Agricultural and Forest Meteorology 187 (2014) 14–21
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Agricultural and Forest Meteorology
journal homepage: www.elsevier.com/locate/agrformet
Radial pattern of sap flow and response to microclimate and soil
moisture in Qinghai spruce (Picea crassifolia) in the upper Heihe River
Basin of arid northwestern China
Xuexiang Chang ∗ , Wenzhi Zhao, Zhibin He
Cold & Arid Regions Environmental and Engineering Research Institute, Chinese Academy of Sciences, Linze Inland River Basin Comprehensive Research
Station, Key Laboratory of Ecohydrology of Inland River Basin, CAS, Lanzhou 730000, China
a r t i c l e
i n f o
Article history:
Received 13 May 2013
Received in revised form
13 November 2013
Accepted 18 November 2013
Keywords:
Sap flow
Sapwood
Radial pattern
Environmental factors
Qinghai spruce
Upper Heihe River Basin
a b s t r a c t
In order to accurately estimate whole-tree water use and individual tree transpiration, it is important
to have reliable information on radial patterns of sap velocity and responses of sap flow to local environmental conditions. Therefore, variation in sap flow and environmental conditions was investigated
in a mature Qinghai spruce (Picea crassifolia) stands during the growing season of 2011 at the Pailougou
watershed, in Qilianshan Mountain, located in the upper Heihe River Basin, in the arid region of Northwest China. Daily sap flow was measured by the heat-pulse technique on nine trees during the growing
season. It was found that the highest daily sap flow velocity in sap flow radial distribution was at 20 mm
sapwood depth, and that from 10 mm to 20 mm sapwood depth, the daily sap flow velocity gradually
increased, whereas from 20 mm to 40 mm sapwood depth, sap flow velocity gradually diminished. A
simple Gaussian regression model for the radial distribution of sap flux velocity was formulated, which
explained 92% of the radial profile variation of sap flow velocity. Sap flow velocity was heightened by
increasing the global short-wave radiation (R, W m−2 ), vapour pressure deficit (D, kPa), and air temperature (T, ◦ C) when R < 800 W m−2 , D < 1.4 kPa, and T < 18.0 ◦ C. It is, however, inherently difficult to establish
firm relationships between sap flow velocity and R, D, and T because of the complex crown environment.
The correlation of daily sap flow velocity to soil moisture content on a clear day was fitted by a logistic
regression. We conclude that measurement of radial flow pattern provides a reliable method of integrating sap flow from individual measuring points to the whole tree. And D, R, T and soil moisture had varying
influences on sap flow velocity in the Qinghai Spruce.
© 2013 Elsevier B.V. All rights reserved.
1. Introduction
Many researchers need accurate estimates of whole-tree water
use in order to assess individual tree transpiration, to scale to stand
and catchment-level transpiration, and to understand the contribution of trees to total ecosystem transpiration (Ford et al., 2008;
Mitchell et al., 2009). To estimate whole-tree transpiration, the
measurement of sap flow provides a widely applicable method
(Ćermák and Nadezhdina, 1998; Köstner et al., 1998; Wullschleger
et al., 1998). In forest environments, sap flow approaches offer the
dual advantages of practicality and repeatability of measurements
(Dragoni et al., 2009). Furthermore, these techniques can provide
critical insights into the effects of spatio-temporal shifts in environmental conditions on the temporal dynamic of sap flow, sap
∗ Corresponding author. Tel.: +86 931 4967129.
E-mail address: [email protected] (X. Chang).
0168-1923/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.agrformet.2013.11.004
velocity and xylem properties in woody trees (Ford et al., 2004b;
Kubota et al., 2005; Kumagai et al., 2007; Fiora and Cescatti, 2008).
The common sap flow methods include heat pulse (Swanson and
Whitfield, 1981; Edwards and Warwick, 1984; Edwards et al., 1996;
Vertessy et al., 1997; Čermák et al., 2004; Chang et al., 2006),
stem segment heat balance (Čermák et al., 1998; Cienciala et al.,
1992; Jiménez et al., 1996), heat dissipation (Granier, 1985; Loustau
et al., 1998; Meinzer et al., 2001; Bush et al., 2010), and heat field
deformation (Čermák et al., 1998; Meiresonne et al., 1999; Čermák
and Nadezhdina, 2000). However, sap flow rates are rarely uniform across the sapwood area because conducting properties vary
widely as wood ages, partly because of the consequent increase in
trunk diameter (Edwards and Booker, 1984; Čermák et al., 1992;
Granier et al., 1994; Phillips et al., 1996; Jiménez et al., 2000;
Nadezhdina et al., 2002). Therefore, successful application of each
of these methods depends on knowledge of the conduction systems of the trees, namely the depth of the sapwood and the radial
pattern of sap velocity along the xylem radius.
At the scale of individual trees, measuring transpiration has
the theoretical advantage of preserving vital information on
X. Chang et al. / Agricultural and Forest Meteorology 187 (2014) 14–21
important plant–environment functional links (Oren et al., 1998;
Wilson et al., 2001; Wullschleger et al., 2001; Meinzer et al.,
2001; Loranty et al., 2008). Sap flow in co-existing tree species
often shows species-specific responses to variation in microclimatic and edaphic parameters, including radiation, vapour
pressure deficit (D), rainfall, temperature, wind speed, soil moisture, and leaf wetness (Meinzer et al., 1993; Granier et al., 1996;
Wullschleger et al., 2000; Oren and Pataki, 2001; Lagergren and
Lindroth, 2002; Pataki and Oren, 2003; O’Brien et al., 2004; Kubota
et al., 2005; Gazal et al., 2006; Asbjornsen et al., 2007; Loranty
et al., 2008). The integrated impact of environmental variables,
therefore, is what actually drives sap flux responses at the wholetree level, and exploiting the underlying structure of co-varying
weather data to predict whole-tree sap flux responses could be
an effective approach, especially for comparing species-specific
responses.
Situated at northwest arid region of China and surrounded by
desert and Gobi, Qilian Mountains receive higher precipitation and
play a role in supplying water to lowlands. Many inland rivers,
such as Shiyanghe river, Heihe river and Shulehe river, originate
from Qilian Mountains. Forest vegetation of Qilian Mountain is
not only valuable forest resource, but also have the ecological
function of water reservation which is very important for retain
oasis ecosystem of middle and lower reaches of inland river system. Qinghai spruce (Picea crassifolia) is the dominant tree species
in Qilian Mountains. In the upper Heihe Basin, Qinghai spruce
forests occupies about 25% of the total forest area and 78% of arbor
stand. To this type, it is important to understand physiological
processes and components of the water balance in stands, and
understanding water use in Qinghai spruce trees is the first and
crucial step.
The main study objectives were: (1) to determine the spatial distribution of sap velocities in Qinghai spruce stems, in
order to describe and analyze its radial profile; (2) to detect
the probe inserted depth, in order to make accurate estimate
of whole-tree water use; (3) to characterize the effects of climatic factors (e.g., vapor pressure deficits, temperature, radiation,
wind, precipitation) and soil moisture on Qinghai spruce sap
flow.
15
2. Materials and methods
2.1. Site description and environmental conditions
This study was carried out on Qilianshan Mountain, located
in the upper Heihe River Basin, in pure stands of P. crassifolia
located on a bench within a north-facing slope at 2800 m elevation in the Pailougou watershed (100◦ 17 E, 38◦ 24 N) (Fig. 1),
50 km south of Zhangye, Gansu province, during the 2011 growing season. From 1994 to 2010, the mean annual air temperature
was 0.5 ◦ C, the mean maximum and minimum temperatures was
28.0 ◦ C and −36.0 ◦ C, respectively. Annual precipitation is between
290.2 mm and 467.8 mm, with rainfall occurring mainly from June
to September (60.0% of the annual total). The pan evaporation was
1051.7 mm.
The frost-free period was about 165 days per year.
The forest in the watershed consists mainly of Qinghai spruce
(P. crassifolia) stands ranging from 80 to 120 years old. The stand
density was 1100 trees/ha, leaf area index (LAI) of stand was 1.84.
Average tree height was 11.8 ± 2.8 m and the average diameter at
breast height (DBH ) was 18.2 ± 6.5 cm. Moss (Abietinella abietina)
covered the entire forest floor. Moss is 10 cm to 20 cm tall and about
95% coverage. In the forest floor, there was no herbaceous vegetation and Qinghai spruce seedlings. The soil is gray-drab with a field
water capacity of 53.8%, a total porosity of 71.4%, a bulk density of
850 kg m−3 , and a soil depth of 0.7 m.
2.2. Meteorology and soil moisture content measurements
Meteorological variables were measured from two weather
stations—one positioned in the forest, and another at 100 m distance from the forest boundary. The global short-wave radiation
(R, W m−2 ) was measured in the open, 100 m distant from the forest boundary, with a pyranometer (CM7B, Kipp & Zonen, Delft,
Netherlands). In the forest area, net downward radiation (Rn,
W m−2 ), air temperature (T, ◦ C), humidity, and wind speed were
measured. Net downward radiation was measured by means
of the radiation balance sensor (Net radiometer 8110, Philipp
Schenk, Wien, Austria). A shielded combination capacitive relative
humidity sensor thermistor probe (HMP35C, Campbell Scientific,
Fig. 1. Map of the Heihe River Basin and its location in China.
16
X. Chang et al. / Agricultural and Forest Meteorology 187 (2014) 14–21
Table 1
Biometric and physiological parameters of sap flow measurements.
No.
Diameter breast height(mm)
Height (m)
Crown Width (m)
Sapwood radius (mm)
Bark depth(mm)
Heartwood radius (mm)
Sapwood area(mm2 )
1
2
3
4
5
6
7
8
9
142.0
205.0
127.0
164.0
211.0
231.0
181.0
276.0
320.0
13.5
14.5
8
12.5
12.5
14.4
12.5
15.8
16.2
3.3
3.9
3.6
4.4
4.5
4.6
3.2
3.3
4.8
32
37
30
33
38
39
35
44
40
7
7
7
7
7
7
7
7
7
32
59
26
42
61
69
49
87
113
9566
17,882
7,892
12,224
18,792
21,992
14,454
30,186
33,410
Inc., Logan, Utah) monitored relative humidity and air temperature
at the height of 1.6 m. Wind speed and wind direction were measured at the height of three meters with a Rotronic sensor (RS2
rotronic AG, Bassersdrof, Switzerland). These factors were measured every 5 min, and then the mean 30-min values were stored
in a datalogger. The precipitation was manually recorded twice a
day (at 08:00 and 20:00 local time, respectively) at a meteorological
station 100 m distant from the forest boundary at 2750 m elevation
above sea level.
The soil moisture content (S, m3 m−3 ) was continuously monitored at a single location with EM50 (Decagon, Inc. Decagon, USA)
after 26 June 2011, and calibrated against the gravimetric method.
There are 5 probes in EM50, and they were set up at depths of 0.2 m,
0.3 m, 0.4 m, 0.5 m, and 0.6 m.
2.3. Sap flow
Two sets of SF-300 heat pulse meters (Greenspan Technology
Pty Ltd., Warwick, Queensland, Australia), with a total of eight
probes (i.e., one per tree), were used to measure sap flow in
individual trees. When installing the probes, the bark of the
sample tree was removed at breast height to expose the cambium.
Between May 25th and June 1st 2011, the largest diameter (No. 9,
Table 1) at breast height was selected at Qinghai spruce forest in
the Pailougou watershed, and the seven probes were implanted
at depths of 10 mm, 20 mm, 30 mm, 40 mm, 50 mm, 60 mm and
70 mm in the xylem of this sample tree in order to determinate
sapwood width. When the probe implanted at a depths, the sap
flow velocity showed fluctuated the same range, as the sap flow
velocity measured by the probes inserted at 10 mm trunk depths
at night. And this depth was determined as sapwood width. After
sapwood width was determined, every probe were re-implanted
at depths of 10 mm, 15 mm, 20 mm, 25 mm, 30 mm, 35 mm, and
40 mm into the xylem of this sample tree (between June 1st and
June 11th 2011) in order to investigate the radial profile of sap flux
density in the tree, and to confirm the probe-inserted depth for
accurate estimates of whole-tree water use. To monitor sap flow
after 12 June 2011, a total of eight probes were installed at 25 mm
depth into the xylem of each sample tree (No. 1 and 8, Table 1),
to cover the range of diameters found in more than 91% of all the
trees in the Qinghai Spruce forest, in our vegetation surveys. The
wound diameter was 2.2 mm. To avoid the sun-exposed side of
the trunk, all sensors were placed on the north-facing side of the
trees. Before insertion, each probe was coated with silicone gel
to ensure good thermal contact between the probe elements and
the sapwood, and after insertion, the exposed cambium was also
covered with silicon gel to reduce evaporation from the wood
surface, followed by aluminum foil to reduce the effects of ambient
temperature fluctuations and solar radiation.
Each probe utilized two sensor probes and a heater probe. The
upstream sensor probe was located 5 mm below the heater probe
and the downstream sensor probe is 10 mm above the heater probe.
On each sensor probe, there are two thermistors. The first was positioned 5 mm from the end of the probe, the second, 5 mm behind
the first. The thermistors were paired on a vertical plane to facilitate
measurement of sap flow velocity. Heat pulses lasting 1.6 s were
produced by the heater probe. Sap flow velocity (Vs , mm h−1 ) was
calculated following the method of Edwards and Warwick (1984).
Vs = Vh (0.505Fm + Fi )
where V
(1)
−1
h (mm h ) is the heat pulse velocity, Fm
is the volume fraction of the woody material, and Fi is the volume fraction of water.
Calculation of Fm and Fi for each tree required the following inputs:
fresh weight (Wf , kg), oven-dried weight (Wd , kg), and weight of
water in the same volume as the sapwood sample (Wi , kg). On this
basis, Fm is
Fm =
Wd
1620Wi
(2)
and Fi is
Fi =
Wf − Wd
(3)
Wi
Sapwood sample was selected with 5 times replication from
sample Tree 9, and measured its fresh weight, oven-dried weight
at 80 ◦ C, and weight of water in the same volume as the sapwood
sample. Then Fm and Fi was calculated. When Calculation of Vs , the
average of Fm and Fi was used. The average of Fm and Fi was 0.36
and 0.27, respectively.
Sap flux (Q, mm3 h−1 ) is a function of the velocity of sap flow
and the area of conducting wood in which the flow occurs
Q = Vs Ac
(4)
where Ac (mm2 ) is the area of conducting wood (Closs, 1958).
Table 2
Minimum, maximum, and mean half-hourly weather variables during the growing season (mean ± S.D.).
Month
June
July
Aug.
Sept.
Oct.*
*
Air temperature (◦ C)
Global shortwave
radiation (W m−2 )
Vapour–pressure deficit (Pa)
Wind speed (m s−1 )
Precipitation
(mm)
Mean
Max.
Mean
Min.
Max.
Mean
Min.
Max.
Mean
Min.
Max.
401.8 ± 188.7
419.8 ± 185.8
402.4 ± 185.4
338.9 ± 159.4
397.1 ± 74.4
1315
1206
1179
957
832
14.0 ± 2.7
14.8 ± 3.3
13.7 ± 3.2
7.2 ± 2.4
4.1 ± 2.2
10.0
7.5
7.4
2.3
−1.8
19.6
20.3
21.2
12.1
8.8
773 ± 497
989 ± 547
706 ± 516
322 ± 185
455 ± 215
82.4
3.2
0
4.2
72.2
1747
1824
1947
691
844
0.7 ± 0.2
0.7 ± 0.1
0.7 ± 0.1
0.6 ± 0.1
0.7 ± 0.1
0.4
0.5
0.4
0.4
0.5
2.0
1.9
1.5
1.6
1.5
The first 10 days of October.
62.3
42.4
109.5
49.3
7.4
X. Chang et al. / Agricultural and Forest Meteorology 187 (2014) 14–21
3. Results
18
17
10 mm
20 mm
30 mm
40 mm
50 mm
A
3.1. Weather and soil water content
15
12
9
6
Sap flow velocity ( kg h-1)
The variations in daily weather variables for each month during
the growing season are summarized in Table 2. A diurnal minimum
temperature of 2.3 ◦ C was observed in September and a maximum
of 21.2 ◦ C was recorded in August. August had both the highest
(D = 1947 Pa) and the lowest (0.0 Pa) values of vapour-pressure
deficit. Daytime maximum global shortwave radiation ranged from
832 W m−2 in September to 1315 W m−2 in July. Wind speed was
between 0.4 m s−1 and 2.0 m s−1 . A total rainfall of 263.5 mm was
recorded during the 2011 growing season. About 70% of the total
annual rainfall was observed between June and September, with
the highest monthly total (109.5 mm) occurring in August.
Table 2 The volumetric soil moisture content of the Qinghai
spruce forest ranged from 0.13 to 0.20 m3 m−3 , with a mean value
of 0.16 ± 0.02 m3 m−3 during the growing season.
3.2. Sap flux density radial profiles
Vsd = 107.54 +
654.77
6.72
⁄2
e
−2(d−20.09)2
45.16
(R2 = 0.92, n = 7)
where d is sapwood depth from the cambium, and Vsd is daily sap
flow velocity at d mm depth in the sapwood.
0
00:00
06:00
12:00
18:00
00:00
25
10 mm
15 mm
20 mm
25 mm
30 mm
35 mm
40 mm
B
20
15
10
5
0
06:00
12:00
18:00
00:00
06:00
12:00
18:00
00:00
Time
200.0
C
175.0
Sap flow velocity(kg d-1)
The largest sampled tree had a diameter of 32.0 cm at breast
height and a 16.2 m overall height (Table 1); probes were inserted
at 10 mm, 20 mm, 30 mm, 40 mm, 50 mm, 60 mm and 70 mm depth.
Diurnal data from the probes inserted in the trunk at depths of
10 mm, 20 mm, 30 mm, and 40 mm showed that sap flow velocity was lower at night, that it increased sharply at 7:30, reached
its maximum value between 12:00 and 14:00, and then decreased
between 16:00 and 18:30 (Fig. 2a). However, diurnal data from
the probes inserted in the trunk at depths of 50 mm, 60 mm,
and 70 mm showed that sap flow velocity fluctuated throughout the day between 2.0 kg h−1 and 4.0 kg h−1 —the same range as
the sap flow velocity measured by the probes inserted at 10 mm,
20 mm, 30 mm, and 40 mm trunk depths at night (Fig. 2a). From
these results it can be concluded that the sampled tree sapwood width was 40 mm. When the probes were re-inserted at
trunk depths of 10 mm, 15 mm, 20 mm, 25 mm, 30 mm, 35 mm
and 40 mm, it can be seen that the sap flow velocity increased
first and then decreased; significantly higher measurements were
observed at the depth of 20 mm (Fig. 2b). Between 10 mm and
20 mm depth in the sapwood, the daily sap flow velocity was
gradually increasing, with flow velocities of 115.3 ± 22.6 kg d−1 ,
131.4 ± 36.2 kg d−1 , 185.6 ± 53.7 kg d−1 , at 10 mm, 15 mm and
20 mm, respectively. However, in the range from 20 mm to 40 mm
sapwood, sap flow velocity gradually diminished; sap flow velocity was 185.6 ± 53.7 kg d−1 , 133.5 ± 28.3 kg d−1 , 113.3 ± 17.7 kg d−1 ,
108.1 ± 16.4 kg d−1 and 96.6 ± 12.3 kg d−1 , at each 5 mm step,
respectively. It is noteworthy, however, that the flow velocity range
was largest between 15 mm and 20 mm, and between 20 mm and
25 mm. Average Sap flow velocity in different sapwood depth was
126.3 kg d−1 . This is the nearest approximation of sap flow velocity
at 25 mm sapwood depth. So, the probes were implanted at 25 mm
sapwood depth to measure Qinghai spruce sap flow. Consequently,
the daily sap flow velocity was overestimated about 5.6%. When
the sap flow velocity was plotted against sapwood depth, then fit
to the following Gaussian function, this simple Gaussian regression
of sap flow velocity to sapwood depth explained 92% of the radial
profile variation of sap flow velocity (Fig. 2c). This method resulted
in a general radial profile function, given by:
3
150.0
125.0
100.0
10
20
30
40
Depth(mm)
Fig. 2. Location of heartwood/sapwood boundary and spatial pattern of trunk water
transfer for Picea crassifolia. (A) Heartwood/sapwood boundary of the P. crassifolia trunk determined the position. (B) The sap flow velocity comparison at various
depths of the P. crassifolia sapwood. (C) Sap flow velocity radial variation patterns
of trunk water transfer for P. crassifolia.
3.3. Sap flow response to environmental variation
Sap flow is greatly affected by meteorological factors such as
solar radiation intensity, air humidity and temperature, etc. Sap
flow velocity for individual Qinghai spruce trees was averaged to
calculate mean sap flow velocity on a sapwood area basis (Vss ). The
daily variation in Vss was closely related to changes in solar radiation intensity, air temperature and vapour pressure deficit. June 24,
July 24, August 24 and September 24 were sunny days. The daily
18
X. Chang et al. / Agricultural and Forest Meteorology 187 (2014) 14–21
10.0
8.0
6.0
4.0
2.0
0
150
300
450
600
750
-2
Global short-wave radiation(W m )
Sap flow velocity ( kg m-2 h-1)
10.0
8.0
6.0
4.0
2.0
Fig. 3. Diurnal course of mean sap flow as a function of (A) global shortwave radiation, (B) temperature, and (C) vapour-pressure deficit on 24 Jun., Jul., Aug., and Sept.
2011. Characteristics of the eight sample trees are presented in Table 1 (No. 1 and
8). Vertical bars represent the standard deviation around the mean for sap flow.
8.0
10.0
12.0
14.0
16.0
18.0
Temperature(°C)
10.0
variation in Vss was closely related to changes in R, D, and T, and
the course of R, D, and T was in accord with variations in sap flow
velocity. Sap flow velocity rose with increasing R, D, and T when
R < 800 W m−2 , D < 1.4 kPa, and T < 18.0 ◦ C, and when R > 800 W m−2 ,
D > 1.4 kPa, and T > 18.0 ◦ C. However, Vss did not increase with
R, D, or T (Fig. 3); rather, R, D, and T peaked slightly after Vss
(Fig. 3). On June 24, July 24, August 24 and September 24, R peaked
between about 13:00 and 13:30, D between about 11:30 and 14:00,
and T between about 14:30 and 15:30; whereas Vss peaked at
between about 10:30 and 12:00. The maximum daytime values
for R were 1009.00 W m−2 , 1108.00 W m−2 , 1152.00 W m−2 and
757.00 W m−2 , respectively; versus 1.81 kPa, 1.95 kPa, 0.98 kPa and
0.55 kPa for D; 20.60 ◦ C, 23.18 ◦ C, 15.70 ◦ C and 11.10 ◦ C for T; and
90.28 ± 28.59, 66.57 ± 16.03 kg m−2 h−1 , 88.75 ± 22.09 kg m−2 h−1
and 67.43 ± 17.25 kg m−2 h−1 for Vss , respectively. Although Sap
flow velocity rose with increasing R, D, and T when R < 800 W m−2 ,
D < 1.4 kPa, and T < 18.0 ◦ C, it did show statistical significance linear
correlation between sap flow velocity and R, explained 54% and 68%
of the variation of Vss in about 0.14 m3 m−3 soil moisture content
condition and about 0.18 m3 m−3 soil moisture content condition
(Fig. 4A), respectively. In the 0.18 m3 m−3 soil moisture content
conditions, the significance linear relationship between sap flow
velocity and T, and D was showed, explained 50% and 34% of the
variation of Vss , respectively; but no observed significant correlation of Vss to T, and D in about 0.14 m3 m−3 soil moisture content
condition (Fig. 4B and C).
Mean sap flow velocity Vss for Qinghai spruce is shown in
Fig. 5A. The mean values of Vss were between 27.8 ± 2.3 kg m−2 h−1
8.0
6.0
4.0
2.0
0.0
300.0
600.0
900.0
1200.0
Vapour Pressure deficit (Pa )
Fig. 4. Relation sap flow velocity on a sapwood area and meteorology factor, such
as vapour pressure deficit (D), global short-wave radiation (R), air temperature
(T). (A) Dependence on R. (B) Dependence on T (C) Dependence on D. Fit curves
between Vss and R, T, D are shown, bole line in about 0.14 m3 m−3 and short dash
line in about 0.18 m3 m−3 soil moisture content conditions. Subscript 1 and 2 are in
about 0.14 m3 m−3 and 0.18 m3 m−3 soil moisture content conditions, respectively.
Dot symbols represent in about 0.14 m3 m−3 and square symbols show in about
0.18 m3 m−3 soil moisture content conditions.
X. Chang et al. / Agricultural and Forest Meteorology 187 (2014) 14–21
=
−
+
Fig. 5. (A)The diurnal mean sap flow velocity on a sapwood area basis (Vss ,
kg m−2 h−1 ) for P. crassifolia trees (stripped vertical lines) and daily precipitation(vertical lines) and (B)the daily soil moisture content during the growing season
in 2011. The bars represent the standard deviation about the mean. (C) Relationships between sapflow velocity and soil moisture content on sunny days during the
growing season in 2011.
and 65.1 ± 19.2 kg m−2 h−1 from June 12 to October 16. After
precipitation of 7.7 mm on 22 June, the mean of Vss rose from
46.8 ± 12.3 kg m−2 h−1 to 56.6 ± 15.3 kg m−2 h−1 on 23 June. Due to
continuous rain from 28 June to 5 July, with a cumulative precipitation of 33.4 mm, the mean of Vss reached 65.1 ± 19.2 kg m−2 h−1 ,
then fell gradually to 41.4 ± 5.9 kg m−2 h−1 by 22 July. And after
continuous rain in the middle of August, the mean of Vss rose again,
to 53.2 ± 10.6 kg m−2 h−1 , and then fell gradually. With these fluctuating rain events, the soil moisture content frequently increased
and diminished (Fig. 5B), as evidenced in the variation in the mean
of Vss . On clear days, Vsd showed an increasing tendency when soil
moisture content (S, m3 m−3 ) was going up (Fig. 5C). The correlation of Vsd to soil moisture content on a clear day was fitted by
a logistic regression, which explained 84% of the variation of Vsd ,
given by
Vsd = 8.44 −
1+
4.11
16.50
S
0.15
R2 = 0.84, n = 93
4. Discussion
To estimate whole-plant water use from the trunk vs , one must
first estimate Q as the product of trunk vs and Ac . Thus, if the trunk vs
varies radially, one must know its radial distribution to accurately
19
estimate sap flow mass. Much work has been conducted on vs radial
variation of coniferous species. Mark and Crews (1973) studied vs
of the radial profile of two Picea engelmannii Parry ex Engelm. and
two Pinus contorta Dougl. ex Loud., and found that vs peaked at
24 mm into the xylem and declined toward the heartwood. Čermák
et al. (1992) confirmed that the radial profile of vs was symmetrical
in Norway spruce (Picea abies (L.) Karst.); that maximum flow
velocity was in the center of the conducting xylem and tailed with
low amplitude in the direction of the cambium and heartwood and
was highly asymmetrical in oak (Quercus robur L.) trees, reaching
a peak at the youngest growth ring and tailing centripetally for
about 10 rings. In Scots pine, the position of maximum sap flow
was more variable in the outer sapwood layers than in the deeper
sapwood layers (Nadezhdina et al., 2002). The vsd of maritime pine
(Pinus pinaster Ait.) declined with increasing sapwood depth, but
the decrease was steeper in trees with large diameters (Delzon
et al., 2004). Irvine et al. (2004) reported on the decline in sap flux
with sapwood depth for ponderosa pine trees (Pinus ponderosa
Dougl. ex P. Laws.). Ford et al. (2004a) found the expected pattern
of high vsd near the cambium and decreasing vsd with depth toward
the center of the southeastern pine (Pinus spp.). For Pinus taeda L.
trees, sap flow occurred maximally in the outer 4 cm of sapwood
and decreased toward the center (Ford et al., 2004b). Kubota et al.
(2005) found that the radial pattern of vsd reached a maximum just
behind the cambium layer and then decreased exponentially in
Japanese beech trees (Fagus crenata Blume). Kumagai et al. (2007)
reported on the decrease in vsd with increasing sapwood depth in
a Japanese cedar (Cryptomeria japonica D. Don). Flora and Cescatti
(2008) reported that sap flux density decreased with depth in the
xylem, but with a secondary peak at a depth of 20–30 mm beneath
the cambium, in a 35-year-old Norway spruce (P. abies). For the
Qinghai spruce tree, the radial pattern of sap flux density vsd was
highest near 20 mm of sapwood depth, with sap flow velocity
gradually increasing from the cambium to a sapwood depth of
20 mm and then decreasing with depth toward the heartwood, as
previously studied in Mark and Crews (1973), Čermák et al. (1992),
Nadezhdina et al. (2002), Ford et al. (2004a, 2004b). This could
be a result of differences in radial profiles of sapwood hydraulic
conductivity among the trees (Spicer and Gartner, 2001), or agerelated changes might cause the inner xylem to be nonfunctional
or to have a higher hydraulic resistance than when first formed
(Ford et al., 2004a). Tracheids and bordered pit membranes closer
to the heartwood may gradually experience chemical or biological
changes that add resistance to flow. Mark and Crews (1973) found
that bordered pit membranes in P. engelmannii and P. contorta
trees were most open at a xylem depth of 24 mm and became
progressively blocked and encrusted as distance to the heartwood
decreased. Older tracheids may also be damaged and nonfunctional
as a result of repeated unrepaired cavitation events that reduce
sapwood water content. Older xylem elements have been shown to
be more vulnerable to embolism as a result of increased pit membrane permeability to air (Sperry et al., 1991). Obtaining accurate
descriptions of the radial profile of sap velocity, Ford et al. (2004b)
used a 3-parameter Gaussian distribution to model the variability
in the radial profile of vs in four different pine species. Kubota
et al. (2005) applied a Weibull function to describe the radial sap
velocity in the Japanese beech tree. For the Qinghai spruce, one of
the parameters of the Gaussian function was applied to model the
radial pattern of vs , the model appear to be close to Ford made.
The integrated impact of the trees physiology and environmental factors is what actually drives sap flux responses at the
whole-tree level. Granier et al. (1992) demonstrated the inhibiting
effect of D > 4 hPa for tropical rain forest species, and Meinzer et al.
(1993) found this strong limitation of transpiration with increasing D resulted from progressive stomatal closure with increasing D
after D was over 1.5 kPa observed during the dry season in the moist
20
X. Chang et al. / Agricultural and Forest Meteorology 187 (2014) 14–21
forests of Central and northern South America. Fetcher et al. (1994)
found that a D greater than 1 kPa reduced stomatal conductance in
Pentaclethra macroloba in Costa Rican rain forests. In a Panamanian
forest, Phillips et al. (1999) found that sap flow in lianas and trees
was more closely related to D than to R on a daily basis, while during
the diurnal course, tree sap flow was most tightly associated with
R. Wullschleger et al. (2000) reported that sap flow in canopy dominant and codominant Acer rubrum was strongly correlated with
both solar radiation and D in an upland oak forest in Tennessee,
U.S.A. Pataki et al. (2000) and Ewers et al. (2002) found that the relationship between sap flow and D was a nonlinear curve, with sap
flow initially increasing, eventually reaching saturation (plateau)
and often declining at high D as a result of stomatal closure. Pataki
and Oren (2003) reported that solar radiation was more important
in controlling stomatal conductance of Liquidambar styraciflua, a
shade-intolerant species of bottomland eastern deciduous forests,
compared to that of four other shade-tolerant species, which
showed stronger correlations with D. O’Brien et al. (2004) observed
that sap flow was positively correlated with higher irradiance, D,
temperature, and wind speed, but negatively correlated to leaf wetness at the La Selva Biological Station in north-eastern Costa Rica.
Asbjornsen et al. (2007) detected that sap flow had the strongest
positive correlation with solar radiation but a negative correlation
with wind speed, and that sap flow diminished at high D. Gyenge
et al. (2008) and Fernández et al. (2009) found that the exotic Douglas fir had higher water use with lower sensitivity to D. Horna
et al. (2011) found that daily sap flux density correlated better with
atmospheric vapor pressure deficit than with shortwave radiation,
in spite of the permanently high atmospheric humidity. Du et al.
(2011) found that vapor pressure deficit, solar radiation and soil
moisture had varying influences on sap flux velocity in the species
and that normalized sap flux velocity values could be fitted to D
using an exponential saturation function. In our study, although
sap flow velocity was heightened with increasing R, D, and T when
R < 800 W m−2 , D < 1.4 kPa, and T < 18.0 ◦ C, it is inherently difficult
to establish firm relationships between sap flow velocity and R, D,
and T because of a complex environment, because the integrated
impact of these factors is what actually drives sap flux responses at
the whole-tree level (O’Brien et al., 2004).
A number of studies have reported an observed decrease in JS
as a result of declines in soil moisture for a variety of species (Gazal
et al., 2006; Lagergren and Lindroth, 2002; Oren and Pataki, 2001;
Pataki et al., 2000; Oren et al., 1996). Ćermák et al. (1995) found
that the relative transpiration of pine increased 3.5 times while
that of spruce increased 5.4 times after rains. Hölscher et al. (2005)
failed to confirm a correlation between drought sensitivity and the
relative reduction in sap flow in dry periods. Chang et al. (2006)
found that the sap flow of Gansu Poplar (Populus gansuensis C. Wang
and H. L. Yang) in a shelter belt experienced a remarkable increase
after the shelter belt was irrigated. Because of the larger rain and
irrigation events, soil moisture content increased significantly.
Köcher et al. (2009) found that less drought-sensitive species of
ash, hornbeam and little-leaf linden showed a lower reduction in
Js with decreasing soil water content. Horna et al. (2011) showed
no effect on mean daily sap flux density because soil moisture did
not vary significantly. To a certain extent, this is due to the species’
capability to ensure water uptake under decreasing soil moisture
content. Tree species confronted with water stress will incur structural or physiological adjustment in order to maintain the integrity
of the hydraulic system and to enable carbon assimilation despite
substantial water losses and a marked deterioration of plant
water status (Bréda et al., 2006). In this study, a logistic functional
relationship was established between sap flow and soil moisture
content, and the models of sap flow velocity to soil moisture content variable explained 84% of the variation of sap flow velocity and
showed large sensitivities. However, only one tree was selected
for sap flow measurement, and EM50 was stalled near the foot of
the tree. This method took no account of the heterogeneity of soil
properties or soil moisture, although it was known that there was
a large spatial variation in soil properties and soil moisture within
the forest land.
5. Conclusions
Sap flow radial distribution patterns are the key to obtaining
more accurate estimates of whole-tree and stand transpiration.
This study showed that sap flow radial distribution in the Qinghai Spruce tree was one of the parameters of the Gaussian function
model.
At the whole-tree level, the integrated impact of environmental
factors is what actually drives sap flux. This study showed that D,
R, T and soil moisture had varying influences on Vss in the Qinghai Spruce. The relationship between sap flow and soil moisture
content was established as a logistic function, although it was a
result at a single tree level. For future studies, it is important to
add the heterogeneity of soil properties and soil moisture in order
to research the relationship between the variation of soil moisture
content and sap flow, and to pursue efforts to characterize relationships between sap flow velocity and environmental drivers, in order
to obtain more accurate estimates of stand transpiration, and to
develop ecological and physiological research on Qinghai Spruce, in
order to have a comprehensive understand more about the Qinghai
Spruce forest hydrologic process, for it be going to provide further
theoretical support for forest management in arid regions.
Acknowledgements
This study was funded under the National Science Foundation of
China project (91025017; 91025014), the Hundred Talents Program
of the Chinese Academy of Sciences (29Y127D11) and the Open
Foundation of Key Laboratory of Ecohydrology of Inland River Basin
(90Y229F51). The authors thank the anonymous reviewers for their
critical review and comments on this manuscript.
References
Asbjornsen, H., Tomer, M.D., Gomez-Cardenas, M., Brudvig, C.M., Greenan, L.A.,
Schilling, K., 2007. Tree and stand transpiration in a Midwestern bur oak savanna
after elm encroachment and restoration thinning. Forest Ecol. Manage. 247,
209–219.
Bréda, N., Huc, R., Granier, A., Dreyer, E., 2006. Temperate forest trees and stands
under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann. For. Sci. 63, 625–644.
Bush, S.E., Hultine, K.R., Sperry, J.S., Ehleringer, J.R., 2010. Calibration of thermal
dissipation sap flow probes for ring- and diffuse-porous trees. Tree Physiol. 30
(12), 1545–1554.
Ćermák, J., Cienciala, E., Kućera, J., 1995. Individual variation of sap-flow rate in
large pine and spruce trees and stand transpiration: a pilot study at the central.
J. Hydrol. 168, 109–120.
Čermák, J., Cienciala, E., Kučera, J., Hallgren, J.E., 1992. Radial velocity profiles of
water flow in trunks of Norway spruce and oak and the response of spruce to
severing. Tree Physiol. 10, 367–380.
Čermák, J., Kuèera, J., Nadezhdina, N., 2004. Sap flow measurements with some thermodynamic methods, flow integration within trees and scaling up from sample
trees to entire forest stands. Trees 18, 529–546.
Ćermák, J., Nadezhdina, N., 1998. Brief review of present techniques used for sap flow
measurements in intact plants. In: Ćermák, J., Nadezhdina, N. (Eds.), Proceedings
of the Fourth International Workshop on Measuring Sap Flow in Intact Plants.
IUFRO Publications, Publishing House, Mendel University, Brno, Czech Republic,
pp. 4–11.
Čermák, J., Nadezhdina, N., 2000. Water relations in mixed versus pure stands.
In: Hasenauer, H. (Ed.), Proceedings of the International Conference on Forest Ecosystem Restoration. Ecological and Economical Impacts of Restoration
Processes in Secondary Coniferous Forests. Institute of Forest Growth Research,
pp. 70–76.
Čermák, J., Nadezhdina, N., Raschi, A., Tognetti, R., 1998. Sap flow in Quercus
pubescens and Q. cerris stands in Italy. In: Čermák, J., Nadezhdina, N. (Eds.),
Proceedings of the Fourth International Workshop on Measuring Sap Flow in
Intact Plants. IUFRO Publications. Mendel University, Brno, Czech Republic, pp.
134–141.
X. Chang et al. / Agricultural and Forest Meteorology 187 (2014) 14–21
Chang, X., Zhao, W., Zhang, Z., Su, Y., 2006. Sap flow of the Gansu Poplar shelter-belt
in arid region of Northwest China. Agric. For. Meteorol. 138, 132–141.
Cienciala, E., Lindroth, A., Čermák, J., Hallgren, J.-E., Kuèera, J., 1992. Assessment of
transpiration estimates for Picea abies trees during a growing season. Trees 6,
121–127.
Closs, R.L., 1958. The heat pulse method for measuring rate of sap flow in a plant
stem. N. Z. J. Sci. 1, 281–288.
Delzon, S., Sartore, M., Granier, A., Loustau, D., 2004. Radial profiles of sap flow with
increasing tree size in maritime pine. Tree Physiol. 24, 1285–1293.
Dragoni, D., Caylor, K.K., Schmid, H.P., 2009. Decoupling structural and environmental determinants of sap velocity. Part II. Observational application. Agric. For.
Meteorol. 149, 570–581.
Du, S., Wang, Y., Kume, T., Zhang, J., Otsuki, K., Yamanaka, N., Liu, G., 2011. Sapflow
characteristics and climatic responses in three forest species in the semiarid
Loess Plateau region of China. Agric. For. Meteorol. 151, 1–10.
Edwards, W.R.N., Warwick, N.W.M., 1984. Transpiration from a kiwi fruit vine as
estimated by the heat pulse technique and the Penman–Monteith equation. N.Z.
J. Agric. Res. 27, 537–543.
Edwards, W.R.N., Becker, P., Èermák, J., 1996. A unified nomenclature for sap flow
measurements. Tree Physiol. 17, 65–67.
Edwards, W.R.N., Booker, R.E., 1984. Radial variation in the axial conductivity of
Populus and its significance in heat pulse velocity measurement. J. Exp. Bot. 35,
551–561.
Ewers, B.E., Mackay, D.S., Gower, S.T., Ahl, D.E., Burrows, S.N., Samanta, S.S., 2002.
Tree species effects on stand transpiration in northern Wisconsin. Water Resour.
Res. 38, 1–11.
Fernández, M.E., Gyenge, J., Schlichter, T., 2009. Water flux and canopy conductance
of natural versus planted forests in Patagonia, South America. Trees—Struct.
Funct. 23 (2), 415–427.
Fetcher, N., Oberbauer, S.F., Chazdon, R.L., 1994. Physiological ecology of trees,
shrubs, and herbs at La Selva. In: McDade, L.A., Bawa, K.S., Hespenheide, H.A.,
Hartshorn, G.S. (Eds.), La Selva: Ecology and Natural History of a Neotropical
Rainforest. University of Chicago Press, Chicago, IL,USA, pp. 128–141.
Fiora, A., Cescatti, A., 2008. Vertical foliage distribution determines the radial pattern
of sap flux density in Picea abies. Tree Physiol. 28, 1317–1323.
Flora, A., Cescatti, A., 2008. Vertical foliage distribution determines the radial pattern
of sap flux density in Picea abies. Tree Physiol. 28, 1317–1323.
Ford, C.R., Goranson, C.E., Mitchell, R.J., Will, R.E., Teskey, R.O., 2004b. Diurnal and
seasonal variability in the radial distribution of sap flow: predicting total stem
flow in Pinus taeda trees. Tree Physiol. 24, 951–960.
Ford, C.R., McGuire, M.A., Mitchell, R.J., Teskey, R.O., 2004a. Assessing variation in
the radial profile of sap flux density in Pinus species and its effect on daily water
use. Tree Physiol. 24, 241–249.
Ford, C.R., Mitchell, R.J., Teskey, R.O., 2008. Water table depth affects productivity,
water use, and the response to nitrogen addition in a savanna system. Can. J. For.
Res. 38, 2118–2127.
Gazal, R.M., Scott, R.L., Goodrich, D.C., Williams, D.G., 2006. Controls on transpiration in a semiarid riparian cottonwood forest. Agric. For. Meteorol. 137 (1–2),
56–67.
Granier, A., 1985. A new method of sap flow measurement in tree stems. Ann. Sci.
For. 42, 193–200.
Granier, A., Anfodillo, T., Sabatti, M., Cochard, H., Dreyer, E., Tomasi, M., Valentini,
R., Breda, N., 1994. Axial and radial water flow in the trunks of oak trees: a
quantitative and qualitative analysis. Tree Physiol. 14, 1383–1396.
Granier, A., Huc, R., Barigah, S.T., 1996. Transpiration of natural rain forest and itsdependence on climatic factors. Agric. For. Meteorol. 78 (1–2), 19–29.
Granier, A., Huc, R., Colin, F., 1992. Transpiration and stomatal conductance of two
rain forest species growing in plantations (Simarouba amara and Goupia glabra)
in French Guyana. Ann. For. Sci. 49, 17–24.
Gyenge, J.E., Fernandez, M.E., Schlichter, T.M., 2008. Are differences in productivity between native and exotic trees in NW Patagonia related to differences in
hydraulic conductance? Trees—Struct. Funct. 22 (4), 483–490.
Hölscher, D., Koch, O., Korn, S., Leuschner, C., 2005. Sap flux of five co-occurring
tree species in a temperate broad-leaved forest during seasonal soil drought.
Trees—Struct. Funct. 19 (6), 628–637.
Horna, V., Schuldt, B., Brix, S., Leuschner, C., 2011. Environment and tree size controlling stem sap flux in a perhumid tropical forest of Central Sulawesi, Indonesia.
Ann. For. Sci. 68, 1027–1038.
Irvine, J., Law, B.E., Kurpius, M.R., Anthoni, P.M., Moore, D., Schwarz, P.A., 2004. Agerelated changes in ecosystem structure and function and effects on water and
carbon exchange in ponderosa pine. Tree Physiol. 24, 753–763.
Jiménez, M.S., Čermák, J., Kuèera, J., Morales, D., 1996. Laurel forests in Tenerife,
Canary Islands: the annual course of sap flow in Laurus trees and stand. J. Hydrol.
183, 307–321.
Jiménez, M.S., Nadezhdina, N., Čermák, J., Morales, D., 2000. Radial variation in sap
flow in five laurel forest tree species in Tenerife, Canary Islands. Tree Physiol.
20, 1149–1156.
Köcher, P., Gebauer, T., Horna, V., Leuschner, C., 2009. Leaf water status and stem
xylem flux in relation to soil drought in five temperate broad-leaved tree species
with contrasting water use strategies. Ann. For. Sci. 66, 101.
21
Köstner, B., Granier, A., Èermák, J., 1998. Sap flow measurements in forest standsmethods and uncertainties. Ann. Sci. For. 55, 13–27.
Kubota, M., Tenhunen, J., Zimmermann, R., Schmidt, M., Kakubari, Y., 2005. Influence of environmental conditions on radial patterns of sap flux density of a
70-year Fagus crenata trees in the Naeba Mountains, Japan. Ann. For. Sci. 62 (4),
289–296.
Kumagai, T., Aoki, S., Shimizu, T., Otsuki, K., 2007. Sap flow estimates of stand transpiration at two slope positions in a Japanese cedar forest watershed. Tree Physiol.
27, 161–168.
Lagergren, F., Lindroth, A., 2002. Transpiration response to soil moisture in pine and
spruce trees in Sweden. Agric. For. Meteorol. 112, 67–85.
Loranty, M.M., MacKay, D.S., Ewers, B.E., Adelman, J.D., Kruger, E.L., 2008. Environmental drivers of spatial variation in whole-tree transpiration in an
aspen-dominated upland-to-wetland forest gradient. Water Resour. Res. 44,
W02441.
Loustau, D., Domec, J.C., Bosc, A., 1998. Interpreting the variations in xylem sap flux
density within the trunk of maritima pine (Pinus pinaster Ait.): application of
a model for calculating water flows at tree and stand levels. Ann. Sci. For. 55,
29–46.
Mark, W.R., Crews, D.L., 1973. Heat-pulse velocity and bordered pit condition in
living Engelmann spruce and Lodgepole pine trees (Picea engelmannii, Pinus
contorta). For. Sci. 19, 291–296.
Meinzer, F.C., Goldstein, G., Andrade, J.L., 2001. Regulation of water flux through
tropical forest canopy trees: do universal rules apply? Tree Physiol. 21, 19–26.
Meinzer, F.C.A., Goldstein, G., Holbrook, N.M., Jackson, P., Cavelier, J., 1993. Stomatal
and environmental control of transpiration in a lowland tropical forest tree.
Plant Cell Environ. 16, 429–436.
Meiresonne, L., Nadezhdina, N., Čermák, J., Van Slycken, J., Ceulemans, R., 1999.
Transpiration of a monoclonal poplar stand in Flanders (Belgium). Agric. For.
Meteorol. 96, 165–179.
Mitchell, P.J., Veneklaas, E., Lambers, H., Burgess, S.S.O., 2009. Partitioning of evapotranspiration in a semi-arid eucalypt woodland in south-western Australia.
Agric. For. Meteorol. 149, 25–37.
Nadezhdina, N., Čermák, J., Ceulemans, R., 2002. Radial patterns of sap flow in woody
stems of dominant and understory species: scaling errors associated with positioning of sensors. Tree Physiol. 22, 907–918.
O’Brien, J.J., Oberbauer, S.F., Clark, D.B., 2004. Whole tree xylem sap flow responses
to multiple environmental variables in a wet tropical forest. Plant Cell Environ.
27, 551–567.
Oren, R., Pataki, D.E., 2001. Transpiration in response to variation in microclimate and soil moisture in southeastern deciduous forests. Oecologia 127 (4),
549–559.
Oren, R., Phillips, N., Katul, G., Ewers, B.E., Pataki, D.E., 1998. Scaling xylem sap flux
and soil water balance and calculating variance: a method for partitioning water
flux in forests. Ann. Des. Sci. For. 55 (1/2), 191–216.
Oren, R., Zimmermann, R., Terborgh, J., 1996. Transpiration in upper Amazonia floodplain and upland forests in response to drought breaking rains. Ecology 77,
968–973.
Pataki, D.E., Oren, R., Smith, W.K., 2000. Sap flux of co-occurring species in a western
subalpine forest during seasonal soil drought. Ecology 81 (9), 2557–2566.
Pataki, D.E., Oren, R., 2003. Species differences in stomatal control of water loss at
the canopy scale in a mature bottomland deciduous forest. Adv. Water Res. 26
(12), 1267–1278.
Phillips, N., Oren, R., Zimmermann, R., 1996. Radial patterns of xylem sap flow in
non-diffuse and ring-porous tree species. Plant Cell Environ. 19, 983–990.
Phillips, N., Oren, R., Zimmermann, R., Wright, S.J., 1999. Temporal patterns of water
flux in trees and lianas in a Panamanian moist forest. Trees 14, 116–123.
Sperry, J.S., Perry, A.H., Sullivan, J.E.M., 1991. Pit membrane degradation and airembolism formation in aging xylem vessels of Populus tremuloides Michx. J. Exp.
Bot. 42, 1399–1406.
Spicer, R., Gartner, B.L., 2001. The effects of cambial age and position within the stem
on specific conductivity in Douglas-fir (Pseudotsuga menziesii) sapwood. Trees
15, 222–229.
Swanson, R.H., Whitfield, D.W.A., 1981. A numerical analysis of heat pulse velocity
theory and practice. J. Exp. Bot. 32, 221–239.
Vertessy, R.A., Hatton, T.J., Reece, P., O’Sullivan, S.K., Benyon, R.G., 1997. Estimating stand water use of large mountain ash trees and validation of the sap flow
measurement technique. Tree Physiol. 17, 747–756.
Wilson, K.B., Hanson, P.J., Mulholland, P.J., Baldocchi, D.D., Wullschleger, S.D., 2001. A
comparison of methods for determining forest evapotranspiration and its components: sap-flow, soil water budget, eddy covariance and catchment water
balance. Agric. For. Meteorol. 106 (2), 153–168.
Wullschleger, S.D., Hanson, P.J., Todd, D.E., 2001. Transpiration from a multi-species
deciduous forest as estimated by xylem sap flow techniques. Forest Ecol. Manage. 143 (1–3), 205–213.
Wullschleger, S.D., Meinzer, F.C., Vertessy, R.A., 1998. A review of whole-plant water
use studies in trees. Tree Physiol. 18, 499–512.
Wullschleger, S.D., Wilson, K.B., Hanson, P.J., 2000. Environmental control of wholeplant transpiration, canopy conductance and estimates of the decoupling
coefficient for large red maple trees. Agric. For. Meteorol. 104, 157–168.