protz etal. 2000,
Schoonmaker etal. 2010), the average tracheid lumen area of
open-grown trees seemed higher and tracheid density was
lower than in suppressed and dominant trees (Table2). However, the differences in tracheid lumen area were not quite statistically significant (P=0.057), probably because of the sampling
of the shoots and the lack of data from the oldest branches in
suppressed trees.
Here, we used simulated values of PAR and transpiration to
characterize the relative evaporative demand at the location of

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and the relation in Figure4b, the water potential decrease per

unit length is expected to be higher in light vs shade shoots in
our results. Also, as the shoot length was higher in light branches
in comparison with shaded branches (Figure5a), the total water
potential decrease over the shoot can be expected to be greater
in open-grown trees.
Hacke (2014) concluded that understorey conifers appear
to invest less carbon into torusmargo pits by producing pit
membranes with a more porous but fragile structure, corresponding to relatively efficient transport but increased xylem
vulnerability. The hydraulic architecture model of Hltt etal.
(2011) can be used to interpret this from a carbon gaincost
perspective. Carbon investment into hydraulic structure gives a
larger return in carbon gain by photosynthesis in conditions of
high light. The larger conduits in branches under high light
require thicker conduit walls, which require a larger carbon
investment (Hacke etal. 2001). However, the higher ratio of
transpiration rate to leaf-area-specific hydraulic conductivity in
the light branches translates into lower water potentials in the
light branches (see Eq. 1 and Figure4b). This lower water
potential demands a pit structure, which is more resistant to
cavitation, and therefore, the pit structure is also likely to be
less conductive (e.g., Hacke etal. 2004). The relative resistance of pits vs lumens should then be higher in light branches
vs shade branches, which is consistent with the larger difference in measured vs theoretical hydraulic conductivity in our
open-grown trees. In summary, the leaf-area-specific hydraulic
conductivity per carbon investment is thus lower, but the carbon gain in photosynthesis per leaf-area hydraulic conductivity
is larger in light branches.
Another possible explanation for this is offered by our results
on the strong dependence of shoot conductivity on parent
branch age despite local transpiration demand. If the opengrown trees had a higher demand of transpiration than was supported by their shoot structure, this could lead to increased
probability of cavitation in their shoots and thus lowered conductivity compared with the other two tree classes (Tyree and
Ewers 1991, Zwieniecki and Holbrook 1998, Martnez-Vilalta
etal. 2004). Trees show an ability to refill cavitated tracheids
until relatively low conductivity values and this phenomenon can
already be seen on a daily time scale (Zwieniecki and Holbrook
1998, Perks etal. 2004, Urli etal. 2013), which suggests that
cavitation can well have been behind the low conductivity values.
However, large amounts of cavitation seem improbable in our
study since Scots pine is known to be a very isohydric species,
and to avoid cavitation to a very great extent (e.g., Irvine etal.
1998, Duursma etal. 2008).
To a certain extent, the large differences between measured
and calculated hydraulic conductivity values in each tree class
are also explained by computational assumptions. In Hagen
Poiseuille, all the tracheids are assumed to be cylindrical, but
actually the shape of lumen area is more rectangular than

12 Grnlund etal.

Conclusions
Xylem conduit size and sapwood-specific conductivity of current
shoots correlate strongly with parent branch age. Specific leaf
area, Huber value and area-specific conductivity are strongly
influenced by light conditions. Based on a comparison between
theoretical and measured hydraulic conductivities, the properties
of the pit membrane may also be significantly influenced by
shoot light conditions. The water potential of the current-year
shoots in high light is likely lower compared with shoots growing
in more shaded environment. These results are consistent with
the hypothesis in earlier literature that shoots in high light should
be able to withstand lower water potential because of their better resistance against cavitation related to a trade-off between
pit conductance and vulnerability to cavitation.

Tree Physiology Volume 00, 2016

Supplementary data
Supplementary data for this article are available at Tree Physiology
Online.

Conflict of interest
None declared.

Funding
This work was supported by Academy of Finland grant #
272041 and LIFE12 grant # ENV/FI000409.

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