Tree Physiology 23, 1021–1030
© 2003 Heron Publishing—Victoria, Canada
Variation in drought response of sal (Shorea robusta) seedlings
SATISH C. GARKOTI,1,4 DONALD B. ZOBEL2,3 and SURENDRA P. SINGH1
1
Department of Botany, Kumaun University, Naini Tal 263 002, India
2
Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA
3
Author to whom correspondence should be addressed ([email protected])
4
Department of Ecology, Assam University, Silchar 788 011, Assam, India
Received August 23, 2002; accepted April 18, 2003; published online September 15, 2003
Summary Plant development and distribution in areas with
seasonal rainfall are often related to the ability of plants to postpone desiccation or tolerate low water potentials during
drought. Regeneration of Shorea robusta Gaertn. (sal), a commercially valuable, widely distributed tree of the Indian tropical belt, is unsuccessful at the base of the Himalaya. Seedling
shoots die back repeatedly during the long drought that follows
the monsoon rain. During the course of one year, we monitored
changes in plant and soil water potentials (Ψ), leaf conductance
(gw), osmotic and elastic adjustment, and xylem conductance
of sal seedlings of different sizes from three landforms: an alluvial plain at 540 m elevation, a slope at 510 m, and a montane
site at 1370 m. Predawn plant Ψ and gw were lowest in the
smallest seedlings (< 20 cm tall). Across sites and seasons,
seedlings > 100 cm tall had higher morning gw than seedlings in
the other size classes. In all size classes, plant Ψ was lowest
during early summer, when leafing begins. Among sites, Ψ and
gw were lowest in seedlings at the montane site. Osmotic potential was lowest during leaf development and highest during the
rainy season, and tissue elasticity was highest during winter. As
leaf area increased during leaf development, xylem conductance per unit of xylem cross-sectional area also increased. We
conclude that low Ψ is unlikely to be a major cause of seedling
mortality. Small seedlings, with low Ψ, had low leaf conductance. Adjustments of osmotic and elastic properties appear to
aid responses of seedlings to drought.
Keywords: forest regeneration, Himalaya, India, leaf conductance, osmotic potential, seedling size, tissue elasticity, water
potential, xylem conductance.
Introduction
Drought limits vegetation development, species distribution,
and plant growth (Kramer and Boyer 1995, Loewenstein and
Pallardy 1998), especially in temperate and tropical climates
where water deficits are severe during the growing season
(Spurr and Barnes 1980). Water potential (Ψ) is used to assess
the availability of water (Kramer and Boyer 1995). Deep rooting in mature trees enables them to maintain an adequate water
supply and thus tolerate seasonal drought (Teskey and Hinck-
ley 1981). In contrast, seedlings with shallow roots and a low
water storage capacity develop lower Ψ during drought.
Plants may adapt to drought by growing in the wet season
and thus avoiding water deficits, by postponing dehydration,
or by tolerating desiccation (Turner 1986b). A combination of
mechanisms is common (Hinckley et al. 1983). Water loss can
be reduced by stomatal closure (Kramer and Boyer 1995), and
plants maintain turgor by lowering osmotic potential or increasing tissue elasticity (Tyree et al. 1978, Hinckley et al.
1983, Doi et al. 1986, Kramer and Boyer 1995). The capacity
for osmotic adjustment during drought is a valuable adaptive
feature of seedlings (Lemcoff et al. 1994).
Shorea robusta Gaertn. (Dipterocarpaceae) (sal), a large,
commercially important tree, grows widely along the base of
the Himalaya and in Himalayan valleys and foothills up to an
elevation of 1500 m (Singh and Singh 1992). At higher elevations, it mixes with chir (Pinus roxburghii Sarg.). In the Himalaya, sal encounters a marked dry season from October to June.
Under such conditions, adaptation to drought is important for
seedling establishment and ecological success of the species.
Regeneration of sal at the base of the Himalaya is often unsuccessful, and has long been a major concern for forest managers in the region (Troup 1921, Rao and Singh 1985). Regeneration failure may be caused by a variety of factors, including
drought (Troup 1921). When the shoots of the seedlings die
but the root remains alive, a new shoot often develops the next
growing season. Several generations of shoots may contribute
to the eventual establishment of a root system that supports a
surviving shoot (Rao and Singh 1985).
We monitored seasonal variations in soil and plant water
potentials, leaf conductance, osmotic potential, tissue elasticity and xylem conductance in sal seedlings of different sizes,
growing in a range of habitats. We analyzed the data to determine how sal copes with seasonal drought during seedling
establishment, and to assess to what extent drought causes
regeneration failure.
Materials and methods
Study area and species
The study area lies in the state of Uttaranchal in northern India,
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GARKOTI, ZOBEL AND SINGH
at 29°18′ to 29°24′ N and 79°20′ to 79°24′ E. Sal seedlings
were sampled in three typical habitats (Singh and Singh 1989):
a fine-textured alluvial plain at 540 m elevation, a lower slope
on coarse sediments at the base of the mountains (locally
known as bhabar) at 510 m, and a rocky upper slope near the
upper limit of the species’ range at 1370 m elevation. At each
site, one permanent plot of about 1 ha, including seedlings of
different sizes, was selected for sampling. Because light availability in the understory may limit seedling growth and survival (Fetcher et al. 1994, Chazdon et al. 1996, Zipperlen and
Press 1997), as well as availability of water (Singh and Singh
1989), we used sample areas between major tree crowns that
supported healthy seedling populations. Small seedlings
crowded by larger ones were not sampled.
Annual rainfall in the region varies from 1050 to 2690 mm
(Dhar et al. 1987), but changes irregularly with elevation
(Singh et al. 1994). Most rain falls during June–September.
Climate data from the nearest weather stations for the study
year are presented in Figure 1. During 1996, there was no rain
during late autumn.
Sal produces leaves late in the dry season, about the time
that the previous-year leaves abscise. Trees are rarely completely leafless and then only for a short time (Troup 1921). A
1-year study at 600 m in the study region (Negi and Singh
1992) showed that mature trees had a mean leaf life span of
385 days, with leaf expansion from mid-March to early May
and a continuing increase in leaf mass until the end of July.
Leaf mass then remained stable at about 2 g leaf –1 until early
December, after which a 20% loss of mass occurred before
abscission.
Measurements
Water relations attributes were sampled during six seasons
representing different conditions relative to water supply and
probable water use by seedlings: spring, before leafing started
(March 3–4); early summer, when warm weather supported
production of new leaves (April 28–29); summer, which is hot
and dry (June 20–21); the rainy season, which is hot and wet,
with high soil water content (July 13–14); fall, after monsoon
rains, with clear, dry and cooling weather (October 22–23);
and winter, cool after the dry fall months (December 3 and 21).
Water relations attributes of seedlings on the alluvial and
lower-slope sites were measured on the same day, whereas attributes of seedlings on the upper-slope site were measured on
a different day.
Temperature and humidity varied substantially among seasons and elevations (Table 1). Plant and soil water potentials
(Ψplant and Ψsoil, respectively) were measured in all seasons.
Leaf conductance (gw) was measured in all seasons except the
rainy season, and osmotic and elastic properties were deter-
Table 1. Environmental conditions during sampling periods. The
mean elevation at the alluvial and lower-slope sites was 525 m; the elevation at the upper-slope site was 1370 m. Temperature and relative
humidity (RH) were measured during morning (AM) and afternoon
(PM) leaf conductance measurements. Light is the midday mean
(µmol m –2 s –1) for the three least-shaded seedlings; na = not measured.
Season and
elevation
Figure 1. Mean monthly rainfall (bars) and maximum (䊉) and minimum (䊊) air temperatures at the nearest representative weather stations. (A) Pantnagar at 300 m elevation and 34 km SSE of Sites 1
and 2. (B) Ranikhet at 1680 m elevation and 52 km NNE of Site 3.
Temperature (°C)
RH (%)
AM
PM
AM
PM
Spring
525 m
1370 m
18.9
16.5
30.6
27.0
35
35
20
35
987
602
Early summer
525 m
1370 m
32.5
26.7
39.0
36.7
39
30
21
30
750
1593
Summer
525 m
1370 m
31.8
22.6
37.5
35.0
63
75
49
45
900
345
Rainy
525 m
1370 m
24.5
21.0
31.5
25.0
92
87
77
74
Fall
525 m
1370 m
20.0
15.5
28.2
27.5
45
40
47
40
388
88
Winter
525 m
1370 m
12.4
9.1
23.3
22.2
50
60
52
60
264
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TREE PHYSIOLOGY VOLUME 23, 2003
Light
na
na
SHOREA SEEDLING WATER RELATIONS
mined in early summer, the rainy season, fall and winter. Twig
xylem conductance was measured in early summer and during
the rainy season. Seedlings of four height classes were studied:
0–20, 20–50, 50–100 and > 100 cm. Seedling height is generally correlated with age (Rao and Singh 1985), but individual
seedling shoots may die back and regenerate, so it was not possible to determine the age of individuals at the time of measurement.
We measured Ψplant of stems with leaves with a pressure
chamber (Model 1000, PMS Instruments, Corvallis, OR).
Plant Ψ was measured before dawn (Ψplant,predawn ), when Ψplant
should be maximal and in equilibrium with Ψsoil (Kramer and
Boyer 1995), and during midday (Ψplant,midday), when Ψplant
should be minimal. Three to five measurements were made for
each size class at each site during each sampling period. Leaf
conductance was measured on the bottom (abaxial) surface of
leaves with a diffusion porometer (Model AP4, Delta-T Instruments, Cambridge, U.K.) after sunrise (morning) and after
noon (midday). In addition, Ψplant and gw were measured periodically for 1 day in early summer from early morning until
1500 h. We measured Ψsoil once on each sampling date. Soil
samples were collected from 10- and 60-cm depths at three
representative locations per site. Samples were immediately
placed in the sample holder of a thermocouple psychrometer
(Model SC-10A, Decagon Devices, Pullman, WA, with an
NT3 microvoltmeter), along with calibration solutions of
0.1 and 0.9 M KCl. Soil water potential was measured after a
30-min equilibration. Readings were confirmed by a second
measurement 10 min later.
To construct pressure–volume (P–V) curves, foliated shoots
of each seedling size class were collected in polyethylene
bags, stored in an insulated plastic container, and brought
quickly to the laboratory. The shoots were recut under water,
covered with polyethylene, and left overnight to resaturate.
The next morning, the shoots were allowed to dehydrate between sequential measurements of shoot mass and Ψplant. From
the P–V curves, the osmotic potential at full turgor (Ψπf), osmotic potential at zero turgor (Ψπz) and relative water content
at zero turgor (RWC z ) were defined by subjectively determining the extent of the linear portion of the curve, and following
the procedures of Pallardy et al. (1991). Bulk modulus of elasticy (ε) (Turner 1986b) was calculated as the slope of a linear
1023
regression of all non-zero values of pressure potential over relative water content.
Xylem conductance was measured on seedlings of all sizes
collected from each site during early summer and the rainy
season. Xylem conductance was estimated by gravity flow of a
dilute oxalic acid solution based on methods described by
Sperry et al. (1988), Ewers et al. (1989), and Cochard and
Tyree (1990). The mass of fluid leaving the twig was measured
each minute until a stable rate was reached. Staining of twigs
with safranin provided an estimate of the proportion of xylem
area that was active. The length and width of each leaf were
measured. The product of length × width was converted to leaf
area based on an equation derived from measurements of leaf
area, taken with a leaf area meter, of 38 leaves collected from
all sites and seedling size classes. Results of twig xylem conductance measurements were expressed as: the ratio of total
xylem cross-sectional area to leaf area (Huber value); the conductance of fluid per unit of active xylem cross-sectional area
(specific conductance); and the conductance of fluid per unit
of leaf area supplied by the twig (leaf-specific conductance).
Results
Soil water potential
Soil water potential did not differ significantly among sites,
but it differed significantly among seasons (Table 2). Although
Ψsoil at 10-cm depth was always lower than at 60-cm depth (Table 2), Ψsoil at the two depths was strongly correlated (r 2 =
0.957, P < 0.0001). At both depths, Ψsoil was lowest in winter,
varying across sites from –3.2 to –3.9 MPa at 10-cm depth and
–2.6 to –3.6 MPa at 60-cm depth (Table 2). In general, Ψsoil decreased from spring until summer, increased during the rainy
season, and then decreased steeply until winter (Table 2). During winter, Ψsoil was most negative at the lower-slope site.
Plant water potential
Predawn plant water potential varied significantly among size
classes, sites and seasons (Table 3). Across seasons and sites,
small (0–20 cm tall) seedlings had the lowest Ψplant,predawn (Table 3). Among seedlings of different size classes at all sites,
Ψplant,predawn varied little from spring to summer, increased during the rainy season, and then decreased in fall and winter (Ta-
Table 2. Soil water potential (MPa) at 10- and 60-cm soil depths at three sites in central Himalayan Shorea robusta forests.1
Site
Depth (cm)
Season
Spring
Early summer
Summer
Rainy
Fall
Winter
Alluvial
10
60
–1.5
–1.2
–2.7
–1.8
–0.9
–0.7
> –0.2
> –0.2
–2.6
–2.5
–3.2
–2.6
Lower slope
10
60
–1.4
–1.2
–0.7
–0.4
–2.1
–1.9
> –0.2
> –0.2
–2.7
–2.4
–3.9
–3.6
Upper slope
10
60
–1.4
–1.0
–2.1
–1.6
–2.1
–1.6
> –0.2
> –0.2
–2.6
–2.5
–3.4
–2.8
1
Analysis of variance for 10- and 60-cm depths: site, nonsignificant; season, P < 0.0001.
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GARKOTI, ZOBEL AND SINGH
Table 3. Variation in predawn plant water potential (MPa) in sal seedlings among sites, seasons and size classes in the central Himalaya.1
Site
Size class (cm)
Season
Spring
Early summer
Summer
Rainy
Fall
Winter
Alluvial
0–20
20–50
50–100
> 100
–0.7
–0.8
–0.6
–0.4
–0.4
–0.5
–0.7
–1.0
–0.6
–0.8
–1.0
–1.3
–0.5
–0.3
–0.5
–0.3
–1.0
–1.0
–1.0
–0.4
–0.4
–0.5
–0.6
–0.4
Lower-slope
0–20
20–50
50–100
> 100
–0.7
–0.7
–0.5
–0.3
–0.9
–0.6
–1.0
–0.8
–0.7
–0.8
–0.7
–0.7
–0.2
–0.4
–0.2
–0.1
–0.8
–0.6
–0.4
–0.4
–0.9
–0.6
–0.7
–0.4
Upper-slope
0–20
20–50
50–100
> 100
–1.0
–1.1
–1.3
–1.2
–2.8
–0.9
–1.2
–0.9
–0.7
–0.5
–0.5
–0.6
–0.4
–0.1
–0.2
–0.2
–1.4
–0.9
–0.8
–1.6
–1.6
–1.3
–1.1
–0.9
Mean
All
–0.78
–0.98
–0.74
–0.28
–0.86
–0.78
1
Analysis of variance: site, P < 0.0001; season, P < 0.0001; size class, P = 0.001.
ble 3). At the upper-slope site, Ψplant,predawn of most seedlings
measured in spring, early summer, fall and winter was below
–1.0 MPa (Table 3). However, at the alluvial and lower-slope
sites, Ψplant,predawn rarely dropped below –1.0 MPa.
Midday plant water potential varied significantly with seedling size and season, but not among sites (Table 4). Midday
plant water potential decreased from spring to early summer,
increased during summer and the rainy season, and then decreased in fall and winter (Table 4). Small seedlings (0–20 cm)
had the lowest Ψplant,midday. Among larger seedlings, Ψplant,midday
exhibited no definite pattern among seasons and sites (Table 4).
Leaf conductance
Variation in gw was significant among sites, seasons and, dur-
ing morning, size classes (Tables 5 and 6). Multiple range
analysis indicated that gw differed significantly among sites: it
was highest at the lower-slope site, intermediate at the alluvial
site, and lowest at the upper-slope site (Tables 5 and 6). Considering all sites and seasons together, seedlings > 100 cm tall
had higher morning gw than seedlings in the two smallest size
classes. During midday, seedlings 50–100 cm tall had higher
gw than the smallest seedlings. Leaf conductance was significantly higher in fall and winter than in the other seasons (Tables 5 and 6).
Small seedlings had higher morning gw in winter than in
other seasons (Table 5). During spring and early summer, near
the end of the dry season and when leafing occurred, minimum
and maximum midday gw was exhibited by the smallest and
largest seedlings, respectively. Although gw declined in all
Table 4. Seasonal variation in midday plant water potential (MPa) in sal seedlings at three sites in the central Himalaya.1
Site
Size class (cm)
Season
Spring
Early summer
Summer
Rainy
Fall
Winter
Alluvial
0–20
20–50
50–100
> 100
–1.3
–1.2
–1.7
–0.6
–2.8
–1.7
–1.3
–1.8
–1.1
–1.5
–1.8
–1.5
–1.2
–0.9
–1.4
–1.1
–1.4
–1.0
–1.2
–1.2
–0.8
–0.9
–1.2
–0.8
Lower-slope
0–20
20–50
50–100
> 100
–1.6
–1.0
–0.8
–1.1
–2.7
–2.2
–2.1
–1.8
–1.6
–1.5
–1.1
–1.1
–1.3
–1.5
–1.0
–0.6
–1.2
–1.6
–0.9
–1.3
–1.7
–1.5
–1.2
–0.9
Upper-slope
0–20
20–50
50–100
> 100
–1.8
–1.1
–1.5
–1.5
–1.9
–1.8
–1.3
–0.7
–1.1
–1.4
–1.3
–1.2
–0.7
–0.4
–0.3
–0.4
–1.8
–1.5
–1.5
–1.8
–1.8
–1.5
–1.6
–1.4
Mean
All
–1.27
–1.84
–1.35
–0.90
–1.37
–1.28
1
Analysis of variance: site, nonsignificant; season, P < 0.0001; size class, P < 0.0001.
TREE PHYSIOLOGY VOLUME 23, 2003
SHOREA SEEDLING WATER RELATIONS
1025
Table 5. Seasonal patterns of morning leaf conductance (mmol m –2 s –1) in sal seedlings of four size classes at three sites in the central Himalaya.1
Site
Size class (cm)
Season
Spring
Early summer
Summer
Fall
Winter
Alluvial
0–20
20–50
50–100
> 100
89
305
355
460
60
31
54
72
65
119
169
188
475
1382
1150
628
918
713
945
1089
Lower-slope
0–20
20–50
50–100
> 100
44
139
409
293
120
570
418
356
56
24
58
19
460
341
376
659
320
321
352
611
Upper-slope
0–20
20–50
50–100
> 100
32
260
133
341
44
132
54
136
53
107
67
97
39
125
65
152
213
96
109
174
Mean
All
238
171
85
488
488
1
Analysis of variance: site, P < 0.0001; season, P < 0.0001; size class, P = 0.005.
sizes during drought, it was significantly lower in the smallest
seedlings.
the lower-slope site, it was correlated with overall Ψ at the alluvial (r 2 = 0.37, P = 0.005) and upper-slope (r 2 = 0.26, P =
0.021) sites.
Diurnal patterns
There was a clear diurnal pattern in Ψplant, with minimal Ψplant
at 1300 h for all size classes (Figure 2A). Seedlings 0–20 cm
tall exhibited lower Ψplant (–1.3 to –2.4 MPa) throughout the
day than larger seedlings (–0.7 to –1.8 MPa). Seedlings at different sites and in other size classes did not differ significantly
from one another.
There was no clear diurnal pattern in gw (Figure 2B). Small
seedlings had significantly lower gw than larger seedlings. Although gw increased in early morning in all seedling size
classes, gw varied among seedling size classes during the rest
of the day. Although gw was not correlated with overall Ψ at
Osmotic potential, tissue elasticity and relative water content
Osmotic potential at full turgor, Ψπz, ∆Ψ (Ψπf – Ψπz), ε and
RWC z varied among seasons, but not among sites or seedling
size classes (Table 7). Osmotic potentials were lowest in early
summer and highest during the rainy season. Tissue was most
elastic (i.e., had the lowest ε) in winter and least elastic during
the rainy season. The RWCz was higher during the rainy season than during other seasons.
Xylem conductance
Huber value and specific conductance of xylem differed sig-
Table 6. Midday leaf conductance (mmol m –2 s –1) patterns in sal seedlings of four size classes at three sites in the central Himalaya.1
Site
Size class (cm)
Season
Spring
Early summer
Summer
Fall
Winter
Alluvial
0–20
20–50
50–100
> 100
38
129
247
516
12
45
63
24
62
103
74
125
1119
1488
1374
978
218
1125
1108
898
Lower-slope
0–20
20–50
50–100
> 100
62
331
395
424
60
31
187
497
99
82
242
78
1194
984
1574
1501
206
264
399
350
Upper-slope
0–20
20–50
50–100
> 100
27
94
139
220
12
63
68
92
179
133
232
81
736
319
390
253
130
152
169
120
Mean
All
219
96
124
993
428
1
Analysis of variance: site, P < 0.0001; season, P < 0.0001; size class, P = 0.066.
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GARKOTI, ZOBEL AND SINGH
Figure 2. Daily courses of (A) plant
water potential (MPa) and (B) leaf conductance (mmol m –2 s –1) for different
seedling size classes. Values are means
for all sites. Bars represent ± 1 standard error. Measurements were made
during early summer. Size classes: 䉭 =
< 20 cm tall; 䉱 = 20–50 cm; 䊐 =
50–100 cm; and 䊏 = > 100 cm.
nificantly among seasons, but not among sites or size classes
(Table 8). Seedlings had higher specific conductances and
higher leaf-specific conductances in the rainy season than in
early summer (Table 8). Percent active xylem and leaf-specific
conductance did not differ among seedling size classes, sites
or seasons.
Correlations among water relations attributes
Values of Ψsoil at 10- and 60-cm depths were strongly correlated with each other and weakly correlated with Ψplant,predawn
(Table 9), but uncorrelated with Ψplant,midday. Soil Ψ was also related to gw measured in the afternoon (midday gw) but not to gw
measured in the morning, as well as to ε, RWC z (but not osmotic potential), Huber value and specific conductance of xylem. Leaf conductance, ε, and the ratio of xylem to leaf area
declined when Ψsoil was high; other water relations attributes
increased with increasing Ψsoil.
Predawn Ψplant was weakly related to Ψplant,midday (Table 10).
Both morning and midday gw were related to Ψplant,midday but
not to Ψplant,predawn. The results of the pressure–volume analysis
and the specific conductance of xylem sometimes varied with
Ψplant. Leaf conductance, osmotic potential, RWC z and xylem
conductance all increased with increasing Ψplant (Table 10).
Values of morning and midday gw were significantly related
to each other, as were osmotic potential at full and zero turgor,
and ε and RWCz (Table 10). Leaf conductance was high when
osmotic potential was high. Osmotic potential was only moderately related to RWC and was not related to ε. Xylem properties did not co-vary with either gw or osmotic properties, but
leaf-specific conductance increased with both Huber value
(more xylem per unit leaf area) (r = 0.60) and specific conductance (conductance per unit active xylem) (r = 0.64).
TREE PHYSIOLOGY VOLUME 23, 2003
SHOREA SEEDLING WATER RELATIONS
Table 7. Seasonal mean values of osmotic potential (MPa), bulk
modulus of elasticity (ε; MPa) and relative water content at zero
turgor (RWC z ; %).1 Abbreviations: Ψπf = osmotic potential at full
turgor; Ψπz = osmotic potential at zero turgor; and ∆Ψπ = (Ψπf – Ψπz).
Within a column, values followed by the same letter are not significantly different (P = 0.05).
Season
Ψπf
Ψπz
∆Ψπ
ε
RWCz
Early summer
Rainy
Fall
Winter
–2.1 c
–1.4 a
–1.8 b
–1.8 b
–2.6 c
–1.7 a
–2.1 b
–2.3 b
0.49 b
0.35 a
0.30 a
0.52 b
6.6 bc
6.8 c
5.3 ab
4.8 a
68.8 a
82.6 b
70.0 a
67.1 a
1
Analysis of variance: site, all values nonsignificant (ns); season,
Ψπf P < 0.0001, Ψπz P < 0.0001, ∆Ψπ P = 0.002, ε P = 0.023, RWC z
P < 0.0001; size class, all values ns.
Discussion
Severity of drought
Sal seedlings, primarily those < 20 cm tall, had Ψplant values
low enough to interfere with their growth and metabolism.
During the study period, Ψplant was lowest in early summer, the
time of initiation of new leaves. This season also induced the
lowest Ψplant and gw in larger trees during a 2-year study near
the alluvial site (Tewari 1999). Seedlings at the 1370 m upperslope site had significantly lower Ψplant than populations at
lower elevations.
Values of Ψplant below –1.0 MPa may adversely affect several aspects of plant performance (Kozlowski et al. 1991,
Larcher 1995). Seedlings sometimes reached Ψplant,predawn values below –1 MPa, especially at the upper-slope site. In contrast, Ψplant,predawn values of mature individuals from nearby
forests were –0.25 to –0.57 MPa (Zobel et al. 2001). The
maintenance of Ψplant,predawn values greater than –1 MPa in
seedlings at the alluvial and lower slope sites during most of
the year (even during dry months) may be related to the deep
root systems developed by seedlings, approaching 1 m in the
first year in favorable circumstances (Troup 1921). Plant Ψ
was often higher than Ψsoil, probably because the seedlings
were rooted deeper than the 60-cm soil sampling depth; a similar discrepancy between Ψplant and Ψsoil is common for trees in
Table 8. Seasonal variation in characteristics related to xylem conductance.1 Units are: specific conductance, kg m –1 s –1 MPa –1; Huber
value × 10 –4, dimensionless; leaf-specific conductance × 10 – 4, kg
m –1 s –1 MPa –1. Within a column, values followed by the same letter
are not significantly different (P = 0.05).
Season
% Active
xylem
Specific
conductance
Huber
value
Leaf-specific
conductance
Early summer
Rainy
83.9 a
87.1 a
0.556 b
1.539 a
4.37 a
2.17 b
2.18 a
2.89 a
1
Analysis of variance: site, all values nonsignificant (ns); season, %
active xylem ns, specific conductance P = 0.013, Huber value P =
0.016, leaf-specific conductance ns; size class, all values ns.
1027
this region (Zobel et al. 2001).
Values of Ψplant,midday were usually less than –1 MPa for most
seedlings, except during the rainy season, as observed for mature sal at the same sites in spring and summer (Zobel et al.
2001). Although Ψplant,midday fluctuated seasonally in seedlings
of all sizes, it remained above the turgor loss point (Ψπz) except in seedlings in the smallest size class at the upper-slope
site during winter.
Mortality of small sal seedlings is high (Troup 1921, Rao
and Singh 1985). At some sites and in some years, most shoots
die during the dry season, although roots often remain alive
and may reestablish shoots from buds when rains arrive (Troup
1921, Rao and Singh 1985). The belowground part thus may
grow using photosynthate from several generations of shoots.
Establishing roots in deeper soil is an important part of the regeneration process, especially in environments with long
drought periods and competition from established trees
(Stoneman et al. 1995). A similar cycle of shoot dieback and
regeneration has been reported in some oak species in Europe
(Becker and Levy 1983), North America (Hibbs and Yoder
1993) and the Himalaya (Troup 1921, Singh and Singh 1992).
Drought is generally considered to be a major predisposing
factor for shoot dieback (Bréda et al. 1992).
Given our finding that Ψplant seldom dropped below the
turgor loss point (even for the smallest seedlings), and the ability of seedlings to replace dead shoots (Singh and Singh 1989),
we conclude that drought does not kill larger seedlings. We
also conclude that drought is not the primary source of regeneration failure for sal in the areas and years we studied.
Measurements made during a more severe drought, as occurred in the Himalaya in 1999 (Singh et al. 2000), and concurrent observations of seedling development and mortality,
are required to confirm this conclusion.
Adaptation to drought
Plant Ψ and gw were the only water relations parameters that
differed with seedling size. Stomatal closure was the primary
adjustment to low Ψplant in small seedlings. Osmotic, elastic
and xylem properties did not differ among seedling size
classes. Consistently lower Ψplant and a continuous decrease in
Ψplant and gw until midday in small seedlings (Figure 2) indicate how readily a young seedling can become stressed.
Seedlings in all size classes sometimes had high gw, especially in fall, winter and spring at the two low-elevation sites.
During wet or cool weather, midday gw remained high for all
sizes of seedlings (Table 6), even at a low Ψsoil. The higher gw
values (Tables 5 and 6) were on the higher side of the range
measured for trees in Himalaya and elsewhere (S.C. Garkoti,
unpublished data). For example, most fall values at the alluvial
and lower-slope sites, and winter values at the alluvial site, exceeded those of all 10 species of potted subtropical evergreens
compared in Taiwan (Liao and Weng 2002).
Seedlings in the smallest size class often had lower gw than
larger seedlings. The higher Ψplant and gw of the large seedlings
probably allowed them to support relatively high rates of photosynthesis, and consequently faster growth compared with
the smallest seedlings (Stoneman et al. 1994a, 1994b).
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
1028
GARKOTI, ZOBEL AND SINGH
Table 9. Spearman rank correlation coefficients of soil water potential (Ψsoil ) with plant water relations properties (Ψplant,predawn = plant water potential measured before dawn; gw = leaf conductance; ε = bulk modulus of elasticity; and RWC = relative water content). There were no significant
correlations with properties not listed in the table. Symbols: *** = P < 0.001; ** = 0.001 < P < 0.01; and * = 0.01 < P < 0.05.
Ψsoil at 10 cm
Ψsoil at 60 cm
Ψsoil at 60 cm
Ψplant,predawn
Midday gw
ε
RWC
Huber value
Specific conductance
0.97***
–
0.29*
0.33**
–0.34**
–0.45***
0.43**
0.43**
0.63***
0.59***
–0.48*
–0.48*
0.60**
0.60**
Table 10. Spearman rank correlation coefficients among plant water relations properties (Ψplant,predawn and Ψplant,midday = plant water potential measured before dawn and during midday, respectively; gw = leaf conductance; Ψπf = osmotic potential at full turgor; Ψπz = osmotic potential at zero
turgor; ε = bulk modulus of elasticity; and RWC = relative water content). There were no significant correlations with properties not listed in the table. Symbols: *** = P < 0.001; ** = 0.001 < P < 0.01; * = 0.01 < P < 0.05; and ns = not significant.
Ψplant,predawn
Ψplant,midday
Morning gw
Midday gw
Ψπf
Ψπz
ε
RWC
Ψplant,midday
Morning gw
Midday gw
Ψπf
Ψπz
ε
RWC
Specific conductance
0.59***
ns
0.35**
ns
0.46***
0.69***
ns
0.37*
0.36*
0.43*
0.33*
0.44**
ns
0.46**
0.84***
ns
ns
ns
ns
ns
ns
0.39**
ns
ns
ns
0.30*
0.42**
0.77***
0.61**
0.61**
ns
ns
ns
ns
ns
ns
Leaf conductance appeared to be related to leaf development, because it decreased in early summer and in summer,
when leaves expanded and matured. After replenishment of
soil water during the rainy season, gw was high in the fall. Despite low Ψsoil, sal seedlings continued to transpire in winter.
High gas exchange in sal seedlings from fall through early
summer indicates that the plants were insensitive to soil and atmospheric drought. This tolerance may allow sal to maintain
positive CO2 assimilation rates under moderate to severe
drought conditions, enabling it to dominate sites over a large
range of environmental conditions.
Seedlings also showed seasonal changes in osmotic and xylem properties. During early leaf growth, osmotic potential
was low; during winter, with dry soil, tissue was the most elastic. There appeared to be a tradeoff between the leaf:xylem ratio and the specific conductance of xylem, with high specific
conductance when the leaf:xylem ratio was high. Thus, leafspecific xylem conductance did not vary among seasons. During the rainy season, seedlings appeared least adapted to
drought, having high osmotic potential (Ψπ ) and RWC z, and
low tissue elasticity.
Osmotic potential was lowest during leafing in early summer, highest during the rainy season, and intermediate during
fall and winter. This seasonal pattern contrasts with that of
some other species in which Ψπ remains high at the time of
leafing and then declines continuously, reaching its lowest values in winter (Abrams 1988, Grossnickle 1989). Evergreen
broadleaf species in a non-monsoon temperate climate also
had their highest Ψπ in newly matured leaves (Zobel 1996).
During the late dry season, plants require access to sufficient
water and nutrients from the soil to support tissue expansion.
Low seedling Ψπ during early summer should increase water
uptake and maintain turgor (Morgan 1984, Turner 1986a).
Low Ψπ during leaf development in early summer may be associated with high solute accumulation. Solute accumulation
during leaf development has been reported for certain North
American broadleaf trees as well as conifers (Tyree et al. 1978,
Parker et al. 1982, Pallardy et al. 1983, Ritchie and Shula
1984).
The decline in Ψπ after the rainy season may have occurred
in response to a decrease in atmospheric and soil water contents during fall. Fall temperatures were moderate, so osmotic
adjustment may allow plants to continue photosynthesis and
growth. Many, but not all, evergreen broadleaf species reduce
Ψπ in the fall (Zobel 1996); in the Himalaya, however, Ψπ values for all 11 species measured declined from the rainy season
to the fall season (S.P. Singh, unpublished data). In a central
Himalayan oak species, seedling Ψπ was substantially reduced
by experimental drought (Sharma et al. 2001); the lowest values for sal in our study were similar to those of non-droughted
oaks.
In winter, when leaf mass started to decline, Ψπ did not decrease significantly, although tissue elasticity was high. Increases in Ψπ during drought have also been reported for
several North American plant species (Cline and Campbell
1976, Hinckley et al. 1980). Calkin and Pearcy (1984) suggest
that osmotic adjustment may respond to the lowest Ψplant during the day; in sal seedlings, Ψπz and Ψplant,midday are significantly correlated. However, it is possible that stomatal closure
limits the minimal Ψplant to near Ψπz. Similar to Ψπ, RWCz de-
TREE PHYSIOLOGY VOLUME 23, 2003
SHOREA SEEDLING WATER RELATIONS
clined and ε rose from the rainy season to the fall and winter,
which would further enhance resistance to desiccation.
Survival of extreme drought may not be as essential for sal
seedlings as the ability to develop under conditions of moderate stress. Plants that can delay stomatal closure at low Ψ can
photosynthesize for longer periods (Bannister 1986). Sal seedlings of all sizes showed high gw in dry fall and winter conditions. In spring, larger seedlings maintained high gw, whereas
small seedlings had much lower gw, indicating that larger sal
seedlings are drought tolerant, whereas small seedlings avoid
dehydration through stomatal closure.
Low gw and shoot dieback (Singh and Singh 1989), producing a high root:shoot ratio, are the chief means of drought
avoidance exhibited by the smallest sal seedlings. A shift toward drought tolerance takes place as seedlings enlarge, enabling the seedlings to keep their stomata open longer and
resulting in less frequent shoot dieback.
Acknowledgments
Funds for the research were provided by a grant from the Department
of Science and Technology, New Delhi, India. Dr. A. Tewari and Mr.
C.M.S. Negi provided help during field measurements.
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