Tree Physiology 24, 701–706
© 2004 Heron Publishing—Victoria, Canada
Why do trees decline or dieback after a strong wind? Water status of
Hinoki cypress standing after a typhoon
MASAFUMI UEDA1,2 and EI’ICHI SHIBATA3
1
Nara Forest Research Institute, Takatori, Nara 635-0133, Japan
2
Corresponding author ([email protected])
3
Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa-ku, Nagoya 464-8601, Japan
Received March 21, 2003; accepted on October 26, 2003; published online April 1, 2004
Summary We examined the water status of Hinoki cypress,
Chamaecyparis obtusa (Siebold & Zucc.) Endl., trees after a
severe typhoon to determine possible causes of the decline and
dieback that can occur in what appear, at first, to be healthy
trees in typhoon-damaged forest stands. We found that in apparently healthy trees in a storm-damaged stand, the water conducting area of the trunk cross section was greatly reduced
compared with that of similarly sized trees in a nearby undamaged stand. Although leaf specific hydraulic resistance (Wl)
from soil to leaf and from trunk to leaf was higher in trees from
the storm-damaged than the undamaged stand, Wl values from
soil to root were similar. Diurnal patterns in the rates of change
in trunk diameter differed between trees in the damaged and the
undamaged stand. We conclude that increased aboveground
hydraulic resistance caused by a reduction in trunk water conducting area could be a major reason for the decline and
dieback of apparently healthy trees in typhoon-damaged
stands.
Keywords: Chamaecyparis obtusa, diameter change, hydraulic resistance, water stress.
thereby causing water stress that may result in dieback or
decline.
Water in xylem is normally under tension. At pressures below the saturation vapor pressure, liquid water is in a
metastable state, susceptible to transition to the stable vapor
phase. When this occurs to water in xylem vessel elements or
tracheids, it causes cavitation and termination of water flow
(Perämäki et al. 2001). Although it is known that wind sway
affects trunk sap flow (Tyree and Zimmermann 2002), few
studies have examined secondary wind damage to trees from
the viewpoint of trunk water flow.
Diurnal changes in the diameter of tree trunks can be measured with stain-gauges (Ueda et al. 1996). Such changes are
largely caused by changes in tree water status (Kozlowski
1967, Kozlowski et al. 1991). Thus, the diurnal changes in
trunk diameter measured at the xylem surface reflect the water
balance (sap flow minus transpiration) of a tree (Ueda and
Shibata 2001).
In this study, we measured trunk hydraulic resistance and diurnal changes in diameter to: (a) clarify the effects of typhoon
winds on stem water flow; and (b) identify potential causes of
dieback and decline in what are, initially, healthy-looking trees
in a typhoon- damaged stand.
Introduction
Typhoons are a major cause of forest disturbance in tropical,
subtropical and warm temperate regions (Everham and
Brokaw 1996). Tree damage can be classified as either primary or secondary. Primary damage includes trunk and branch
breakage, uprooting (Kozlowski et al. 1991), and mechanical
damage to roots (Muramoto et al. 1998). Secondary damage
consists in the aftereffects of a typhoon, including tree dieback
and decline (Fukuda et al. 1997, Muramoto et al. 1998).
Water stress has been suggested as a cause of secondary
damage (Fukuda et al. 1997, Muramoto et al. 1998). Primary
damage may result in increased penetration of the canopy by
solar radiation, leading to higher temperatures and reduced
humidities. Such changes in stand microclimate may increase
crown transpiration and thereby affect soil water availability
(Fukuda et al. 1997). Damage caused by partial uprooting reduces water flow from soil to trees (Muramoto et al. 1998),
Materials and methods
Plant materials
We studied two 31-year-old stands of Hinoki cypress,
Chamaecyparis obtusa (Siebold & Zucc.) Endl., which were
located about 100 m apart, at Murou Village, Nara Prefecture,
Japan (34°35′ N, 136°0′ E, 580 m above sea level) on a
semi-arid brown forest soil. The stands were approximately
400 m 2 in area and had a density of about 3600 trees ha –1.
Mean tree height and breast height diameter (dbh) were 15.8 ±
1.6 m and 17.4 ± 4.5 cm, respectively, in one stand, which was
subsequently damaged by a typhoon, and 16.3 ± 2.0 m and
17.1 ± 4.0 cm, respectively, in the other stand, which showed
no visible signs of damage as a result of the storm.
On September 22, 1998, a typhoon with peak winds of
37.5 m s –1 hit Murou village. In the damaged stand, many trees
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UEDA AND SHIBATA
were uprooted or suffered stem breakage, reducing tree density to 2700 trees ha –1. In the other stand, the storm caused no
serious visible damage. In October 1998, we thinned trees in
the undamaged stand to the same density as that in the damaged stand. We selected three healthy-looking trees, i.e., without visible signs of storm damage, from each stand for study
(Table 1).
Diurnal change in trunk diameter
Diurnal changes in trunk diameter were measured by the
strain-gauge method (Ueda et al. 1996) (Figure 1) from
April 1, 1999 to July 29, 2000. Strain gauges (length: 16.0 mm,
width: 5.2 mm, KFG-10-120-C1-11, Kyowa Electronic Instruments, Tokyo, Japan) were attached to the xylem surface on
the east side of each tree trunk at 3 m above ground level. The
outer and inner bark and phloem tissues were stripped away
over an area of 20 × 10 mm to expose the xylem surface. Each
strain gauge was fixed horizontally to the xylem surface with
cyanoacrylate adhesive and then covered with Vaseline, silicon resin and aluminum foil to maintain electrical isolation of
the gauge and to shelter it from the sun. The strain (ε) measured by a strain gauge is determined by the ratio of the increase or decrease in the length of the gauge relative to its
original length. This value is independent of atmospheric humidity, but not temperature. However, the drift in ε due to variation in temperature was less than ± 5 × 10 –6 °C –1. Values of ε
were logged every minute with a data logger (TDS303, Tokyo
Sokki Kenkyujo, Tokyo, Japan). Strain change rates (Rε; h –1)
(Ueda and Shibata 2001) were calculated from ε as: Rε = dε/dt.
Sap flux
Before dawn on July 30, 2000, the experimental trees were
felled at ground level and placed in tubs filled with 100 liters of
distilled water (Figure 1). Each tub was placed on three 50-kg
load cells (resolution: 0.015 kg, LTZ50KA, Kyowa Electronic
Instruments) and water absorption, as estimated from the decrease in weight of the tub, determined at 1-min intervals and
recorded with a data logger (TDS303, Tokyo Sokki Kenkyujo)
from July 30 to August 7, 2000. Sap flux (F; kg h –1 kg –1) was
estimated from water absorption per unit leaf dry mass.
(1958) (Figure 1). One set of sensors (a heater probe (2.5 Ω,
1.2 A, diameter (Φ) 2 × 50 mm, Hayashidenko, Tokyo, Japan)
and two thermistor probes (Φ 2 × 50 mm, Hayashidenko) were
installed on the west side of the trunk of each examined tree at
3 m above ground level and inserted 10 mm deep from the xylem surfaces. A heater probe was installed radially into the
stem to release a heat pulse as a tracer (pulse duration: 1.5 s).
The two thermistor probes were located asymmetrically
around the heater probe. The downstream probe spacing (Dd)
and the upstream probe spacing (Du) were 10 and 5 mm, respectively. The probes were installed in a hole (Φ 2 mm)
drilled with a gauge guide in the outer xylem to reach a set
depth. We measured HPV at 20-min intervals with a sap flow
meter (HP-2, Hayashidenko) and corrected for the effect
of sensor implantation wounds (Swanson and Whitfield 1981).
The temperature difference between thermistor probes was
measured every 0.1 s. The time delay (t; s) for the same temperature increase at both thermistor probes was recorded. We
calculated HPV as:
HPV =
Du + Dd
× 10−3 × 3600
2t
Leaf water potentials
Predawn (from 0500 to 0530 h) leaf water potentials (ΨPDleaf;
MPa) and midday (from 1000 to 1400 h) leaf water potentials
(ΨMDleaf; MPa) were measured with a pressure chamber
(Model 1003, PMS, Corvallis, OR) (Scholander et al. 1965)
before and after falling the trees (July 21 to 29 and July 30 to
August 7, 2000, respectively). Measurements were made on
current-season leaves at 10 m above ground level at 10- or
30-min intervals.
Microclimatology
Soil water matric potentials around each tree were monitored
at 60-min intervals with tensiometers at depths of 20 and
60 cm (six replicate sensors). The water-vapor saturation deficits of the air were calculated from dry- and wet-bulb temperature measurements 12 m above ground.
Water conducting area in trunk cross sections
Heat pulse velocities
Heat pulse velocities (HPV; m h –1) were measured before and
after felling the trees (April 1, 1999 to July 29, 2000 and July
30 to August 7, 2000, respectively) as described by Marshall
After completing the sap flux measurements, trees were
placed in tubs filled with 60 l of dye solution (1% aqueous
acid-fuchsin) for 7 days (August 8–14, 2000) to determine the
water conducting area of the trunk. On August 15, all leaves
Table 1. Characteristics of the studied Hinoki cypress trees. Abbreviation: DBH = diameter at breast height.
Tree number (undamaged stand)
Height (m)
DBH (cm)
Crown length (m)
Total leaf mass (kg)
Tree number (damaged stand)
U-1
U-2
U-3
D-1
D-2
D-3
13.04
13.3
3.60
4.85
15.30
17.8
6.00
12.57
13.43
15.5
4.20
8.57
13.42
14.5
3.50
4.85
13.40
16.7
3.90
9.37
14.09
16.8
4.00
10.49
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WHY DO TREES DECLINE AFTER A TYPHOON?
703
by calibrating HPV against F measured after tree felling. We
calculated resistance differences as Wl before cutting – Wl after cutting.
Results
The ascent of dye in trunk cross sections
Figure 1. Diagram showing experimental device and procedure. Stem
diameter changes, heat pulse velocity and predawn and midday leaf
water potential were measured before tree felling and then remeasured (except stem diameter changes) as distilled water was absorbed
by the cut tree trunk. Felled trees were hung by wires from towers
constructed around them. The arrow at LWP indicates where leaves
were sampled for leaf water potential measurements.
were plucked from the trees and total leaf dry mass (105 °C for
72 h) determined. To determine the dye ascent area in the
trunk, the trunk was cut into 10-cm-thick disks and the cross
sections photocopied. Dyed and undyed areas were measured
by tracing with a planimeter.
Calculations
Leaf-specific hydraulic resistances before tree felling (Wl before
–1
h kg) and after tree felling (Wl after cutting; MPa
cutting; MPa kg
–1
kg h kg) were calculated as: Wl = (ΨMDleaf – ΨPDleaf)/FMD,
where FMD (kg h –1 kg –1) is sap flux (F) at midday (from 1000
to 1400 h). To calculate Wl before cutting and Wl after cutting, we used
the data (ΨPDleaf, ΨMDleaf and FMD) measured before and after
tree felling, respectively. We calculated FMD before tree felling
In trees from the undamaged stand, sapwood was dyed evenly,
whereas the heartwood and intermediate areas were undyed
(Figure 2a). In trees from the damaged stand, the dye ascended
the sapwood unevenly, creating a mosaic of stained and unstained areas in the trunk cross sections. The total area stained
was much less in sections of trees from the damaged stand than
in trees from the undamaged stand (Figure 2b). In damaged
trees, new annual rings, added after the typhoon, were also
only partly dyed. The undyed parts in new annual rings were
discolored by formation of compression wood (Figure 2b arrow).
Vertical distribution of dyed area
In trunk cross sections of trees from the undamaged stand, the
dyed area relative to the total stem cross-sectional area was
smallest at the stem base and increased progressively with increasing stem height (Figure 3). The dyed area, especially at
the stem base relative to total stem cross-sectional area, was
substantially lower in trees from the damaged stand than in
trees from the undamaged stand.
Leaf water potential, sap flux and hydraulic resistance
Before tree felling, midday leaf water potentials were lower in
trees from the damaged stand than in trees from the undamaged stand (P < 0.001; t-test) (Figure 4). Sap flux (F) was significantly lower in trees from the damaged stand than in trees
from the undamaged stand, especially during the day (P <
0.001; t-test) (Figure 5). Values of Wl before cutting and Wl after cutting
were significantly lower in trees from the undamaged stand
than in trees from the damaged stand (P < 0.001; t-test); however, values of Wl before cutting – Wl after cutting were similar in trees
from the damaged stand and in trees from the undamaged
stand (P > 0.05 by t-test) (Figure 6).
Figure 2. Dyed areas in the trunk
cross section of a tree from the
undamaged (a) and damaged (b)
Hinoki cypress stands taken at
about 3 m above ground level.
Arrow shows the compression
wood formed after the typhoon.
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704
UEDA AND SHIBATA
Figure 5. Mean sap flux (F) before felling of apparently healthy trees
from the undamaged (䊉) and damaged (䊊) Hinoki cypress stands.
Values are means for three clear days between July 21 and 29. Error
bars = SD.
Figure 3. Vertical distributions of dyed trunk cross-sectional area as a
percent of total cross-sectional area in trees from the undamaged
(left-hand panels) and damaged (right-hand panels) Hinoki cypress
stands.
Microclimatology and changes in trunk diameter
the Rε of September 1999 is used as an example). The weather
in September in Japan is relatively stable, with little cloud and
little rainfall. Diurnal changes in Rε of trees from the undamaged stand showed similar patterns to those reported previously (Ueda et al. 1996, Ueda and Shibata 2001). Values were
negative in the morning and positive in the afternoon. They decreased at dawn, reached a minimum and then increased rapidly to a peak in late afternoon. Thereafter, they decreased
rapidly at first and then gradually during the night. In contrast,
diurnal changes in Rε of trees from the damaged stand fluctuated between negative and positive after dropping to a minimum in the morning, even under moderate weather conditions.
Soil water conditions and water vapor saturation deficits were
similar in the damaged and undamaged stands (Figure 7; only
Figure 4. Mean leaf water potentials before felling of apparently
healthy trees from the undamaged (䊉) and damaged (䊊) Hinoki cypress stands. Values are means for 3 clear days between July 21 and
29. Error bars = SD.
Figure 6. Leaf specific hydraulic resistance (Wl ) in Hinoki cypress.
Symbols: 䊉 = leaf-specific hydraulic resistances before tree felling
(Wl before cutting); 䊊 = leaf-specific hydraulic resistances after tree felling (Wl after cutting); and 䊏 = resistance differences between Wl before cutting and Wl after cutting (Wl before cutting – Wl after cutting ). Error bars = SD.
TREE PHYSIOLOGY VOLUME 24, 2004
WHY DO TREES DECLINE AFTER A TYPHOON?
705
Figure 7. Diurnal patterns in the rate of change in stem diameter (R ε ), water vapor saturation deficit (D) and soil water potentials (Ψs ) at 20 cm
(solid lines) and 60 cm (broken lines) in apparently healthy trees from the undamaged (left-hand side) and damaged (right-hand side) Hinoki
cypress stands. Error bars = SD.
Discussion
When a typhoon strikes, tree trunks are shaken violently. Water flow in trees has been explained by the cohesion theory, according to which water in xylem is under negative pressure
(Tyree and Zimmermann 2002). At pressures below the saturation vapor pressure, liquid water is in a metastable state and is
vulnerable to transition to the stable vapor phase; a transition
that causes cavitations in xylem vessel elements and tracheids
(Perämäki et al. 2001). In our study of trees from a typhoon-damaged stand, dye ascended the sapwood unevenly,
forming a mosaic of stained and unstained areas: the the total
area of stained wood being much less than that seen in cross
sections of trees from an undamaged stand (Figures 2 and 3).
In addition, compression wood, which was unstained, was apparent in sections of trees from the damaged stand, but not
from the undamaged stand (Figure 2b arrow). We speculate
that the shaking of the trunk by the typhoon caused xylem cavitation and termination of water flow, and promoted compression wood formation, and thereby greatly reduced the hydroactive xylem area.
Values of Wl before cutting and Wl after cutting provide measures of
the hydraulic resistance from soil to leaf and from stem to leaf,
respectively, and Wl before cutting – Wl after cutting is a measure of the
hydraulic resistance from soil to root. The hydraulic resistances from soil to leaf (Wl before cutting ) and from trunk to leaf
(Wl after cutting ) were significantly higher in trees from the damaged stand than in trees from the undamaged stand, whereas
the hydraulic resistance from soil to root (Wl before cutting – Wl after
cutting ) was similar in trees from the undamaged and the damaged stands (Figure 6). This suggests that severe trunk shaking
caused by the typhoon resulted in a marked reduction in trunk
water transport area and increased aboveground hydraulic resistance; however, underground hydraulic resistance was unaffected. Fredericksen et al. (1994) reported that artificial trunk
bending decreases the functional xylem conducting area without compromising trunk hydraulic conductivity. The discrepancy between these studies may be explained on the basis of
the extent of disturbance of the functional xylem conducting
area. Severe trunk shaking in every direction by a strong windstorm not only reduced the functional xylem conducting area
(Figures 2 and 3), but greatly disturbed the arrangement of the
water conduit in the trunk cross section (Figure 2).
Diurnal changes in ε reflect diurnal changes in trunk diameter (Ueda et al. 1996). The diurnal pattern of Rε calculated from
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706
UEDA AND SHIBATA
ε measured at the xylem surfaces provides an indication of the
the diurnal change in water balance, i.e., sap flow velocity minus transpiration rate (Ueda and Shibata 2001). Diurnal
changes in Rε of trees from the undamaged stand showed similar patterns to those reported previously (Ueda et al. 1996,
Ueda and Shibata 2001). In trees from the damaged stand,
however, Rε fluctuated between negative and positive after
dropping to minima in the morning even under mild weather
conditions (Figure 7), indicating that suppression of transpiration caused by transient water stress occurred soon after the
daily onset of transpiration (Ueda and Shibata 2002). Furthermore, both sap flux and midday leaf water potentials were
lower in trees from the damaged stand than in trees from the
undamaged stand (Figures 4 and 5). Thus, trees from the damaged stand barely maintained hydraulic sufficiency and were
susceptible to water stress, because of increased aboveground
hydraulic resistance caused by a reduction in water conducting
area as a result of trunk shaking.
Decline and dieback of healthy-looking trees several years
after a typhoon has been attributed to increased water stress
caused by damaged root systems and changes in stand microclimate (Fukuda et al. 1997, Muramoto et al. 1998). However,
we found little evidence of increased hydraulic resistance from
soil to root in the damaged stand (Figure 6). Moreover, stand
microclimates in our damaged and undamaged stands were
very similar (Figure 7). We conclude that tree decline and
dieback after a large typhoon is associated with increased
aboveground hydraulic resistance caused by a large reduction
in trunk water conducting area.
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