AZIMUTHAL VARIATIONS IN XYLEM STRUCTURE AND WATER RELATIONS IN CORK OAK (QUERCUS SUBER) - BRILL
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IAWA Journal, Vol. 32 (1), 2011: 25– 40
Azimuthal variations in xylem structure and water
relations in cork oak (Quercus suber)
Nadia Barij1, Jan Čermák2 and Alexia Stokes 3 *
Summary
Azimuthal variations in xylem conductivity and transpiration can occur
in trees and may be due to heterogeneity in environmental factors. In cork
oak (Quercus suber L.), it can be hypothesized that such modifications
may be more pronounced because the insulating layer of bark is harvested
every 9–10 years, thus cambial cells will be exposed to fluctuations in
the microenvironment. To investigate whether xylem structure and water
relations differed around the stems of mature cork oak, sap flow per sec-
tion and xylem structure were measured on the northern (N) and southern
(S) sides of nine trees during three months in Portugal, using the Trunk
Sector Heat Balance method. Crown size was measured on both sides of
each tree and increment wood cores were extracted from the sites where
sap flow was measured in five trees. Wood moisture content, earlywood
(EW) vessel size and density were measured and theoretical hydraulic
conductivity for individual vessels (L th) was calculated along the N and S
stem radial profiles. No significant differences in crown size between the
two sides of the tree were found, but sap flow was higher on the S side
of the tree in May only. No differences in wood moisture content were
observed along the length of each wood core throughout the heartwood.
Significant differences in vessel size occurred, with a greater diameter
and surface area on the N side of the tree, and consequently Lth was
significantly greater. These conduit diameters on the S facing side of the
tree may be smaller in response to a combination of signals and trade-offs
due to the heterogeneous air and soil environment around the tree.
Key words: Wood anatomy, vessel lumina, hydraulic conductivity, sap
flow.
Introduction
Portugal accounts for over 50% of the world cork harvest (FAO 1997). Cork is derived
from the outer bark of the evergreen cork oak (Quercus suber L.), a Mediterranean
species which is highly resistant to drought stress and elevated summer temperatures
(Nardini & Tyree 1999; Ghouil et al. 2003; Otieno et al. 2006; Kurz-Besson et al. 2006).
1) Université Bordeaux I, INRA, CNRS, UMR US2B, 33400 Talence, France.
2) Institute of Forest Botany, Dendrology and Geobiocenology, Faculty of Forestry and Wood Technol-
ogy, Mendel University in Brno, Zemědělská 3, 61300 Brno, Czech Republic.
3) INRA, AMAP, TA A51 / PS2, Boulevard de la Lironde, 34398 Montpellier Cedex 5, France.
*) Corresponding author [E-mail: alexia.stokes@cirad.fr].
Associate Editor: John Sperry
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Nevertheless, in recent years the number of cork oak trees in Portugal dying through
drought stress and stress related attacks by insects and fungi has increased (Brasier &
Scott 2008). Although one of the mechanisms contributing to drought stress resistance
is the presence of the thick, insulating layer of phellem, this phellem is harvested as
cork every 9–10 years, thus placing trees under physiological stress. The effects of
cork removal include increased water loss from the exposed surface, which may induce
a decrease in stomatal activity and the death of the newly exposed inner bark tissues
with subsequent formation of a traumatic periderm (see Silva et al. 2005). As a result,
photosynthetic efficiency is reduced (Werner & Correia 1996). Although several studies
have been carried out on the effects of climate on ecophysiology and growth of cork
oak stands (Costa et al. 2002; Aranda et al. 2005), little information exists concerning
the influence of very local environmental factors on water relations and xylem structure
(Leal et al. 2006, 2007, 2008; Knapic et al. 2007).
In cork oak, most radial growth is linked to winter and autumn precipitation (Caritat
et al. 2000; Costa et al. 2002). In the Mediterranean evergreen oaks Q. coccifera L. and
Q. ilex L., maximal vessel diameter was positively regressed with mean annual rainfall
(Villar-Salvador et al. 1997). However, in a more detailed study, earlywood (EW) vessel
size in Q. petraea and Q. pubescens from a drought-prone site was largely governed by
accumulated precipitation during the second half of the previous growing season, but
at a mesic site, by spring precipitation of the current year (Fonti & García-González
2008). Cork oak is semi ring-porous in nature (Leal et al. 2007), therefore the size of
vessels and their radial distribution along the stem radius are the most significant con-
tributors to the theoretical hydraulic conductivity of wood (L th) and hence water trans-
port and efficiency along the whole water transport pathway (Ellmore & Ewers 1985).
Lth depends strongly on vessel diameter, as according to the Hagen-Poiseuille equation,
hydraulic conductance of capillaries is proportional to the fourth power of the radius
(Zimmermann 1983). Therefore, EW formed at the beginning of the growing season
will largely determine the hydraulic architecture of the stem and any changes in EW
structure as a result of external abiotic factors, e.g. drought or temperature, will be
reflected in hydraulic conductivity and safety (Fonti & García-González 2004). In a
typical sparse forest stand, which can be highly heterogeneous, variations in sunlight,
temperature and water availability could therefore result in large inter- and intra-tree
variability in EW vessel structure. However, tree density in cork oak stands is typical-
ly low, and mature trees are usually isolated with little competition from neighbours.
Therefore, differences in environmental parameters, e.g. solar radiation, will be related
to canopy orientation and azimuth (cardinal direction) rather than vertical gradient
(Infante et al. 2001).
Several authors have suggested that physiological changes occur in trees subjected
to uneven solar radiation levels around trees. Stokes et al. (1995) showed that in Picea
sitchensis (Bong.) Carr., uneven irradiance levels resulted in asymmetric growth of both
shoots and roots. Muth & Bazzaz (2002a) found that leaf number and canopy area were
greater on the sides of Betula papyrifera Marsh. seedlings subjected to higher levels
of photosynthetically active radiation (PAR). Muth & Bazzaz (2002b) also mapped
tree canopies with regard to the heterogeneous light environments at the edges of six
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experimental gaps and showed that the magnitude and precision of canopy displace-
ment were generally greater for hardwoods than for conifers. With regard to xylem
structure, Liese and Dadswell (1959) suggested that sunlight and temperature variations
acting directly on the tree trunk can affect cell number and size. More significantly,
recent work on Q. ilex has shown that sap flow density in mature trees was higher in
the NE and NW orientations compared to that on the S side of the tree and differences
were attributed to changes in spatial leaf area distribution, which were, however, not
measured (Infante et al. 2001). These authors also suggest that the relationship between
xylem conductivity and foliar transpiration will be reflected in long-term changes in
sapwood vessel diameter and density in different orientations around the trunk.
If azimuthal variations in xylem conductivity and transpiration occur in trees, and
are found to be due to heterogeneity in environmental factors around stems, it can be
hypothesized that in cork oak such modifications may be more pronounced. In this
species, the protective, insulating layer of bark is harvested every 9–10 years, thus the
cambial cells will be exposed to fluctuations in the microenvironment, especially just
after the harvest. Therefore, we carried out a study aimed at improving the understand-
ing between xylem structure and water relations around the stems of mature cork oak
in Portugal. Stem sap flow was measured at different positions around nine trees for
three months. Increment wood cores were extracted from the sites where sap flow was
measured in five trees and relative water content along the core was determined. Ves-
sel size and density were measured using a light microscope on thin sections cut from
wood cores. L th was then estimated for individual vessels. Results are discussed with
regard to the influence of xylem structure on hydraulic conductance in cork oak.
Materials and Methods
Experimental site characteristics
The field plot was located near the town of Pinhal Novo, 35 km south-east of Lisbon
and between the estuaries of Tagus (Tejo) and Sado in Portugal (38° 38 ' latitude and
8° 51' W longitude) at an altitude of 30 m. The climate at the field site is Mediterranean
with an Atlantic influence. Total annual precipitation (average over 30 years) is 750 mm
and occurs mainly in spring, winter and autumn (maximum in winter). Potential eva-
potranspiration ranged from 2–8 mm d -1 during the growing season (Nadhezhdina et al.
2008). Typical for a Mediterranean climate, summers are hot and dry with a high inter-
annual variability of precipitation. The average temperature throughout the year is
16.1 °C, with an average minimum temperature in January of 5.3 °C and an average
maximum temperature in August of 28.9 °C. A full description of geology and soil
types in the region is given in Nadhezhdina et al. (2008).
The study site was a stand of 80-year-old cork oak (Quercus suber L.). Trees had
been planted in rows 10 × 11 m apart, and had a density of 76 trees ha-1 in 2001 with
some reduction in early 2003. The average canopy height was 10 m. The understorey
was patchy and varied between dry grass and low shrubs, e.g. Cistus spp., which reach-
ed heights up to 0.4 m. Except for the study trees, cork was last harvested between
30/06/2003 and 12/07/2003 and before that in 1994.
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Sampling procedure and sap flow measurements
Since healthy trees were needed for the study of sap flow, we used acoustic tomog-
raphy to determine if any decay existed inside the stems. Twelve accelerometers were
placed on the trunk of each tree at breast height (BH). Striking the tree with an impact
device induced stress waves. The elapsed time for the signal to reach the other side of
the tree and be detected by a second accelerometer was converted to a wave propaga-
tion speed, which gives information about the physical conditions inside the tree. Full
methodology is described in Lorra & Kathage (2004). After sampling 30 trees, nine
without any signs of decay were chosen for the study of sap flow. Mean diameter at
breast height (DBH) was 0.42 ± 0.02 m (means are ± standard error). The mean crown
radius was measured on the northern (N) and southern (S) sides of each tree.
Sap flow was measured in two cardinal directions (north and south) of each of the
nine trees using the Trunk Sector Heat Balance method (THB, Čermák et al. 1973,
2004; Tatarinov et al. 2005). Sap flow sensors were inserted into the trunk at BH.
Each sensor consisted of three electrodes inserted at the same height in parallel into
sapwood, keeping the central electrode in a radial direction relative to the tree trunk.
The electrodes comprised three stainless steel plates (25 mm wide and 1 mm thick),
which were inserted into the sapwood at a depth of 0.02 m, which was approximately
the depth of sapwood. A fourth plate of the same size was inserted 0.1 m below these
electrodes. The temperature difference dT between the upper plates and the reference
plate below was measured with copper-constantan (Cu-Cst) thermocouples placed into
1-mm-thin stainless steel hypodermic needles inserted in slots through the electrode
axes. A constant heating power 0.6 W was supplied to the sapwood via the upper set of
electrodes and the electric current running through the wood between the plates results
in even heating between the plates according to equation 1:
P = Q.dT. c w + dT. λ [Equation 1]
where:
Q = (P/dT cw) i – (P/dT cw)0 [Equation 2]
Variable P is the constant heat input power [W], Q is the sap flow rate between the upper
electrodes [kg.sec-1], dT is the temperature difference between the upper (heated) and
lower (reference) electrodes [K], cw is the specific heat of water [J.kg-1.K-1] and λ is
the coefficient of heat loss from the measuring point [W.K-1]. This heat loss is visible
in the recorded flow data as the so called “fictive flow”, which can be calculated from
the same input variables, but under conditions approaching that of zero sap flow (e.g.,
at night after prolonged rain). Full methodology and equations for calculating sap flow
are given in Čermák et al. (1973, 2004) and Tatarinov et al. (2005).
Measuring points were protected against direct illumination and rain by covering the
sap flow sensors with polyurethane foam, and sheets of aluminium and plastic tight-
ened over slightly sanded stem bark. To avoid changing the microclimate of the stem,
insulation was restricted to the sensors themselves, and not the surrounding stem sur-
face, which was protected sufficiently by the thick bark. Data were measured every
minute and recorded as means over 15 min intervals with a Campbell CR10 datalogger
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(Campbell Scientific Inc. NE, USA) for three months. All cables (between sensors and
data loggers) were buried in a 0.05 m deep trench to protect them from animals. Data
are presented as daily means averaged monthly from May to July 2003. Global radia-
tion, Rg, (CM6B, Kipp and Zonen, Delft, Netherlands) was measured every minute and
recorded as means over 15 min intervals during this period.
Sampling of wood cores
Five trees were randomly chosen from the 30 which had been examined using acous-
tic tomography and increment cores (5 mm in diameter) were extracted from breast
height (BH) during the morning hours in early May, using a Suunto© wood corer. Two
cores were extracted from due north and two from due south. The two cores taken at each
position were 20 mm apart with one taken above the other. Each core was long enough
to reach the stem pith; therefore the entire cross section of the stem was sampled. Cores
were immediately wrapped in aluminium foil and plastic bags and were then transported
to the laboratory and stored at 4 °C. With this method, water loss from samples should
not be greater than approximately 10% (Morales et al. 2002). One core from each po-
sition was used for subsequent estimation of wood water content (Wc ) and the second
core was used for anatomical analysis.
Wood water content (Wc )
Wood water content (Wc ) was measured using the method described in Kravka
et al. (1999). Within 24 hours of extracting the wood cores, we measured Wc along the
length of the core. Both functional sapwood and heartwood were present in the core
and could be distinguished by differences in colour. No dry transition zone occurred
between the sap- and heartwood (Krejzar & Kravka 1998; Čermák & Kučera 1990).
Samples 20 mm long were cut from the entire length of the core. The fresh mass (M f )
of each sample was determined using a balance with a resolution of 1.0 mg. The dry
mass was obtained after drying in an oven at 80 °C for three days or until a constant
dry mass (Md) was attained. Wc was calculated using:
M f – Md
Wc = –––––––– [Equation 3]
Md
Microscopic analysis of vessel lumina
Using the intact cores, 20-mm-long samples were cut from each core which corre-
sponded to the segments in the cores used for determining Wc. Thin transverse sections
(20 µm thick) were then cut from each segment in the radial direction, using a sliding
microtome whilst the wood was still fresh. The thin sections were then mounted onto
glass slides and stained with a solution of phloroglucinol (1,3,5-trihydroxybenzene)
diluted in hydrochloric acid, which stains cell wall lignin a red colour (Chaffey 2002).
The phloroglucinol solution was left for 1 min and samples were then washed with dis-
tilled water. Coverslips were placed on the sections to protect them.
Wood sections were examined using a light microscope at ×200 magnification. In
order to scale the photographs processed by the software, a calibrated carbon lead was
placed near the samples. Photographs were taken of the transversal surface of the wood
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conducting vessels present in each annual growth ring. Several parameters were then
measured using the image analysis software, WinCell© (Régent Instruments Inc.,
Quebec, Canada).
Maximum (d max ) and minimum (dmin ) vessel lumen diameters were measured for
earlywood (EW) within each growth ring. Hydraulic diameter (dh ) of each EW vessel
was then calculated using (Lewis 1992):
___________
2d 2max) d 2min
1 × ––––––––––––
√(___________
dh = –– [Equation 4]
2 √d 2max + d 2min
Anatomical lumen area (Alum) of conducting EW vessels was calculated as the el-
lipse:
Alum = π (dmax × dmin ) [Equation 5]
We calculated dh and Alum as opposed to weighted vessel diameter (Sperry & Sullivan
1992) so that minimum and maximum diameters were taken into account in the calcu-
lation of vessels with an elliptical shape. EW vessel density was obtained by counting
the number of vessels per unit area of wood.
Theoretical hydraulic conductivity (Lth ) of single vessels
The theoretical assessment of hydraulic conductivity (Lth) was carried out using the
Hagen-Poiseuille equation (Equation 6, Zwieniecki et al. 2001) for all single vessels of
EW along the stem core (mean per tree: n = 1315 vessels on the N side and n = 1270
vessels on the S side of the stem). Lth ignores the hydraulic resistance of end-walls,
which account for the majority of the flow resistance, hence the calculated Lth is over
twice as great as the actual conductivity (L), and the proportionality between Lth and
actual L is likely to be quite variable.
r4 π
Lth = ––––– [Equation 6]
8η
Where η is the viscosity of water (1.002 e-9 MPa s) at 20 °C.
Statistical analysis
Sap flow was analysed considering daily data recorded between 8-00 and 24-00
only. Mean daily sap flow was calculated using mean data from both the N and S sides
of the trees and analysis of variance was used to determine if differences in mean sap
flow existed between the months of May, June and July and between the N and S sides
of the trees.
Vessel size and Lth data were tested for normality using an Anderson-Darling test.
All data had normal distributions (P > 0.05). Regressions were carried out to determine
the relationship between crown radius and DBH on both N and S sides of the tree. The
radial distance from the cambium was represented as a percentage of distance from the
cambium in order to allow a better comparison of trees of different sizes. The relation-
ship between mean Wc, Alum, dh and Lth, between the N and S sides of the trees, was
examined using analysis of covariance with depth of wood as a covariate.
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Results
Site characteristics
The mean crown radius on the N side of the tree was 4.8 ± 0.5 m and on the S side
5.4 ± 0.7 m. No significant differences in crown size between the two sides of the tree
were found. No significant relationship was found between mean crown radius and DBH.
120 -
––0–– May ––/–– June ––:–– July
100 -
Mean sap flow (g.cm-2.h-1 )
80 -
60 -
40 -
20 -
0- | | | | | | | |
0 3 6 9 12 15 18 21 24
Time of day (h)
Figure 1. Mean sap flow was higher in June and July than in May on the S side of cork oak stems.
Data are means of daily sap flow ± standard error (n = 1 tree).
Measurements of sap flow
Mean sap flow at all times of the day was lower in May compared to June and July
(Fig. 1). Between 12.00 and 18.00 h, mean sap flow ranged from 60–65 g.cm-2.h-1 in
May, increasing to 80–90 g.cm-2.h -1 in June and July (Fig. 1). Mean sap flow was sig-
nificantly greater on the S side of the tree during the month of May only (Fig. 2). On
1.80 - North / South
Mean sap flow (kg.cm-2.day -1 )
1.60
1.40
1.20
1.00
0.80
0.60
0.40
0.20
0.00
May June July
Month
Figure 2. Mean daily sap flow was significantly higher on the S side (white bars) of cork oak
stems compared to that on the N side (black bars) in May only (F1,8 = 8.42, P = 0.02). Data are
means ± standard error (n = 9 trees).
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3.00 -
Sunny day
2.50 -
Sap flow (kg.cm-2)
2.00 -
1.50 -
Cloudy day
Cloudy day
1.00 -
0.50 -
| | | | | | | | | | | | | | | |
0.00 -
8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24
Time of day (h)
Figure 3. Daily variation in sap flow on a sunny (Rg = 19 MJ m-2 d-2 on June 5) and a cloudy
day (Rg = 10 MJ m-2 d-2 on 30 May). Differences in sap flow between the N (black circles) and
S (white squares) sides of the tree stem were greater on cloudy days than on sunny days.
very sunny days, sap flow was higher on the S side of the tree until 14.00 h. Between
14.00 and 18.00 h, sap flow was similar on both sides of the tree, when the sun was
situated overhead. In the evening, sap flow was lower on the N side of the tree (Fig. 3).
On cloudy days, sap flow was similar on both sides of the tree (Fig. 3). A full detailed
analysis of seasonal sap flow results are presented in Nadhezhdina et al. (2008).
Wood water content (Wc )
Mean Wc in all cores was 60.0 ± 0.2%. No significant differences in Wc in either
sapwood or heartwood were found either along the increment cores or between the N and
S sides of the tree, although sample length (20 mm) may have been too long to deter-
mine differences.
Microscopic analysis of vessel lumina
We observed precise boundaries between EW and latewood (LW) with regard to
vessel size. Wood was semi ring-porous to ring-porous and EW was characterized by
large lumina and LW by smaller lumina. The presence of tyloses (Cochard & Tyree
1990; Nardini et al. 1999) in vessel lumina was also observed but the quantity was not
measured.
Mean Alum decreased significantly from the cambium (30000 µm²) towards the
pith (5000 µm²). Significant differences in Alum were found between both sides of the
tree, with the S side having a significantly smaller Alum with regard to depth (Fig. 4a).
Mean vessel density was constant along the outer 50% of xylem depth, but increased
significantly towards the pith (Fig. 4b). Vessel density was not significantly different
between the N and S sides of the tree.
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a b
45000 350
40000 300
Vessel density (n/cm 2 )
35000
250
30000
Alum (µm2 )
25000 200
20000 150
15000
100
10000
5000 50
0 0
10 20 30 40 50 60 70 80 90 10 20 30 40 50 60 70 80 90
c 120
d
2.5E-09
100
2.0E-09
L th (m 4 MPa -1 s -1)
80
1.5E-09
dh (µm)
60
1.0E-09
40
0.5E-09
20
0 0.0E-09
10 20 30 40 50 60 70 80 90 10 20 30 40 50 60 70 80 90
Radial distance from cambium (%)
Figure 4. Variations in xylem characteristics on the S side (white bars) of tree stems compared
to the N side (black bars). – a: Lumen area (Alum) of vessels decreased significantly from the
cambium towards the pith (F1,15 = 71.44, P < 0.001) and was significantly smaller on the S side of
the tree (F1,15 = 23.19, P < 0.001). – b: Vessel density increased significantly from the cambium
towards the pith (F1,15 = 111.73, P < 0.001) but no significant differences were found between
the two sides of the tree stem. – c: Hydraulic diameter (dh) of vessels decreased significantly
from the cambium towards the pith (F1,15 = 51.89, P < 0.001) and was significantly smaller on
the S side of the tree (F1,15 = 18.10, P < 0.001). – d: Hydraulic conductivity (Lth) decreased
significantly from the cambium towards the pith (F1,15 = 47.74, P < 0.001) and was significantly
lower on the S side of the tree (F1,15 = 14.58, P = 0.002).
Hydraulic diameter and theoretical hydraulic conductivity (Lth) of single vessels
Mean hydraulic diameter (dh) was 72.5 ± 24.8 µm and increased significantly from
the pith to the cambium (Fig. 4c). When the N and S sides of the tree were compared,
dh was similar in the outer wood between both sides of the tree but was significant-
ly smaller towards the pith on the S side of the tree (Fig. 4c). Results show that the
outer stem wood (up to 50% radial distance from cambium) had a significantly higher
Lth than inner wood (Fig. 4d). Except for wood in the outer 20%, Lth was significant-
ly higher in cores extracted from the N side of the tree compared to wood from the
S side.
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Discussion
Results show that in cork oak, even when crown size does not differ around the tree,
xylem structure can be influenced by the cardinal direction. In edge trees of plantations,
crowns and root systems are often asymmetrical, which may be due to competition
for space and light (Muth & Bazzaz 2002b; Cucchi et al. 2004). However, the cork
oaks we studied were inside the plantation and planted at a low density, with little or
no competition for space between the crowns. It is probable that crowns were asym-
metrical with regard to gaps in the canopy, rather than cardinal directions, when the
spacing was about 10 m. Muth and Bazzaz (2002a) found that leaf number and canopy
area in Betula papyrifera seedlings were always greatest on the side of the tree with
the highest PAR, and therefore grew towards gaps in the canopy. We did not measure
gap size in the canopy of the cork oak plantation, nor the direction of greatest crown
asymmetry; therefore these parameters would be useful to estimate in future studies.
Kagawa et al. (2005) also showed through studies of pulse labelling and the distribution
of 13C tracer in Cryptomeria japonica D. Don, that a given side of the stem is connected
to different branches depending on the season. Nadezhdina (2010) demonstrated that
water transport was integrated in the diffuse porous species Acer platanoides L. Large
parts of the tree crown were supplied with water from the same root sector, therefore
integration probably occurs through the cross-grained network of axial vessels. Thus
studies of crown asymmetry may not necessarily reflect the exact nature of the internal
hydraulic architecture of a tree.
Sap flow differed significantly between the N and S sides of the trunks during the
month of May only, when EW is laid down. Sap flow was higher on the S side, which
is in agreement with Loustau et al. (1998) and Kubota et al. (2005) who suggested that
azimuthal variations were due to either xylem structure or were the result of differential
solar heating (Granier 1987). However, more recent research has shown that root archi-
tecture can influence stem sap flow. Sap flow asymmetry near the stem base corresponds
to different root distributions and rooting depths around the stem (Nadezhdina et al.
2002; Čermák et al. 2008). However, this asymmetry is less marked further up the stem
(Čermák & Kučera 1990) and it is unlikely that a group of mature trees will possess the
same asymmetric rooting patterns which similarly affect sap flow, although this has been
observed in mature, leaning Pinus sylvestris L. subjected to strong prevailing winds
(Čermák et al. 2008). To our knowledge, no studies of azimuthal sap flow have been
combined with measurements of vessel size and hydraulic conductivity in oak trees.
However, Infante et al. (2001) measured sap flow in three directions around the stem
in Quercus ilex L. Results showed that sap flow was higher on the northeastern and
northwestern sides than the S side of the tree. It was hypothesized that internal crown
shading occurs during the day, affecting azimuthal sap flow. Also, if leaf water poten-
tials differed depending on leaf orientation during drought, as found in some Quer-
cus species (Hinckley et al. 1978), differences in leaf water potential could explain
the lower transpiration rates of the S oriented leaves compared with leaves in other
directions. Infante et al. (2001) also suggest that the lower sap flow measured in the
S orientation could be explained as an adaptation of this part of the xylem to more
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severe water stress than in other orientations. David et al. (2007) demonstrated that
Q. ilex possessed more effective drought avoidance and drought tolerance mechanisms
than Q. suber, which may explain why we did not observe lower sap flow on the S side
of the tree. Quercus suber is also regularly debarked, which may increase sensitivity
to environmental signals and reflected in xylem structure.
Xylem structure in cork oak was semi ring-porous to ring-porous, with large EW
vessels and smaller LW vessels. Variations in EW vessel size and density along the
radial profile were similar to that of other oak species (Krejzar & Kravka 1998; Inside
Wood 2004) and dicot woods in general. Significantly greater EW vessel Alum, dh and
Lth were found on the N sides of the trees compared to the S sides. As canopy structure
did not change between both sides of the trees, another factor must exist which influ-
ences wood formation in springtime. The conduit diameters on the S facing side of the
tree may be smaller in response to a greater potential for cavitation, as sap flow was
higher during the period of EW formation and cell expansion. Smaller conduit diam-
eter is one possible mechanism for achieving greater safety from cavitation, but ves-
sels would have greater hydraulic resistivity. We calculated vessel Lth , but this parameter
does not consider the hydraulic resistance of end walls, which accounts for the major-
ity of the flow resistance (Wheeler et al. 2005). In Q. petraea and Q. pubescens growing
on a drought-prone site, EW vessel formation was found linked to the accumulation
of reserves during the second half of the previous summer (Fonti & García-González
2008). Therefore, vessel size may be regulated in expectation of water demand, al-
though the current year’s spring precipitation will likely also influence vessel expan-
sion.
Other candidates for factors which affect xylem formation are water availability and
variations in light and temperature (Fonti & García-González 2004). It is unlikely that
spatial patterns in soil moisture content occur to such an extent as to differ significantly
in cardinal directions around a tree (Barij et al. 2007), although root distribution and
depth can result in asymmetric sap flow at the stem base (Nadezhdina 2010). Uneven
irradiation levels or temperature changes can affect wood formation, but very little
information exists with regard to irradiation effects on wood formation. In thick-barked
trees such as cork oak, light transmission would be extremely difficult. However, in this
species, the insulating cork layer is harvested every nine years, therefore exposing the
cambial region to direct environmental influences. With regard to temperature effects,
recent evidence has shown that air temperature significantly influences xylem structure
in trees (Gričar et al. 2007). Thomas et al. (2004) grew Eucalyptus camaldulensis Dehnh.
at three temperatures for nine weeks at a constant vapour pressure deficit. Wood density
was found to increase with higher growth temperature, and wood hydraulic conductivity
per unit area decreased. Vessel area was also reduced at higher temperatures due to a
decrease in vessel diameter. These authors showed that this phenomenon was due to
water viscosity being sensitive to higher temperatures, therefore smaller or fewer vessels
would be required to transport water to leaves at higher temperatures when water has
lower viscosity (Roderick & Berry 2001). We did not measure wood temperature around
the trunk of the cork trees we studied; however, Wieser (2002) found that sapwood
temperature (measured at a depth of 0.01 m) was significantly greater on the S facing
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via free access36 IAWA Journal, Vol. 32 (1), 2011
side of 50-year-old Pinus cembra L. trees than on the N-facing side. Consequently,
annual respiration was up to 13% higher on the south side of the trees. Pinus spp. are
generally thick-barked, therefore in debarked cork oak, temperatures could be higher
on the exposed S side of the tree, particularly when the sun is not overhead, thus affect-
ing both xylem structure and water relations. However, Knapic et al. (2007) and Leal
et al. (2008) showed that wood xylem structure differed little in old bark-harvested and
never debarked Q. suber trees. These results indicate that it is necessary to carry out
further research in this domain, to ensure that the scaling-up of stem respiration using
data taken from one position in the tree is correct (Nadezhdina et al. 2002; Delzon
et al. 2004), especially in thin-barked species, or species where the bark is removed
as in cork oak.
No differences in wood Wc occurred along with radial distance from the cambium,
even with regard to sap- and heartwood. Generally, it is thought that in coniferous
trees, the water content in heartwood is usually lower than that for sapwood (Čermák
& Nadezhdina 1998; Fromm et al. 2001) whereas in some hardwood species water
content varies little between sap- and heartwood (Phillips et al. 1996; Fromm et al.
2001; Morales et al. 2002; Barij et al. 2007). However, it has been observed in other
oak species, e.g., Quercus robur, Q. petraea and Q. pubescens, that water content was
lower in heartwood than in sapwood (Čermák, unpublished data). In our study, Wc did
not differ between the N and S sides of the tree stems, although 20-mm sections may
have been too long to register subtle differences. Similar results were also found in
Q. pubescens by Barij et al. (2007) and Bucci et al. (2004), who suggested that xylem
structure was a better indicator of stem storage capacity than saturated water content,
as it reflects biophysical properties of the sapwood related to the efficiency of recharge
and utilisation of stored water as well as the potential amount of stem water storage.
We suggest therefore that in studies of hydraulic relations in trees, sap flow studies
combined with xylem structure are more useful indicators of long-term water uptake
than Wc.
In conclusion, differences in EW xylem structure occur around oak trees and are
likely related to a variety of environmental signals. However, without a series of focused
experiments, it is not easy to suggest which is the dominant, or limiting, factor affecting
xylem growth. Most likely, a combination of signals and trade-offs in structure exist. In
a species able to demonstrate a certain degree of plasticity in response to environmental
signals, internal and local modifications will allow a more optimal regulation of water
transport in a dry environment.
Acknowledgements
This study was funded by the European projects WATERUSE (EVK1-CT-2000-00079) and Eco-Slopes
(QLK5-2001-00289), and research intention MSM 6215648902. Thanks are due to S. Lorra and I. Fer-
reira (Technical University of Lisbon) for help with fieldwork. AMAP (Botany and Computational
Plant Architecture) is a joint research unit, which associates CIRAD (UMR51), CNRS (UMR5120),
INRA (UMR931), IRD (2M123), and Montpellier 2 University (UM27).
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via free accessBarij, Čermák & Stokes — Azimuthal variation in cork oak wood 37
References
Aranda, I., L. Castro, M. Pardos & J. A. Pardos. 2005. Effects of the interaction between drought
and shade on water relations, gas exchange and morphological traits in cork oak (Quercus
suber L.) seedlings. For. Ecol. Manage. 210: 117–129.
Barij, N., A. Stokes, T. Bogaard & L. P. H. van Beek. 2007. Does growing on a slope influence
xylem structure and water relations? Tree Physiol. 27: 757–764.
Brasier, C.M. & J. K. Scott. 2008. European oak declines and global warming: a theoretical
assessment with special reference to the activity of Phytophthora cinnamomi. EPPO Bull.
24: 221–232.
Bucci, S. J., G. Goldstein, F. C. Meinzer, F. G. Scholz, A.C. Franco & M. Bustamente. 2004.
Functional convergence in hydraulic architecture and water relations of tropical savannah
trees: from leaf to whole plant. Tree Physiol. 24: 891–899.
Caritat, A., E. Gutierrez & M. Molinas. 2000. Influence of weather on cork-ring width. Tree
Physiol. 20: 893–900.
Čermák, J., M. Deml & M. Penka. 1973. A new method of sap flow rate determination in trees.
Biol. Plant. (Praha) 15: 171–178.
Čermák, J. & J. Kučera. 1990. Scaling up transpiration data between trees, stands and watersheds.
Silva Carel. 15: 101–120.
Čermák, J., J. Kučera & N. Nadezhdina. 2004. Sap flow measurements with some thermodynamic
methods, flow integration within trees and scaling up from sample trees to entire forest stands.
Trees: Struct. Func. 18: 529–546.
Čermák, J. & N. Nadezhdina. 1998. Sapwood as the scaling parameter - defining according to xylem
water content or radial pattern of sap flow? Ann. Sci. For. 55: 509–521.
Čermák, J., N. Nadezhdina, L. Meiresonne & R. Ceulemans. 2008. Scots pine root distribution de-
rived from radial sap flow patterns in stems of large leaning trees. Plant and Soil 305: 61–75.
Chaffey, N. J. (ed.). 2002. Wood formation in trees: Cell and molecular biology techniques.
Taylor & Francis, London.
Cochard, H. & M. Tyree. 1990. Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation,
and seasonal changes in embolism. Tree Physiol. 6: 393–407.
Costa, A., H. Pereira & A. Oliveira. 2002. Influence of climate on the seasonality of radial growth
of cork oak during a cork production cycle. Ann. Sci. For. 59: 429–437.
Cucchi, V., C. Meredieu, A. Stokes, S. Berthier, D. Bert & M. Najar. 2004. Root anchorage of
inner and edge trees of Maritime pine (Pinus pinaster Ait.) growing in different soil podzolic
conditions. Trees: Struct. Func. 18: 460– 466.
David, T.S., M.O. Henriques, C. Kurz-Besson, J. Nunes, F. Valente, M. Vaz, J.S. Pereira, R. Sieg-
wolf, M.M. Chaves, L. C. Gazarini & J. S. David. 2007. Water-use strategies in two co-
occurring Mediterranean evergreen oaks: surviving the summer drought. Tree Physiol. 27:
793–803.
Delzon, S., M. Sartore, A. Granier & D. Loustau. 2004. Radial profiles of sap flow with increas-
ing tree size in maritime pine. Tree Physiol. 24: 1285–1293.
Ellmore, G. S. & F.W. Ewers. 1985. Hydraulic conductivity in trunk xylem of elm, Ulmus ameri-
cana . IAWA Bull. n.s. 6: 303–307.
F.A.O. 1997. An information bulletin on non-wood forest products. Non-Wood Forest Products
Vol. 1, No. 4: 84.
Fonti, P. & I. García-González. 2004. Suitability of chestnut earlywood vessel chronologies for
ecological studies. New Phytol. 163: 77–86.
Fonti, P. & I. García-González. 2008. Earlywood vessel size of oak as a potential proxy for spring
precipitation in mesic sites. J. Biogeog. 35: 2249–2257.
Downloaded from Brill.com10/09/2020 10:47:54AM
via free access38 IAWA Journal, Vol. 32 (1), 2011
Fromm, J. H., I. Sautter, D. Matthies, J. Kremer, P. Schumacher & C. Ganter. 2001. Xylem water
content and wood density in spruce and oak trees detected by high-resolution computed
tomography. Plant Physiol. 127: 416– 425.
Ghouil, H., P. Montpied, D. Epron, M. Ksontini, B. Hanchi & E. Dreyer. 2003. Thermal optima
of photosynthetic functions and thermostability of photochemistry in cork oak seedlings.
Tree Physiol. 23: 1031–1039.
Granier, A. 1987. Evaluation of transpiration in a Douglas-fir stand by means of sap flow meas-
urements. Tree Physiol. 3: 309–320.
Gričar, J., M. Zupančič, K. Čufar, & P. Oven. 2007. Regular cambial activity and xylem and
phloem formation in locally heated and cooled stem portions of Norway spruce. Wood Sci.
Tech. 41: 463–475.
Hinckley, T. M., J.P. Lassoie & S.W. Running. 1978. Temporal and spatial variations in the water
status of forest trees. For. Sci. Monogr. 20: 72 pp.
Infante, J. M., A. Mauchamp, R. Fernández-Alés, R. Joffre & S. Rambal. 2001. Within-tree vari-
ation in transpiration in isolated evergreen oak tree: evidence in support of the pipe model
theory. Tree Physiol. 21: 409– 414.
InsideWood. 2004-onwards. Published on the Internet. http://insidewood/ lib.ncsu.edu/search
[accessed 06/03/06].
Kagawa, A., A. Sugimoto, K. Yamashita & H. Abe. 2005. Temporal photosynthetic carbon iso-
tope signatures revealed in a tree ring through 13 CO 2 pulse-labelling. Plant Cell. Environ.
28: 906–915.
Knapic, S., J. L. Louzada, S. Leal & H. Pereira. 2007. Radial variation of wood density compo-
nents and ring width in cork oak trees. Ann. For. Sci. 64: 211–218.
Kravka, M., T. Krejzar & J. Čermák. 1999. Water content in stem wood of large pine and spruce
trees in natural forests in central Sweden. Agric. Forest Meteorol. 98-9: 555–562.
Krejzar, T. & M. Kravka. 1998. Sap flow and vessel distribution in annual rings and petioles of
large oaks. Lesnictvi-Forestry 44: 93–201.
Kubota, M., J. Tenhunen, R. Zimmermann, M. Schmidt, S. Adiku & Y. Kakubari. 2005. Influences
of environmental factors on the radial profile of sap flux density in Fagus crenata growing at
different elevations in the Naeba Mountains, Japan. Tree Physiol. 25: 545–556.
Kurz-Besson, C., D. Otieno, R. Lobo do Vale, R. Siegwolf, M. Schmidt, A. Herd, C. Nogueira,
T. Soares David, J. Tenhunen, J. Santos Pereira & M. Chaves. 2006. Hydraulic lift in cork
oak trees in a savannah-type Mediterranean ecosystem and its contribution to the local water
balance. Plant and Soil 282: 361–378.
Leal, S., E. Nunes & H. Pereira. 2008. Cork oak (Quercus suber L.) wood growth and vessel
characteristics variations in relation to climate and cork harvesting. Eur. J. For. Res. 127:
33– 41.
Leal, S., V. B. Sousa & H. Pereira. 2006. Within and between-tree variation in the biometry of
wood rays and fibres in cork oak (Quercus suber L.). Wood Sci. Tech. 40: 585–597.
Leal, S., V. B. Sousa & H. Pereira. 2007. Radial variation of vessel size and distribution in cork
oak wood (Quercus suber L.). Wood Sci. Tech. 41: 339–350.
Lewis, A.M. 1992. Measuring the hydraulic diameter of a pore or conduit. Amer. J. Bot. 79:
1158–1161.
Liese, W. & H.E. Dadswell. 1959. Über den Einfluss der Himmelsrichtung auf die Länge von
Holzfasern und Tracheiden. Holz Roh Werkst. 17: 421–427.
Downloaded from Brill.com10/09/2020 10:47:54AM
via free accessBarij, Čermák & Stokes — Azimuthal variation in cork oak wood 39
Lorra, S. & A.F. Kathage. 2004. Sound tomography for stem investigations providing structural
information for stem water/sap flow measurements and analysis. In: Workshop on Wateruse
of Woody Crops, May 20-21, 2004, Ílhavo, Portugal, pp 97–101.
Loustau, D., J-C. Domec & A. Bosc. 1998. Interpreting the variations in xylem sap flux density
within the trunk of Maritime pine (Pinus pinaster Ait.): application of a model for calculating
water flows at tree and stand levels. Ann. Sci. For. 55: 29–46.
Morales, D., M.S. Jimenez, A.M. Gonzalez-Rodriguez & J. Čermák. 2002. Laurel forests in
Tenerife, Canary Islands: Vessel distribution in stems and in petioles of Laurus azorica trees.
Trees: Struct. Func. 16: 529–537.
Muth, C. C. & F. A. Bazzaz. 2002a. Tree seedling canopy responses to conflicting photosensory
cues. Oecologia 132: 197–204.
Muth, C. C. & F. A. Bazzaz. 2002b. Tree canopy displacement at forest gap edges. Can. J. For.
Res. 32: 247–254.
Nadezhdina, N. 2010. Integration of water transport pathways in a maple tree: responses of sap
flow to branch severing. Ann. For. Sci. 67: 107–117.
Nadezhdina, N., J. Čermák & R. Ceulemans. 2002. Radial patterns of sap flow in woody stems
of dominant understorey species: scaling errors associated with positioning of sensors. Tree
Physiol. 22: 907–918.
Nadezhdina, N., M. I. Ferreira, R. Silva & C. Arruda Pacheco. 2008. Seasonal variation of water
uptake of a Quercus suber tree in Central Portugal. Plant Soil 305: 105–119.
Nardini, A., M. A. Lo Gullo & S. Salleo. 1999. Competitive strategies for water availability in
two Mediterranean Quercus species. Plant Cell Environ. 22: 199–116.
Nardini, A. & M.T. Tyree. 1999. Root and shoot hydraulic conductance of seven Quercus species.
Ann. For. Sci. 56: 371–377.
Otieno, D.O., C. Kurz-Besson, J. Liu, M.W. T. Schmidt, R. Vale-do-Lobo, T.S. David, R. Sieg-
wolf, J. S. Pereira & J. D. Tenhunen. 2006. Seasonal variations in soil and plant water status
in a Quercus suber L. stand: roots as determinants of tree productivity and survival in the
Mediterranean-type ecosystem. Plant and Soil 283: 119–135.
Pereira, J. S., M. Conceição & J. M. Rodrigues. 1999. As causas da mortalidade do sobreiro
revisitadas. Rev. Florestal 12: 20–23.
Phillips, N., R. Oren & R. Zimmermann. 1996. Radial patterns of xylem sap flow in non-, diffuse-
and ring-porous tree species. Plant Cell Environ. 19: 983–990.
Roderick, M. L. & S. L. Berry. 2001. Linking wood density with tree growth and environment:
a theoretical analysis based on the motion of water. New Phytol. 149: 473–485.
Silva, S. P., M. A. Sabino, E. M. Fernandes, V.M. Correlo, L.F. Boesel & R.L. Reis. 2005. Cork:
properties, capabilities and applications. Int. Mat. Rev. 50: 345–365.
Sperry, J. S. & J. E.M. Sullivan. 1992. Xylem embolism in response to freeze-thaw cycles and
water stress in ring-porous, diffuse-porous, and conifer species. Plant Physiol. 100: 605–613.
Stokes, A., A. H. Fitter & M. P. Coutts. 1995. Responses of young trees to wind and shading:
effects on root architecture. J. Exp. Bot. 46: 1139–1146.
Tatarinov, F., J. Kučera & E. Cienciala. 2005. The analysis of physical background of tree sap
flow measurements based on thermal methods. Meas. Sci. Technol. 16: 1157–1169.
Thomas, D.S., K.D. Montagu & J. P. Conroy. 2004. Changes in wood density of Eucalyptus
camaldulensis due to temperature - the physiological link between water viscosity and wood
anatomy. For. Ecol. Manage. 193: 157–165.
Downloaded from Brill.com10/09/2020 10:47:54AM
via free access40 IAWA Journal, Vol. 32 (1), 2011
Villar-Salvadore, P., P. Castro-Díez, C. Pérez-Rontomé & G. Montserrat-Martí. 1997. Stem xylem
features in three Quercus (Fagaceae) species along a climatic gradient in NE Spain. Trees:
Struc. Func. 12: 90 –96.
Werner, C. & O. Correia. 1996. Photoinhibition in cork-oak leaves under stress: Influence of the
bark-stripping on the chlorophyll fluorescence emission in Quercus suber L. Trees: Struct.
Func. 10: 288–292.
Wheeler, J. K., J. S. Sperry, U. G. Hacke & N. Hoang. 2005. Inter-vessel pitting and cavitation in
woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off
in xylem transport. Plant Cell Environ. 28: 800–812.
Wieser, G. 2002. The role of sapwood temperature variations within Pinus cembra on calculated
stem respiration: implications for upscaling and predicted global warming. Phyton-Ann.
Rei. Bot. A. 42: 1–11.
Zimmermann, M.H. 1983. Xylem structure and the ascent of sap. Springer-Verlag, New York.
Zwieniecki, M.A., P. J. Melcher & M. Holbrook. 2001. Hydraulic properties of individual xylem
vessels of Fraxinus americana. J. Exp. Bot. 52: 257–264.
Downloaded from Brill.com10/09/2020 10:47:54AM
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