Tree Physiology 27, 1595–1605
© 2007 Heron Publishing—Victoria, Canada
Plasticity of shoot and needle morphology and photosynthesis of two
Picea species with different site preferences in northern Japan
HIROAKI ISHII,1,2 SATOSHI KITAOKA,3,4 TAIJI FUJISAKI,1 YUTAKA MARUYAMA4,5 and
TAKAYOSHI KOIKE3,6
1
Graduate School of Science and Technology, Kobe University, Kobe 657-8501, Japan
2
Corresponding author ([email protected])
3
Field Science Center for Northern Biosphere Studies, Hokkaido University, Sapporo 060-0809, Japan
4
Hokkaido Research Center, Forestry and Forest Products Research Institute, Sapporo 062-8516, Japan
5
Present address: Research Planning and Coordination Division, Forestry and Forest Products Research Institute, Tsukuba 305-8687, Japan
6
Present address: Silviculture and Forest Ecology Studies, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
Received May 29, 2006; accepted April 20, 2007; published online August 1, 2007
Summary We compared shoot and needle morphology and
photosynthesis in Picea glehnii (Friedr. Schmidt) M.T. Mast.
and Picea jezoensis (Sieb. et Zucc.) Carr. trees planted on immature volcanic ash and well-developed brown forest soils to
investigate whether species differences in morphological and
physiological plasticity affected tree growth on different soil
types. Height growth of P. glehnii was reduced by about 10%
on volcanic ash compared with forest soil, whereas that of
P. jezoensis was reduced by more than 60%. Needle morphology of P. glehnii was unaffected by soil type. In contrast, needles of P. jezoensis trees growing on volcanic ash were shorter,
narrower and thicker, with less dry mass and area, than those of
trees growing on forest soil, and specific needle area was lower,
indicating lower foliar light-interception efficiency. In both
species, changes in needle morphology with increasing irradiance were similar in trees growing on both soil types, indicating that plasticity of needle morphology was unaffected by
soil type. In both species, shoot mass and shoot silhouette area
were lower and needle mass per unit shoot mass was higher in
trees growing on volcanic ash than in trees growing on forest
soil. Trees of both species had more needles per unit shoot
length, lower shoot silhouette to projected needle area ratios
and lower shoot silhouette areas per unit shoot mass (SAM) on
volcanic ash than on forest soil, indicating lower shoot-level
light-interception efficiency. For P. glehnii, the response of
shoot morphology to increasing irradiance was similar on both
soil types, with the exception of SAM, which showed lower
plasticity in trees growing on volcanic ash. In contrast,
shoot-level morphological plasticity of P. jezoensis was reduced in trees growing on volcanic ash. Light-saturated maximum photosynthetic rate (Pmax ) of P. glehnii was unaffected by
soil type, whereas mass-based Pmax of P. jezoensis was lower in
trees growing on volcanic ash than in trees growing on forest
soil. In P. jezoensis trees growing on forest soil, area-based Pmax
increased with increasing irradiance, but this response was not
observed in trees growing on volcanic ash. As a result, areabased Pmax at the top of the canopy was 39 to 54% lower in trees
growing on volcanic ash than in trees growing on forest soil.
Our results indicate that constraints on morphological acclimation to high irradiances may contribute to reduced height
growth of P. jezoensis on volcanic ash.
Keywords: morphological plasticity, photosynthetic acclimation, Picea glehnii, Picea jezoensis, shoot architecture.
Introduction
Conifer needles and shoots show great morphological and
physiological plasticity in response to changes in irradiance.
Morphological acclimation to the vertical light gradient from
the lower to the upper canopy, including increasing needle
mass per area, decreasing shoot area to needle area ratio and
decreasing needle mass to shoot mass ratio (Oker-Blom and
Smolander 1988, Smolander et al. 1994, Niinemets and Kull
1995a, 1995b, Richardson et al. 2001, Stenberg et al. 2001),
contributes to the vertical gradient of photosynthetic rates
within the canopy of conifer stands (Carter and Smith 1985,
Jordan and Smith 1993, Palmroth and Hari 2001). Light penetrates more deeply into conifer canopies than into broadleaved canopies, allowing conifers to develop deep canopies
with high leaf area indices (Whitehead et al. 1990, Stenberg
1998). The corresponding changes in shoot and needle morphology with the vertical light gradient are expected to optimize photosynthetic rate per unit of light intercepting area and
maximize carbon gain of the canopy (Stenberg 1996, Niinemets 1997a, Bernier et al. 2001, Cescatti and Zorer 2003).
Tree growth may be reduced if factors such as nutrient or
hydraulic limitation constrain morphological acclimation to
light. For example, nutrient limitation reduces morphological
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ISHII, KITAOKA, FUJISAKI, MARUYAMA AND KOIKE
and physiological plasticity of shoots and needles of Pinus
sylvestris L. such that the capacity for acclimation to high
irradiance is lower on infertile soil than on fertile soil
(Niinemets et al. 2001, 2002a). In tall trees, needle morphology is affected by hydraulic limitation such that low turgor
during needle development prevents cell expansion, resulting
in reduced needle size in the upper crown (Koch et al. 2004,
Woodruff et al. 2004). Constraints on morphological acclimation to high irradiance may reduce light-interception efficiency and thus, the area-based photosynthetic capacity of upper-crown shoots (Niinemets 2002).
We investigated whether constraints on morphological and
physiological acclimation to light affect height growth of
Picea glehnii (Friedr. Schmidt) M.T. Mast. and Picea jezoensis (Sieb. et Zucc.) Carr. In northern Japan, P. glehnii is relatively tolerant of poor growing conditions and forms monospecific stands in swamps and on immature volcanic ash and
serpentine soils (Nakata and Kojima 1987, Matsuda 1989,
Takahashi et al. 2006). In contrast, P. jezoensis prefers well-developed soils and coexists with other species in mixed
broadleaf–conifer forests (Tatewaki and Igarashi 1971, Hiura
et al. 1995, Kayama et al. 2002). Symbiotic mycorrhizae may
contribute to the tolerance of P. glehnii to poor substrates
(Ooishi 2002). Although, on well developed soils, the growth
rate of P. jezoensis is higher than that of P. glehnii, its growth
rate is significantly reduced on immature soils (Kayama 2002,
Ooishi 2002, Ishii et al. 2003, Kayama et al. 2005).
Previous studies showed that height growth of 30-year-old
trees of both species planted in experimental stands on immature volcanic ash were lower than those of trees planted on
well-developed brown forest soil (Ooishi 2002, Ishii et al.
2003). Mean tree height of P. glehnii was about 10% less on
volcanic ash than on forest soil, whereas mean tree height of
P. jezoensis was more than 60% less on volcanic ash than on
forest soil (Ishii et al. 2003, their Table 2). In addition, compared with P. jezoensis, morphological and physiological characteristics of P. glehnii, such as needle longevity, thickness and
nutrient content, were less negatively affected by volcanic ash
(Kayama 2002, Kayama et al. 2002). In both species, massbased photosynthetic rates of lower-canopy shoots were lower
in trees growing on volcanic ash than on forest soil, but
area-based photosynthetic rates were unaffected (Ishii et al.
2003). These findings led to the suggestion that morphological
changes induced by poor growing conditions on volcanic ash
compensate for reduced mass-based photosynthetic rates of
the lower-crown shoots. However, constraints on morphological acclimation to increasing irradiance may limit the extent of
such compensation, and area-based photosynthetic capacity of
upper-crown shoots may be lower in trees growing on volcanic
ash than in trees growing on forest soil. This effect may be
greater for P. jezoensis, which would explain the large difference in this species in height growth between trees growing on
volcanic ash and on forest soil. In this study, we investigated
whether acclimation to high irradiance is constrained by reduced morphological and physiological plasticity of trees
growing on volcanic ash and determined if this effect is greater
for P. jezoensis than for P. glehnii.
Materials and methods
Study site
We compared 30-year-old trees of Picea glehnii and Picea
jezoensis growing in experimental stands planted on immature
volcanic ash or well-developed brown forest soil (Table 1).
The stands were established from seedlings in 1975 at the experimental forest of the Hokkaido Research Center, Forestry
and Forest Products Research Institute in Sapporo, Japan
(43°35′ N, 141°23′ E, 130 m a.s.l.). Mean annual temperature
and total precipitation are 9.1 °C and 1015 mm, respectively.
The trees in the experimental stands are planted on a grid spacing of about 1.5 to 1.7 m (2600–3700 trees ha – 1 ). The stands
on volcanic ash are located within 200 m of each other, and the
stands on brown forest soil are adjacent to each other.
Immature volcanic ash soils in Japan are generally a poor
substrate for tree growth (Tsutsumi 1989). The soil has a low
nutrient content and low microbial activity, and thus low nutrient availability (Ministry of Agriculture and Forestry 1964,
Kawata 1977, Kurobe 1983, Shoji et al. 1993, Nira 2003). Volcanic ash soils are characterized by a high C content (Prévosto
et al. 2004) and high C/N ratio (Shoji et al. 1993). The amount
and activity of soil microorganisms decrease with increasing
C/N ratio and decreasing pH (Okinaga 1952, Yoshida et al.
1979), resulting in low rates of N and P mineralization in soils
with high C/N ratio and low pH (Thompson et al. 1954, Jones
and Parsons 1970, Kawata and Nishida 1973, Kawata 1977).
Low N availability in immature volcanic ash soils is associated
with low water-holding capacity and high silt content, which
limit microbial activity (Nira 2003). In contrast, brown forest
soil has a high nutrient content and high microbial activity, and
thus high nutrient availability (Kawata and Nishida 1973,
Kawata 1977, Ohta and Kumada 1978, Yoshida et al. 1980).
The nutrient content of the volcanic ash soil was one-fourth
that of the forest soil (0.14 g N and 0.30 mg P 100 g – 1, and
0.56 g N and 1.93 mg P 100 g – 1 for volcanic ash and forest soil,
respectively). Soil pH did not differ significantly between the
soil types (5.61 and 5.35 for volcanic ash and forest soil, respectively) (Ooishi 2002). Thus, we inferred that nutrient
availability and soil water content are lower in the volcanic ash
stand than in the forest soil stand, as reflected in needle nutrient concentrations (Table 1).
Light environment, morphology and photosynthesis
Field sampling was done in late August 2003. Three trees
growing along the edge of each stand were chosen for the
study. The edges of the volcanic-ash stands face southwest,
whereas those of the forest-soil stands face south. There were
no trees growing within 5 m of the stand edges. We divided the
crown of each tree into five equal depths from the top
downward. At each depth, we sampled branches growing toward the stand edge. To quantify the light environment at each
sample branch, we measured photosynthetic photon flux
(PPF) with a quantum sensor (LI-190SA, Li-Cor) on a uniformly overcast day. Simultaneous above-canopy measurements were made from a tower located about 200 m from the
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MORPHOLOGICAL AND PHYSIOLOGICAL PLASTICITY IN PICEA
Table 1. Mean tree height, diameter at breast height (DBH) and needle
nutrient concentrations of Picea glehnii and Picea jezoensis stands growing on infertile volcanic ash (VA) and fertile brown forest soil (FS) in
Hokkaido, northern Japan (after Ishii et al. 2003).
Soil type
Height
(m)
DBH
(cm)
Needle nutrient concentration
Nitrogen
(mg g –1 )
Phosphorus
(mg g – 1 )
Picea glehnii
VA
5.7
FS
6.3
11.4
7.4
5.83
9.75
1.28
1.36
Picea jezoensis
VA
2.7
FS
7.4
3.1
12.3
5.89
14.92
1.41
2.05
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boundary threshold value between black and white by referring to the histogram of pixel counts of gray values in the image. Area measurements were made with the “analyze particles” command, which calculates the total area of black pixels
in the image. Measurements of images of metal disks of
known area (10 and 50 cm2 ) confirmed that the relative error
for the method was less than 1%. From the scanned images of
the needles, we obtained the total number of needles per shoot
(n N ) and mean needle length (L N ). Needle width (W N ) and
thickness (T N ) were determined from images of the needle
cross sections.
In addition to the morphological measurements based on
image analysis, the shapes of midpoint needle cross sections
were compared in 50× magnified photographs.
Data analysis
experimental stands and relative PPF (rPPF) was calculated
for each sample branch.
The distal end of each sample branch was cut with a polepruner, immediately recut under water, covered with a plastic
bag and transported to the laboratory. The sample branches
were kept in darkness overnight. We sampled one second-year
shoot (hereafter referred to as the sample shoot) from a second-order axis attached to the main axis of each sample
branch. We measured light-saturated maximum photosynthetic rate (Pmax ) of the sample shoots with a Li-Cor LI-6400
portable gas exchange system fitted with a conifer chamber.
Air temperature and CO2 concentration in the cuvette were
maintained at 25 °C and 370 mmol mol –1, respectively. An external halogen-type light-source (MHF-M1001, Moritex) provided a PPF of 800–1500 µmol m – 2 s –1 for measurement of
Pmax. Because of time constraints, we measured Pmax on only
10 sample shoots covering the full range of irradiances in each
stand.
After making the photosynthetic measurements, we measured the length (L S ) and shoot silhouette area (A S ) of each
sample shoot. For AS measurements, each shoot was placed on
a flatbed scanner (CanoScan 660, Canon) with the upper side
of the shoot facing down. A light box containing two 23-watt
white florescent bulbs was placed over the shoots to illuminate
the background uniformly and eliminate shadows, and the
shoots were scanned at 300 dpi resolution and the maximum
contrast setting to obtain the shoot silhouette image. All needles were then detached from the twig, laid without overlap on
the scanner bed, flattened with a piece of Plexiglas, illuminated with the light box and scanned at 300 dpi to determine
projected needle area (A N ). Five needles from each sample
shoot were cross sectioned at their midpoint, and scanned at
1200 dpi resolution to examine the cross-sectional shape of the
needles. Finally, all needles and shoot axes were oven dried to
constant mass at 80 °C to obtain needle dry mass (M N ) and
shoot dry mass (M S , needles plus shoot axis).
The scanned images of the sample shoots and needles were
analyzed with the Scion Image analysis program (Scion). The
images were converted to binary black and white with the
“threshold” command, which automatically determines the
Specific needle area (SNA = A N /M N ) provided a measure of
foliar light-interception efficiency per unit dry mass invested
in foliage. Needle mass ratio (NMR = M N /M S ) provided a
measure of relative mass allocation to foliage. Needle frequency (n N /L S ), shoot silhouette to projected needle area ratio
(SPAR = A S /AN ) and shoot silhouette area per unit mass (SAM
= A S /M S ) provided measures of foliage display and the lightinterception efficiency of shoots. Shoot silhouette area per unit
mass consists of three components of needle- and shoot-level
light-interception efficiency:
SAM = SNA·NMR·SPAR
(1)
Light-saturated maximum photosynthetic rates of needles
and shoots were converted to mass- and area-based rates
(Pmax /M N , Pmax /A N and Pmax /A S ) and were taken as measures
of photosynthetic capacity. The Pmax /A S rate consists of three
components of needle- and shoot-level morphology and photosynthetic capacity:
Pmax Pmax 1
P NMR
1
=
= max
A S M N SNA SPAR M N SAM
(2)
Effects of irradiance on morphological and photosynthetic
characteristics of needles and shoots were assessed by regression analysis. For each variable, separate linear regressions
were fitted for each species and soil type. The slopes of the relationships were considered to be measures of plasticity in response to irradiance, i.e., steeper slope reflects greater plasticity. For each species, intercepts and slopes of the relationships
were compared by analysis of covariance (separate slope
model) with soil type as the main effect and rPPF as the
covariate. A significant main effect and interaction indicate a
significantly different intercept and slope, respectively.
In closed canopies, irradiance decreases exponentially with
decreasing height, and rPPF values tend to be non-normally
distributed. In such cases, researchers have used log-transformed values of rPPF in regression analyses (e.g., Niinemets
et al. 2003). To avoid a skewed distribution of irradiance, we
chose sample trees on the forest edge. The relationships be-
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ISHII, KITAOKA, FUJISAKI, MARUYAMA AND KOIKE
tween rPPF and various dependent variables in this study were
linear. We compared residuals of regression analyses based on
both raw rPPF values and log-transformed values and determined that log-transformation did not improve the variance
structure of the dependent variable. Therefore, we used raw
rPPF values in our regression analyses, as have others (e.g.,
Niinemets 1997a, 1997b, Niinemets et al. 1998).
Results
Needle and shoot morphology differed between soil types
(Figure 1). Shoot and needle lengths were shorter and needles
were lighter green in trees growing on volcanic ash than in
trees growing on forest soil. Cross-sectional shapes of the needles, however, were similar between soil types (Figure 2).
Needle morphology (L N , W N , TN ), size (MN /n N , A N /n N )
and light-interception efficiency (SNA) of Picea glehnii were
unaffected by soil type (Table 2). In contrast, Picea jezoensis
trees had shorter, narrower and thicker needles with less mass,
less area and lower SNA on volcanic ash than on forest soil. In
both species, needle length and projected area were uncorrelated with irradiance, whereas needle mass increased and
SNA decreased with increasing irradiance (Table 2, Figure 3).
For all measures of needle morphology, soil type had no effect
on the slopes of the relationships with irradiance (P > 0.05).
In P. glehnii, MS and A S were smaller and NMR was higher
Figure 1. Shoot structure of 30-year-old Picea glehnii and Picea
jezoensis growing on infertile volcanic ash (VA) and fertile brown forest soil (FS) in Hokkaido, northern Japan. On volcanic ash, both upper-crown (top row) and lower-crown (bottom row) shoots are shorter
and needles are shorter and lighter in color than on brown forest soil.
on volcanic ash than on forest soil (Table 2). In P. jezoensis,
shoot mass was similar between the soil types, but AS was
smaller and NMR was higher on volcanic ash than on forest
soil. In P. glehnii, MS and A S increased and NMR decreased
with increasing irradiance on both soil types. Soil type had no
effect on the slopes of the relationships with irradiance
(P > 0.05). In contrast, in P. jezoensis growing on volcanic ash,
shoot mass and NMR were uncorrelated with irradiance, indicating less plasticity of shoot size and biomass allocation to foliage than in trees growing on forest soil.
In P. glehnii, needle frequency (n N /L S ) was higher and
SPAR was lower on volcanic ash than on forest soil (Table 2).
Soil type had no effect on SAM of P. glehnii. In P. jezoensis,
needle frequency was higher and SPAR and SAM were lower
in trees growing on volcanic ash soil, indicating greater
within-shoot self-shading and thus lower light-interception efficiency than on forest soil. In P. glehnii, needle frequency,
SPAR and SAM showed significant correlations with irradiance on both soil types (Figure 4). The slopes of the relationships for needle frequency and SPAR were unaffected by soil
type, but the slope for SAM was less steep on volcanic ash than
on forest soil. For P. jezoensis, needle frequency showed no response to irradiance on volcanic ash, whereas SPAR and SAM
decreased with increasing irradiance on both soil types. The
slope for SPAR was unaffected by soil type, but the slopes for
needle frequency and SAM were less steep on volcanic ash, indicating less shoot-level plasticity of light-interception efficiency, than on forest soil.
In P. glehnii, Pmax /M N and Pmax /A N were unaffected by soil
type, whereas Pmax /A S was higher on volcanic ash than on forest soil (Table 2). In contrast, in P. jezoensis, all measures of
Pmax were lower on volcanic ash soil than on forest soil. In
P. glehnii, Pmax was uncorrelated with irradiance (Figure 5). In
P. jezoensis, Pmax /M N was uncorrelated with irradiance, but
Pmax /A N and Pmax /A S increased with increasing irradiance in
trees growing on forest soil. In trees growing on volcanic ash,
however, neither Pmax /A N nor Pmax /A S was correlated with
irradiance. As a result, Pmax /A N and Pmax /A S at the top of the
canopy on volcanic ash soil were reduced by 54 and 39%, respectively, relative to the rates observed on forest soil.
Figure 2. Needle cross sections of 30-year-old Picea glehnii and
Picea jezoensis trees growing on infertile volcanic ash (VA) and fertile brown forest soil (FS) in Hokkaido, northern Japan. Top row: upper-crown, bottom row: lower-crown.
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Table 2. Morphological and photosynthetic characteristics of needles and shoots in relation to irradiance for 30-year-old Picea glehnii and Picea
jezoensis growing on infertile volcanic ash (VA) and fertile brown forest soil (FS) in Hokkaido, northern Japan. Data shown are intercepts, slopes
and coefficients of determination (r 2 ) for each variable in relation to relative photosynthetic photon flux. Abbreviations: L N , needle length (mm);
W N , needle width (mm); T N , needle thickness (mm); M N /n N , dry mass per needle (mg); A N /n N , projected area per needle (mm2 ); SNA, specific
needle area (cm2 g –1 ); M S , shoot mass (g); A S , shoot silhouette area (cm2 ); NMR, needle mass ratio (M N /M S ); n N /L S , number of needles per cm
shoot length; SPAR, shoot silhouette area to projected needle area ratio (A S /A N ); SAM, shoot silhouette area per unit mass (cm2 g – 1 ); Pmax /M N ,
light-saturated maximum photosynthetic rate per needle mass (nmol CO2 g – 1 s – 1 ); Pmax /A N , projected needle area (µmol CO2 m – 2 s – 1 ); and
Pmax /A S , shoot silhouette area (µmol CO2 m – 2 s –1 ). Asterisks denote statistically significant differences between soil types in the intercept or
slope (* P < 0.05, ** P < 0.01, *** P < 0.001). Slope estimates in parenthesis denote insignificant regressions.
Variable
Soil type
Needle morphology
LN
VA
FS
P. glehnii
P. jezoensis
Intercept
Slope
r2
Intercept
Slope
r2
8.55
8.34
(0.014)
(0.012)
0.129
0.093
13.0***
19.2
(0.018)
(0.019)
0.068
0.048
WN
VA
FS
0.72
0.54
0.006
0.011
0.737
0.427
1.18*
1.29
(0.001)
(0.002)
0.084
0.128
TN
VA
FS
0.84
0.82
(0.001)
0.003
0.049
0.297
0.23*
0.29
0.002
0.002
0.678
0.506
M N /n N
VA
FS
1.72
1.41
0.015
0.019
0.564
0.295
2.00***
3.36
0.018
0.018
0.426
0.309
A N /n N
VA
FS
6.81
6.89
(0.020)
(0.014)
0.216
0.051
12.9***
22.7
SNA
VA
FS
–0.121
–0.255
0.802
0.444
0.010
0.012
0.048
0.053
Shoot morphology
MS
VA
FS
38.5
47.2
–0.02*
0.08
AS
VA
FS
2.06***
4.22
NMR
VA
FS
0.85***
0.68
n N /L S
VA
FS
SPAR
VA
FS
SAM
VA
FS
Photosynthetic capacity
Pmax /M N
VA
FS
29.9***
20.9
0.54***
0.68
19.5
24.8
8.8
10.0
Pmax /A N
VA
FS
2.25
2.26
Pmax /A S
VA
FS
3.56*
2.94
(0.032)
(–0.008)
0.080
0.006
57.8*
67.4
–0.174
–0.271
0.391
0.682
0.641
0.693
0.31
0.38
(0.006)
0.007
0.117
0.425
0.516
0.641
9.0***
13.5
(–0.026)
(0.001)
0.035
< 0.001
0.454
0.220
0.72*
0.73
(–0.0001)
–0.002
< 0.001
0.324
0.199
0.163
0.519
0.395
31.1***
16.5
(0.002)*
0.135
< 0.001
0.594
–0.002
–0.003
0.786
0.595
0.51**
0.65
–0.139**
–0.260
0.890
0.740
(–0.045)
(–0.064)
0.276
0.365
(–0.005)
(–0.006)
0.059
0.071
(0.011)
(0.002)
0.084
0.003
(–0.002)
(–0.003)
Discussion
Differences in height growth and morphology between trees
growing on volcanic ash and forest soil were less in Picea
glehnii than in Picea jezoensis, whereas P. jezoensis had a
higher growth rate than P. glehnii on brown forest soil. We
–0.002
–0.003
0.287
0.453
23.1**
32.6
–0.142*
–0.251
0.393
0.711
14.4***
21.9
(–0.024)
(–0.006)
0.078
0.002
2.55***
3.18
(0.002)
0.015
0.031
0.495
2.55*
3.93
(0.025)*
0.071
0.031
0.821
found that differences in morphological plasticity, and the degree to which it is affected by soil conditions, may explain the
differences in the effect of soil type on the growth rates of
P. glehnii and P. jezoensis.
Needle morphology of P. glehnii was unaffected by soil
type, whereas needle size of P. jezoensis was smaller in trees
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ISHII, KITAOKA, FUJISAKI, MARUYAMA AND KOIKE
Figure 3. Dry mass and projected needle
area of individual needles (MN /n N and
AN /n N , respectively) and specific needle
area (SNA; projected needle area per unit
mass) in relation to relative photosynthetic
photon flux (rPPF) of 30-year-old Picea
glehnii and Picea jezoensis growing on infertile volcanic ash (open symbols, thin
line) and fertile brown forest soil (filled
symbols, thick line) in Hokkaido, northern
Japan. Separate linear regressions were fitted for each species and soil type. Solid
lines denote significant (P < 0.05) and
dashed lines denote insignificant relationships.
growing on volcanic ash. However, in both species, soil type
had no effect on foliar plasticity in response to the vertical
within-canopy light gradient, indicating that soil conditions
did not affect needle-level morphological acclimation to light.
In both species, shoots were smaller, relative mass allocation
to foliage was greater and shoot-level light-interception efficiency was less in trees growing on volcanic ash compared
with trees on forest soil. In Picea glehnii, NMR was greater
and SPAR was lower in trees growing on volcanic ash than on
forest soil (Table 2); however, SAM was unaffected by soil
type. Picea glehnii allocated less biomass per unit light-intercepting area (i.e., greater SAM) at high irradiances on volcanic ash than on forest soil, but this trend was reversed at low irradiances (significant interaction between soil type and rPPF,
Figure 4). As a result of the shift in shoot-level mass-area allocation pattern, shoot-level light-interception efficiency was
unaffected by soil type. However, the change in shoot-level
mass-area allocation resulted in reduced plasticity of SAM in
trees growing on volcanic ash compared with forest soil, although morphological plasticity of other measures was unaffected by soil type. In contrast, in P. jezoensis, SAM and all of
its components were affected by soil type, indicating that both
needle- and shoot-level morphological changes contributed to
reduced light-interception efficiency on volcanic ash. The
light-related response of NMR was constrained and shootlevel morphological plasticity was reduced on volcanic ash,
indicating that the poor growing conditions on volcanic ash
constrain shoot-level morphological acclimation to increasing
irradiance in P. jezoensis.
Ishii et al. (2003) showed that needle- and shoot-level morphological responses compensated for reduced mass-based
Pmax in lower-canopy shoots of P. glehnii, such that area-based
TREE PHYSIOLOGY VOLUME 27, 2007
MORPHOLOGICAL AND PHYSIOLOGICAL PLASTICITY IN PICEA
1601
Figure 4. Measures of light-interception
efficiency of shoots: needle frequency
(n N /L S ; number of needles per cm shoot
length), SPAR (shoot silhouette to projected needle area ratio) and SAM (shoot
silhouette area per unit mass) in relation to
relative photosynthetic photon flux (rPPF)
of 30-year-old Picea glehnii and Picea
jezoensis growing on infertile volcanic ash
(open symbols, thin line) and fertile brown
forest soil (filled symbols, thick line) in
Hokkaido, northern Japan. Separate linear
regressions were fitted for each species
and soil type. Solid lines denote significant (P < 0.05) and dashed lines denote insignificant relationships.
Pmax was similar or greater for trees growing on volcanic ash
compared with trees growing on forest soil. In our study, soil
type did not affect Pmax /M N or Pmax /A N of P. glehnii. Furthermore, Pmax /A S of P. glehnii was greater in trees growing on
volcanic ash than on forest soil, indicating that shoot-level
morphological acclimation compensates for reduced Pmax /M N
in this species. In contrast, Pmax /M N of P. jezoensis was reduced in trees growing on volcanic ash. However, Pmax /A N and
Pmax /A S were less affected by soil type, indicating that morphological adjustments, such as lower SNA, SPAR and SAM,
compensate for reduced Pmax /M N. In P. jezoensis, light-related
responses of NMR and SAM were constrained on volcanic
ash. The constraint on morphological acclimation to high
irradiance led to reduced plasticity in area-based photosynthetic capacity and resulted in a large difference between the
two soil types in area-based Pmax in the upper crown. Reduced
photosynthetic capacity of upper-crown shoots likely contrib-
uted to reduced height growth of P. jezoensis growing on volcanic ash.
Canham (1988) proposed that morphological acclimation to
light gradients may be more readily achieved than physiological acclimation because the former incurs less metabolic costs.
Macro-scale morphological properties, such as specific leaf
area, are more effective at increasing carbon gain than cellular-level acclimation (Evans and Poorter 2001, Niinemets et
al. 2002b). Theoretical investigation suggests that, although
alterations in leaf anatomy and foliar biochemistry are equally
important for photosynthetic acclimation to shade, leaf anatomical responses are more important than changes in foliar
biochemistry for acclimation to high irradiance (Niinemets
and Tenhunen 1997). For broad-leaved species exposed to
high irradiances, increasing leaf thickness is necessary to create space for chloroplasts along the surface of mesophyll cells
(Oguchi et al. 2003). In conifers, shoot-level morphological
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
1602
ISHII, KITAOKA, FUJISAKI, MARUYAMA AND KOIKE
Figure 5. Mass- and area-based light-saturated photosynthetic rates per unit needle
mass (P max /M N ), projected needle area
(P max /A P ) and shoot silhouette area
(P max /A S ) in relation to relative
photosynthetic photon flux (rPPF) of
30-year-old trees of Picea glehnii and
Picea jezoensis growing on infertile volcanic ash (open symbols, thin line) and fertile brown forest soil (filled symbols, thick
line) in Hokkaido, northern Japan. Separate linear regressions were fitted for each
species and soil type. Solid lines denote
significant (P < 0.05) and dashed lines denote insignificant relationships.
acclimation (e.g., needle orientation and within-shoot shading) contributes to shade acclimation by increasing light-interception efficiency (Smith et al. 1991). Similarly, changes in
shoot morphology contribute to acclimation to high irradiance. For example, increasing needle mass per area and decreasing SPAR in response to increasing irradiance compensates for decreasing mass-based photosynthetic capacity in
P. abies and P. sylvestris (Stenberg et al. 2001, Niinemets
2002).
Morphological acclimation to high irradiance may be constrained by nutrient availability (Grassi and Minotta 2000,
Niinemets et al. 2001, 2002a). With sufficient nutrients, saplings of P. abies transferred from low to high irradiance
showed increases in both mass- and area-based photosynthetic
capacity, but area-based photosynthetic capacity showed no
increase when nutrients were limited (Grassi and Minotta
2000). Nutrient availability affects photosynthetic capacity
per unit volume or mass, whereas photosynthetic capacity per
unit area is influenced by morphological changes (Hom and
Oechel 1983, Sims et al. 1998). In conifers, the negative effect
of nutrient limitation on morphological acclimation to high
irradiance may be incurred at different levels of morphological
organization. For example, plasticity in morphological and
photosynthetic characteristics are constrained by nutrient limitation at both the needle and shoot levels in P. sylvestris
(Niinemets et al. 2001, 2002a). Nutrient constraints on shootlevel morphological acclimation to light has marked effects on
tree growth in P. abies (Grassi and Minotta 2000).We observed
that soil type had no effect on needle-level morphological
plasticity of P. glehnii or P. jezoensis, whereas shoot-level
plasticity was less on volcanic ash. As a result, area-based
photosynthetic capacity of P. jezoensis was lower in trees
growing on volcanic ash.
The observed constraints on shoot-level morphological acclimation to high irradiance may be the result of nutrient limitation on immature volcanic ash. Photosynthetic rates of trees
TREE PHYSIOLOGY VOLUME 27, 2007
MORPHOLOGICAL AND PHYSIOLOGICAL PLASTICITY IN PICEA
growing on infertile soils are generally lower than those of
trees growing on fertile soils because of shortages of important
nutrients such as N and P (Linder 1987, Kozlowski and
Pallardy 1996, Niinemets et al. 2001). This has been demonstrated for various coniferous species through comparative
studies of trees and saplings growing on sites differing in fertility (e.g., Smolander and Oker-Blom 1989, Niinemets et al.
2001) and through experimental fertilization studies (e.g.,
Mitchell and Hinckley 1993, Grassi and Minotta 2000,
Ripullone et al. 2003). Although some studies show no positive effect of fertilization on photosynthetic rate (Brix and
Ebell 1969, George et al. 1999) or shoot morphology (Palmroth et al. 2002), nutrient limitation may have significant negative effects. Nutrient availability directly affects mass-based
photosynthetic rate, whereas photosynthetic rate per light intercepting area is affected by changes in needle and shoot morphology (Carter and Smith 1985, Stenberg et al. 1995,
Niinemets et al. 2001). Morphological changes such as increases in needle mass per area can compensate for reduced
mass-based photosynthetic rate on infertile soils and maintain
or increase area-based photosynthetic rates (Niinemets 1999,
Ishii et al. 2003). However, if nutrient limitation constrains
morphological acclimation, the negative effects of low nutrient availability on photosynthetic capacity may be exacerbated.
Water availability is another factor that affects shoot and
needle morphology. In 100-m-tall Sequoia sempervirens (D.
Don.) Endl. trees, shoots become shorter and needles more
appressed to the shoot axis with increasing height as a result of
hydraulic limitation (Koch et al. 2004). In tall Pseudotsuga
menziesii Franco var. menziesii trees, hydraulic limitation reduces turgor pressure in the upper crown and may prevent cell
expansion during needle development, resulting in shorter
needles (Woodruff et al. 2004). Hydraulic limitation induces
lower stomatal conductance in the upper crown, and the resulting decline in photosynthetic rate is postulated to limit height
growth (Ryan and Yoder 1997, Ryan et al. 2006). Aside from
reduced stomatal conductance, hydraulic constraints on shoot
and needle morphology reduces light-interception efficiency
of upper-crown shoots, and this may exacerbate the negative
effects of hydraulic limitation on photosynthesis and height
growth (Niinemets 2002). In our study, differences in soil texture between the two soil types, resulting in lower water-holding capacity of volcanic ash, may be an additional factor contributing to reduced morphological and physiological plasticity.
We demonstrated that P. glehnii and P. jezoensis differ in
morphological plasticity in response to changes in soil conditions. Picea jezoensis exhibits characteristics adapted to
brown forest soil, i.e., greater morphological plasticity allows
this species to exploit favorable growing conditions and realize high growth rates, which may contribute to its survival in
competition with other tree species in mixed broadleaf–conifer forests. By contrast, P. glehnii exhibits characteristics
adapted to poor growing conditions on immature substrate
such as volcanic ash. Although this species has low morphological plasticity and its growth rate increased little on brown
1603
forest soil, it is less affected by poor growing conditions.
Mechanisms to increase nutrient uptake, nutrient-use efficiency and mean residence time of nutrients are important for
survival and growth on infertile soils (Aerts and Chapin 2000).
The proportion of roots with symbiotic mycorrhizae increases
significantly in P. glehnii trees planted on volcanic ash compared with trees on brown forest soil, whereas no such increase
is observed in P. jezoensis (Ooishi 2002). Picea glehnii also
shows a smaller reduction in foliar nutrient content and a
greater increase in leaf longevity than P. jezoensis when
planted on nutrient-poor soils (Kayama et al. 2002). These
adaptive responses may contribute to the ability of this species
to form mono-specific stands on immature soils.
Acknowledgments
We thank the staff of FFPRI and FSC Hokkaido University for assistance in the field, and the technical staff of ILTS Hokkaido University
for developing the equipment for measurement of shoot silhouette
area with a flatbed scanner. Many thanks to Drs. M. Kayama,
S. Matsuki and members of the forest eco-physiology lab FSC for assistance and helpful discussions, and to Dr. Y. Watanabe for skillful
preparation and photography of the needle cross sections. Drs. Ülo
Niinemets, Y. Inagaki, Y. Matsuura and T. Suzuki provided helpful
comments during revision.
References
Aerts, R. and F. Chapin, III. 2000. The mineral nutrition of wild plants
revisited: a re-evaluation of processes and patterns. Adv. Ecol. Res.
30:1–67.
Bernier, P.Y., F. Raulier, P. Stenberg and C.-H. Ung. 2001. Importance
of needle age and shoot structure on canopy net photosynthesis of
balsam fir (Abies balsamea): a spatially inexplicit modeling analysis. Tree Physiol. 21:815–830.
Brix, H. and L.F. Ebell. 1969. Effects of nitrogen fertilization on
growth, leaf area, and photosynthetic rate in Douglas-fir. For. Sci.
15:189–196.
Canham, C.D. 1988. Growth and canopy architecture of shade-tolerant trees: response to canopy gaps. Ecology 69:786–795.
Carter, G.A. and W.K. Smith. 1985. Influence of shoot structure on
light interception and photosynthesis in conifers. Plant Physiol.
79:1038–1043.
Cescatti, A. and R. Zorer. 2003. Structural acclimation and radiation
regime of silver fir (Abies alba Mill.) shoots along a light gradient.
Plant Cell Environ. 26:429–442.
Evans, J.R. and H. Poorter. 2001. Photosynthetic acclimation of
plants to growth irradiance: the relative importance of specific leaf
area and nitrogen partitioning in maximizing carbon gain. Plant
Cell Environ. 24:755–767.
George, E., S. Kircher, P. Schwartz, A. Tesar and B. Seith. 1999. Effect of varied soil nitrogen supply on growth and nutrient uptake of
young Norway spruce plants grown in a shaded environment.
J. Plant Nutr. Soil Sci. 162:301–307.
Grassi, G. and G. Minotta. 2000. Influence of nutrient supply on
shade–sun acclimation of Picea abies seedlings: effects on foliar
morphology, photosynthetic performance and growth. Tree
Physiol. 20:645–652.
Hiura, T., K. Fujiwara, H. Hojyo et al. 1995. Stand structure and
long-term dynamics of primeval forests in Nakagawa Experimental
Forest, Hokkaido University. Research Bulletin of the Hokkaido
University Forest 52:85–94.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
1604
ISHII, KITAOKA, FUJISAKI, MARUYAMA AND KOIKE
Hom, J.L. and W.C. Oechel. 1983. The photosynthetic capacity, nutrient content, and nutrient use efficiency of different needle ageclasses of black spruce (Picea mariana) found in interior Alaska.
Can. J. For. Res. 13:834–839.
Ishii, H., M. Ooishi, Y. Maruyama and T. Koike. 2003. Acclimation of
shoot and foliage morphology and photosynthesis of two Picea
species to differences in soil nutrient availability. Tree Physiol.
23:453–461.
Jones, M.J. and J.W. Parsons. 1970. The incluence of soil C/N ratio
on nitrogen mineralization during anaerobic incubation. Plant Soil
32:258–262.
Jordan, D.N. and W.K. Smith. 1993. Simulated influence of leaf geometry on sunlight interception and photosynthesis in conifer needles. Tree Physiol. 13:29–39.
Kawata, H. 1977. Nitrogen forms of representative Japanese forest
soils. Bull. Gov. For. Exp. Sta. 297:105–131.
Kawata, H. and T. Nishida. 1973. Phosphorus forms in representative
Japanese forest soils. Bull. Gov. For. Exp. Sta. 250:1–34.
Kayama, M. 2002. Adaptations of Picea species to serpentine soils:
applications to environmental restoration. Ph.D. Thesis, Faculty of
Agriculture, Hokkaido University, 136 p.
Kayama, M., K. Sasa and T. Koike. 2002. Needle life span, photosynthetic rate and nutrient concentration of Picea glehnii, P. jezoensis and P. abies planted on serpentine soil in Northern Japan.
Tree Physiol. 27:707–716.
Kayama, M., A.M. Quoreshi, S. Uemura and T. Koike. 2005. Differences in growth characteristics and dynamics of elements absorbed
in seedlings of three spruce species raised on serpentine soil in
northern Japan. Ann. Bot. 95:661–672.
Koch, G.W., S.C. Sillett, G.M. Jennings and S.D. Davis. 2004. The
limits to tree height. Nature 428:851–854.
Kozlowski, T.T. and S.G. Pallardy. 1996. Physiology of woody plants.
Academic Press, San Diego, 411 p.
Kurobe, T. 1983. Volcanic ash and soil. Hakuyusha, Tokyo, 310 p. In
Japanese.
Linder, S. 1987. Responses to water and nutrients in coniferous ecosystems. In Potentials and Limitations of Ecosystem Analysis. Eds.
E.-D. Schulze and H. Zwölfer. Springer-Verlag, Berlin,
pp 180–202.
Matsuda, K. 1989. Regeneration and growth in the Picea glehnii forest. Research Bulletin of the Hokkaido University Forest 46:
595–717.
Ministry of Agriculture and Forestry. 1964. Volcanic ash soils in Japan. Secretariat of Agriculture, Forestry and Fisheries Research
Council, Tokyo, 211 p. In Japanese.
Mitchell, A.K. and T.M. Hinckley. 1993. Effects of foliar nitrogen
concentration on photosynthesis and water use efficiency in Douglas-fir. Tree Physiol. 12:403–410.
Nakata, M. and S. Kojima. 1987. Effects of serpentine substrate on
vegetation and soil development with special reference to Picea
glehnii forest in Teshio District, Hokkaido, Japan. For. Ecol. Manage. 20:265–290.
Niinemets, Ü. 1997a. Distribution and patterns of foliar carbon and
nitrogen as affected by tree dimensions and relative light conditions
in the canopy of Picea abies. Trees 11:144–154.
Niinemets, Ü. 1997b. Acclimation to low irradiance in Picea abies:
influences of past and present light climate on foliage structure and
function. Tree Physiol. 17:723–732.
Niinemets, Ü. 1999. Components of leaf dry mass per area—thickness and density—alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol. 144:35–47.
Niinemets, Ü. 2002. Stomatal conductance alone does not explain the
decline in foliar photosynthetic rates with increasing tree age and
size in Picea abies and Pinus sylvestris. Tree Physiol. 22:515–535.
Niinemets, Ü. and O. Kull. 1995a. Effects of light availability and tree
size on the architecture of assimilative surface in the canopy of
Picea abies: variation in needle morphology. Tree Physiol. 15:
307–315.
Niinemets, Ü. and O. Kull. 1995b. Effects of light availability and tree
size on the architecture of assimilative surface in the canopy of
Picea abies: variation in shoot structure. Tree Physiol. 15:791–798.
Niinemets, Ü. and J.D. Tenhunen. 1997. A model separating leaf
structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant Cell
Environ. 20:845–866.
Niinemets, Ü., O. Kull and J.D. Tenhunen. 1998. An analysis of light
effects on foliar morphology, physiology and light interception in
temperate deciduous woody species of contrasting shade tolerance.
Tree Physiol. 18:681–696.
Niinemets, Ü., D.S. Ellsworth, A. Lukjanova and M. Tobias. 2001.
Site fertility and the morphological and photosynthetic acclimation
of Pinus sylvestris needles to light. Tree Physiol. 21:1231–1244.
Niinemets, Ü., A. Cescatti, A. Lukjanova, M. Tobias and L. Truus.
2002a. Modification of light-acclimation of Pinus sylvestris shoot
architecture by site fertility. Agric. For. Meteorol. 111:121–140.
Niinemets, Ü., A. Portsmuth and L. Truus. 2002b. Leaf structural and
photosynthetic charactersitics, and biomass allocation to foliage in
relation to foliar nitrogen content and tree size in three Betula species. Ann. Bot. 89:191–204.
Niinemets, Ü., F. Valladares and R. Ceulemans. 2003. Leaf-level
phenotypic variability and plasticity of invasive Rhododendron
ponticum and non-invasive Ilex aquifolium co-occuring at two contrasting European sites. Plant Cell Environ. 26:941–956.
Nira, R. 2003. Microbial, physical and chemical factors causing
higher gross rate and lower net rate of nitrogen mineralization in
volcanic ash soils than in alluvial soils in the Tokachi District. Soil
Sci. Plant Nutr. 49:417–423.
Oguchi, R., K. Hikosaka and T. Hirose. 2003. Does photosynthetic
light-acclimation need change in leaf anatomy? Plant Cell Environ.
26:505–512.
Ohta, S. and K. Kumada. 1978. Studies on the humus forms of forest
soils. VI. Mineralization of nitrogen in brown forest soils. Soil Sci.
Plant Nutr. 24:41–54.
Oker-Blom, P. and H. Smolander. 1988. The ratio of shoot silhouette
area to total needle area in Scots pine. For. Sci. 34:894–906.
Okinaga, T. 1952. Microbiological studies of forest soils II. The soil
microflora of the forest of Thujopsis hondai. J. Jpn. For. Soc.
34:227–231.
Ooishi, M. 2002. The effects of symbiotic mycorrhiza on the nutrient
dynamics and photosynthesis of Picea glehnii planted on undeveloped volcanic ash. M.Sc. Thesis, Faculty of Agriculture, Hokkaido
University, 54 p.
Palmroth, S. and P. Hari. 2001. Evaluation of the importance of acclimation of needle structure, photosynthesis and respiration to available photosynthetically active radiation in a Scots pine canopy.
Can. J. For. Res. 31:1235–1243.
Palmroth, S., P. Stenberg, S. Smolander, P. Voipio and H. Smolander.
2002. Fertilization has little effect on light-interception efficiency
of Picea abies shoots. Tree Physiol. 22:1185–1192.
Prévosto, B., E. Dambrine, C. Moares and T. Curt. 2004. Effects of
volcanic ash chemistry and former agricultural use on the soils and
vegetation of naturally regenerated woodlands in the Massif Central, France. Catena 56:239–261.
Richardson, A.D., P.M.S. Ashton, G.P. Berlyn, M.E. McGroddy and
I.R. Cameron. 2001. Within-crown foliar plasticity of western
hemlock, Tsuga heterophylla, in relation to stand age. Ann. Bot.
88:1007–1015.
TREE PHYSIOLOGY VOLUME 27, 2007
MORPHOLOGICAL AND PHYSIOLOGICAL PLASTICITY IN PICEA
Ripullone, F., G. Grassi, M. Lauteri and M. Borghtti. 2003. Photosynthesis–nitrogen relationships: interpretation of different patterns
between Pseudotsuga menziesii and Populus × euroamericana in a
mini-stand experiment. Tree Physiol. 23:137–144.
Ryan, M.G. and B.J. Yoder. 1997. Hydraulic limits to tree height and
tree growth. BioScience 47:235–242.
Ryan, M.G., N. Phillips and B. Bond. 2006. The hydraulic limitation
hypothesis revisited. Plant Cell Environ. 29:367–381.
Shoji, S., M. Nanjo and R. Dahlgren. 1993. Volcanic ash soils: genesis, properties and utilization. Elsevier, Tokyo, 288 p.
Sims, D.A., J.R. Seeman and Y. Luo. 1998. The significance of differences in mechanisms of photosynthetic acclimation to light, nitrogen and CO2 for return on investment in leaves. Funct. Ecol.
12:185–194.
Smith, W.K., A.W. Schoettle and M. Cui. 1991. Importance of the
method of leaf area measurement to the interpretation of gas exchange of complex shoots. Tree Physiol. 8:121–127.
Smolander, H. and P. Oker-Blom. 1989. The effect of nitrogen content
on the photosynthesis of Scots pine needles and shoots. Ann. Sci.
For. 46:473–475.
Smolander, H., P. Stenberg and S. Linder. 1994. Dependence of light
interception efficiency of Scots pine shoots on structural parameters. Tree Physiol. 14:971–980.
Stenberg, P. 1996. Simulations of the effects of shoot structure and
orientation on vertical gradients in intercepted light by conifer canopies. Tree Physiol. 16:99–108.
Stenberg, P. 1998. Implications of shoot structure on the rate of photosynthesis at different levels in a coniferous canopy using a model
incorporating grouping and penumbra. Funct. Ecol. 12:82–91.
Stenberg, P., S. Linder and H. Smolander. 1995. Variation in the ratio
of shoot silhouette area to needle area in fertilized and unfertilized
Norway spruce trees. Tree Physiol. 15:705–712.
1605
Stenberg, P., S. Palmroth, B.J. Bond, D.G. Sprugel and H. Smolander.
2001. Shoot structure and photosynthetic efficiency along the light
gradient in a Scots pine canopy. Tree Physiol. 21:805–814.
Takahashi, K., M. Yogo and S. Ishibashi. 2006. Stand development
and regeneration during a 33-year period in a seral Picea glehnii
forest, northern Japan. Ecol. Res. 21:35–42.
Tatewaki, M. and T. Igarashi. 1971. Forest vegetation in the Teshio
and the Nakagawa District Experimental Forests of Hokkaido University. Research Bulletin of the Hokkaido University Forest 28:
1–192.
Thompson, L.M., C.A. Black and J.A. Zoellner. 1954. Occurrence
and mineralization of organic phosphorus in soils, with particular
reference to associations with nitrogen, carbon and pH. Soil Sci.
77:185–196.
Tsutsumi, T. 1989. Forest Silviculture. Asakura Shoten, Tokyo, 234 p.
Whitehead, D., J. Grace and M.J.S. Godfrey. 1990. Architectural distribution of foliage in individual Pinus radiata D. Don crowns and
the effects of clumping on radiation interception. Tree Physiol.
7:135–155.
Woodruff, D.R., B.J. Bond and F.C. Meinzer. 2004. Does turgor limit
growth in tall trees? Plant Cell Environ. 27:229–236.
Yoshida, S., D. Miyake and I. Nioh. 1979. Nitrogen dynamics in forest soils. I. Distribution of nitrifying bacteria and nitrifying activity
in the forest surface soils. J. Jpn. For. Soc. 61:21–25. In Japanese.
Yoshida, S., Y. Haruta and I. Nioh. 1980. Nitrogen dynamics in forest
soils. II. Mineralization and nitrifying activity of nitrogen in the
different soil types of brown forest soils under natural vegetation.
J. Jpn. For. Soc. 62:230–233. In Japanese with English abstract.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com