Tree Physiology 20, 1007–1018
© 2000 Heron Publishing—Victoria, Canada
Influence of light availability on leaf structure and growth of two
Eucalyptus globulus ssp. globulus provenances
SHELLEY A. JAMES1,2 and DAVID T. BELL1
1
2
Department of Botany, The University of Western Australia, Nedlands, WA 6907, Australia
Present address: Department of Botany, University of Hawaii, 3190 Maile Way, Honolulu, HI 96822, USA
Received June 30, 1999
Summary Light availability strongly affects leaf structure of
the distinctive ontogenetic leaf forms of Eucalyptus globulus
Labill. ssp. globulus. Late-maturing plants from St. Marys,
Tasmania and early maturing plants from Wilsons Promontory, Victoria (hereafter referred to as Wilsons Prom.) were
grown for 9 months in 100, 50 or 10% sunlight. Growth, biomass and leaf area were significantly reduced when plants
were grown in 10% sunlight. Provenance differences were
minimal despite retention of the juvenile leaf form by the
Tasmanian plants throughout the study. The time taken for initiation of vegetative phase change by the Wilsons Prom. saplings increased with decreasing light availability, but the nodal
position of change on the main stem remained the same. Both
juvenile and adult leaves remained horizontal in low light conditions, but became vertical with high irradiance. Leaf dimensions changed with ontogenetic development, but were unaffected by light availability. Juvenile leaves retained a dorsiventral anatomy and adult Wilsons Prom. leaves retained an
isobilateral structure despite a tenfold difference in light availability. Stomatal density and distribution showed ontogenetic
and treatment differences. At all irradiances, juvenile leaves
produced the smallest stomata and adult leaves the largest
stomata. Amphistomy decreased with decreasing irradiance.
Detrended, correspondence analysis ordination highlighted
the structural changes influenced by ontogenetic development
and light availability. Adult leaves had characteristics similar
to the xeromorphic, sun-leaf type found in arid, high-light conditions. Although juvenile leaves had characteristics typical of
mesomorphic leaves, several structural features suggest that
these leaves are more sun-adapted than adult leaves.
components (Givnish 1988). Genetic adaptation to the light
environment prevailing in the native habitat results in sun-requiring or shade-tolerant species (Boardman 1977, Björkman
1981, Larcher 1995). At the individual level, leaves adapted to
different irradiances are found within the canopy. Adaptations
to high temperatures, dry air or restricted water supply are secondary effects of light availability.
The relationship between leaf form and environment has often been studied, but different species or populations are generally considered (Turesson 1922, de Soyza and Kincaid 1991,
Smith et al. 1998). At any stage in the development of a shoot,
leaves are morphologically and functionally dissimilar as a result of microenvironment and ontogenetic leaf form differences. This is particularly true of Eucalyptus globulus Labill.
ssp. globulus, which develops successive and distinctive juvenile, transitional and adult ontogenetic leaf forms (James
1998). Effects of light availability on the growth and vegetative phase change of Eucalyptus species are poorly described
in the scientific literature. Few studies document the effects of
light availability on eucalypt leaf morphology with respect to
vegetative phase change (Cameron 1970, Ashton and Turner
1979). It has been noted that juvenile leaves of Eucalyptus
species have the morphology and structure of leaves developed under shade conditions, whereas adult leaves form in the
high-light environment of the mature tree canopy and are considered to be sun-adapted (Cameron 1970, Ashton and Turner
1979). We have determined the effects of manipulated irradiances on the structure of juvenile and adult leaves, and the
growth of two Eucalyptus globulus ssp. globulus provenances.
Keywords: irradiance, leaf morphology, leaf anatomy, mesophyll, Myrtaceae, ontogeny, sun-shade leaves.
Materials and methods
Cultivation
Introduction
Light environment and interception of light strongly influence
plant growth and development. Whole-plant growth and competitive ability at different irradiances are dependent on photosynthetic rate and structure of individual leaves, canopy
geometry and dynamics, and biomass allocation among plant
Plants of two Eucalyptus globulus ssp. globulus provenances
were grown in 100, 50 or 10% sunlight for 9 months. A late
maturing provenance from St. Marys, Tasmania (Tasmanian
provenance: CSIRO forest research seedlot provenance 16474
sib. CL002) produced juvenile foliage throughout the experimental period. An early-maturing provenance from Wilsons
Promontory, Victoria (Wilsons Prom. provenance: 16399 sib.
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JAMES AND BELL
DFC 219) produced adult foliage within the first year of
growth.
Thirteen-week-old seedlings were transplanted to 1.7-m 3
pots containing freely draining soil. Seedlings were watered
twice daily to field capacity and fertilized with controlled-release nutrient pellets. One week after transplanting, the seedlings were placed outdoors at The University of Western Australia in three light treatments. Shading was achieved by placing seedlings in 2-m tall shade-houses covered with water- and
air-permeable acrylic shade nets. Ambient sunlight available
within the nominally 50 and 10% shade-houses, determined
with an integrating photometer (LI-188B, Li-Cor Inc., Lincoln, NE) with a quantum sensor (LI-190SB), was 48 and 3%
of full sunlight, respectively. Daily ambient temperatures,
measured by maximum–minimum thermometers, were similar for the three treatments over the experimental period. Differences in light quality between the treatments were not determined. However, light quality beneath mature Eucalyptus
canopies does not vary greatly from open locations because
the vertical adult leaf orientation allows a high proportion of
direct light to penetrate the canopy (Rokich and Bell 1995).
Growth analysis
Saplings were harvested over a 3-day period after 9 months of
treatment. Height, node number and basal diameter 2 cm
above the soil surface were determined for 12 Tasmanian and
14 Wilsons Prom. saplings. Internode length was calculated as
shoot height divided by node number. Numbers of axillary
branches and leaves were determined for each plant. Shoots
were separated into immature and fully expanded leaves,
axillary branches and the mainstem. Fully expanded leaves of
the Wilsons Prom. provenance were separated into juvenile
and petiolate (transitional and adult) leaf forms (James 1998).
Leaves were immediately placed in plastic bags and kept cool
for a maximum of 48 h. Areas of immature and fully expanded
leaves were measured with a leaf area meter (LI-3000, Li-Cor,
Inc.). The developmental timing of vegetative phase change of
each Wilsons Prom. sapling was recorded as the node on the
mainstem at which the first petiolate leaf developed.
Ratios of leaf weight to stem weight, stem height to stem
weight, and leaf area to stem height were calculated for each
sapling. Specific leaf area was calculated as the ratio of total
leaf area to dry weight for the juvenile and petiolate leaves.
For the Wilsons Prom. saplings, the ratio of petiolate leaf
weight to total leaf weight was calculated. The mean and standard error of the mean were calculated for each measured
characteristic for the Tasmanian and Wilsons Prom. saplings
within each light treatment. Multivariate analyses between
provenance and treatment and Fisher’s pairwise least significant difference were made with Minitab software (release
10.51, Minitab Inc., State College, PA).
Allometric relationships between plant components provide
a direct indication of dry matter allocation, and eliminate the
effects of size and ontogeny with chronological time (Hunt
1982, Shepherd and Sa-ardavat 1984, Cromer and Jarvis
1990). The allometric relationships between plant component
log-transformed dry weights, total leaf area and stem height
were analyzed by linear regression with SPSS software (release 7.0, SPSS Inc., Chicago, IL), allowing slopes and intercept parameters to vary according to the treatment or
provenance, or both. The initial model allowed different intercepts and slopes for all treatment by provenance combinations. Interaction and main effects were assessed sequentially
for statistical significance by standard F-tests, with non-significant terms being omitted and the model refitted until only
significant terms remained.
Leaf morphology and anatomy
Juvenile leaves of the late maturing Tasmanian provenance,
and juvenile, transitional and adult leaves of the early-maturing Wilsons Prom. provenance were collected from the outermost branches and classified based on overall shape and
petiole length (James 1998). An additional collection of transitional and adult leaves of Wilsons Prom. saplings in the 10%
light treatment was made after 21 months of treatment because
phase change was not complete at the 9-month harvest. Leaf
length, maximum width and petiole length were measured for
10 representative leaves (30 for transitional and adult leaves in
10% light), and the ratio of leaf length to maximum width was
calculated.
Pieces (1 cm 2) of leaf lamina between the margin and midvein at the leaf mid-length were removed from four representative leaves of each ontogenetic form and light treatment (12
for 10% sunlight transitional and adult leaves). Tissues were
fixed with 2.5% glutaraldehyde in 0.1 M phosphate buffer and
dehydrated in an alcohol series (Feder and O’Brien 1968).
Leaf tissues were embedded in glycol methacrylate and transversely sectioned at 3 µm thickness. Sections were stained
with periodic acid–Schiff’s reagent and counterstained with
toluidine blue (pH 4.4) to enhance cell wall and starch grain
visibility.
Leaf thickness was determined as the mean of 10 measurements along the leaf section. The number of palisade mesophyll cell layers and the total number of cell layers spanning
the leaf section were determined. Epidermal cell and cuticle
thickness, adaxial and abaxial palisade mesophyll and spongy
mesophyll thickness were measured. The lengths of five
adaxial and five abaxial palisade cells within the first palisade
layer beneath the epidermis were determined and the mean
value computed for each leaf.
Adaxial and abaxial stomatal density, and surface oil gland
density were determined for 10 representative leaves of each
ontogenetic form and treatment (20 for transitional and adult
leaves in 10% sunlight). An impression of 50 mm2 between
the margin and mid-vein at the leaf mid-length was created
with clear nail polish and viewed with the aid of a compound
light microscope (James and Bell 1995). Stomatal density per
leaf was determined as the mean of 10 0.06-mm 2 fields of
view. Oil gland density was determined from the same impressions with a 1.06-mm 2 field of view. Stomatal pore length was
determined as the mean length of 10 stomata.
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LIGHT AVAILABILITY AFFECTS EUCALYPT LEAF STRUCTURE
The mean and standard error of the mean were calculated
for each characteristic measured for the leaf forms in each
light treatment with Minitab software. Statistical comparisons
between the leaf forms, treatments and leaf surfaces were
made by one-way and multivariate analyses of variance and
Fisher’s pairwise least significant difference. Data were logtransformed and reanalyzed if the standard deviations were
found to be variable.
Mean values of leaf morphological, anatomical and epidermal characteristics were grouped for juvenile, transitional and
adult leaves, and partial detrended canonical correspondence
analysis (DCA) was completed with CANOCO software (version 3.11, Agricultural Mathematics Group, Wageningen, The
Netherlands). Values were range standardized. Ordination
axis values for each of the leaf forms and light treatments were
analyzed statistically by multivariate analysis of variance with
Minitab software.
Results
Growth analysis
Within each light treatment, Tasmanian and Wilsons Prom.
saplings had a similar initial height and number of leaves. After 9 months of treatment, saplings of both provenances grown
in full or 50% sunlight were significantly greater in height,
number of nodes, number of leaves and basal diameter than
saplings grown in 10% sunlight (Table 1). For both provenances, the shortest internodes were produced by saplings
grown in 10% sunlight (Table 1).
Significant treatment differences but no provenance differences were found for leaf area, and leaf, axillary branch and
mainstem dry weights of the saplings (Table 1). The number
of leaves, leaf area and component dry weights were greatest
in saplings in full sunlight and least for saplings in 10% sunlight. Wilsons Prom. saplings showed a significant decline in
total leaf weight, leaf number, leaf area and stem weight with
decreasing light availability (Table 1). In contrast, values for
these characteristics were not significantly different for Tasmanian saplings in the full and 50% sunlight treatments. The
two provenances produced similar numbers of axillary branches in full and 50% sunlight, but significantly fewer in 10%
sunlight (Table 1). Biomass of woody tissues of the two provenances was significantly reduced in the 10% sunlight treatment.
Among treatments, the leaf weight to stem weight ratio was
significantly greater for saplings grown in 10% sunlight (Table 1). When ontogenetic development was taken into consideration, the allometric relationship between stem and leaf
weight differed significantly between treatments (P < 0.01),
with the slope or allometric coefficient (k) being highest in
50% sunlight (k = 1.18), intermediate in 10% sunlight (k =
0.80), and lowest in full sunlight (k = 0.78). Saplings in 50%
sunlight preferentially allocated biomass to stems, whereas
saplings in the full and 10% sunlight treatments preferentially
allocated biomass to leaf production. Wilsons Prom. saplings
had a greater stem weight per unit leaf weight than Tasmanian
1009
saplings at high irradiances. The stem weight intercept for the
10% sunlight treatment was similar for the two provenances,
but the intercept value for Tasmanian saplings in the full and
50% sunlight treatments was 0.15 lower than that for the
Wilsons Prom. saplings.
For both provenances, the instantaneous ratio of stem height
to stem weight increased significantly from the full and 50%
sunlight treatments to the 10% sunlight treatment (Table 1),
suggesting that saplings in 10% sunlight increased in height at
the expense of increasing stem diameter. However, no treatment or provenance effect was found for the stem height to
stem dry weight allometric coefficient (k = 0.27). Wilsons
Prom. saplings were significantly shorter per unit stem weight
than Tasmanian saplings (P < 0.05).
The leaf area to stem height ratio increased with increasing
irradiance (Table 1). When ontogenetic development was
taken into consideration, the allometric coefficient for the relationship between leaf area and stem height was similar for
both provenances (k = 2.11). Saplings in full sunlight had the
greatest leaf area per stem height (P < 0.05).
The allometric coefficient for the relationship between leaf
area and leaf weight was constant for both provenances and
across treatments (k = 0.92, P < 0.01). However, saplings in
10% sunlight had a leaf area intercept 0.18 lower than saplings
in full and 50% sunlight (P < 0.05), indicating that saplings in
10% sunlight had greater specific leaf area (Table 1). The Tasmanian provenance had a 0.89 higher leaf area intercept than
the Wilsons Prom. provenance (P < 0.05), reflecting production of adult leaves by the Wilsons Prom. saplings.
In all treatments, Wilsons Prom. saplings were undergoing
vegetative phase change by the 9-month harvest. The chronological time before transitional leaves were produced increased with decreasing irradiance. At full and 50% sunlight,
transitional leaves were produced after 4 months, and saplings
grown in 10% sunlight were producing transitional leaves by
9 months. However, the mean and range of mainstem nodes at
which vegetative phase change was initiated were similar in
all treatments (Table 2). After 9 months, the ratio of petiolate
leaf to total leaf weight was lower in Wilsons Prom. saplings
in 50% and 10% sunlight than that for saplings in full sunlight
(Table 1).
Leaf morphology and anatomy
Leaf morphology and anatomy were dependent on ontogenetic leaf form and sunlight availability. In full sunlight, juvenile leaves of both provenances were inclined. Juvenile
leaves produced in 10% sunlight were horizontal and nonoverlapping as a result of stem and blade twisting. Adult
leaves were pendulous in full sunlight, but were horizontal in
10% sunlight. Leaves in 10% sunlight did not have starch
grains, whereas leaves in full and 50% sunlight had a high density of starch grains in the leaf mesophyll.
There was no consistent difference in light treatment effects
on leaf length or width between the ontogenetic leaf forms
(Figure 1A). Within a treatment, leaf width declined and the
ratio of leaf length to width increased significantly with
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JAMES AND BELL
Table 1. Growth and biomass characteristics of Tasmanian and Wilsons Prom. Eucalyptus globulus ssp. globulus saplings grown in 100, 50 and
10% sunlight for 9 months. Each value is the mean and standard error of the mean for 12 Tasmanian and 14 Wilsons Prom. individuals. Values
with the same letter are not significantly different at P < 0.05.
Biomass characteristics
Height (cm)
Tasmanian
Wilsons Prom.
Node number
Tasmanian
Wilsons Prom.
Internode length (cm)
Tasmanian
Wilsons Prom.
Basal diameter (mm)
Tasmanian
Wilsons Prom.
Fully expanded leaf number
Tasmanian
Wilsons Prom.
Total leaf number
Tasmanian
Wilsons Prom.
Fully expanded leaf weight (g)
Tasmanian
Wilsons Prom.
Total leaf weight (g)
Tasmanian
Wilsons Prom.
Petiolate leaf weight:total leaf weight
Tasmanian
Wilsons Prom.
Fully expanded leaf area (m 2)
Tasmanian
Wilsons Prom.
Total leaf area (m 2)
Tasmanian
Wilsons Prom.
Axillary branch number
Tasmanian
Wilsons Prom.
Axillary branch weight (g)
Tasmanian
Wilsons Prom.
Mainstem weight (g)
Tasmanian
Wilsons Prom.
Specific leaf area (cm 2 g –1)
Tasmanian juvenile
Wilsons Prom. juvenile
Wilsons Prom. petiolate
Leaf weight:stem weight (g g –1)
Tasmanian
Wilsons Prom.
Stem height:weight (cm g –1)
Tasmanian
Wilsons Prom.
Leaf area:stem height (cm 2 cm –1)
Tasmanian
Wilsons Prom.
Light availability (%)
100
50
10
189.5 ± 23.4 b
199.8 ± 18.0 b
209.0 ± 14.3 b
176.4 ± 13.5 b
116.2 ± 13.4 a
90.9 ± 7.6 a
39.0 ± 5.3 c
37.1 ± 1.3 bc
40.0 ± 1.0 c
35.0 ± 0.6 bc
30.2 ± 2.1 ab
27.3 ± 2.0 a
4.8 ± 0.3 b
5.3 ± 0.4 b
5.2 ± 0.2 b
5.0 ± 0.4 b
3.8 ± 0.3 a
3.3 ± 0.2 a
21.4 ± 3.7 c
22.1 ± 2.1 c
18.2 ± 1.2 bc
15.1 ± 1.2 b
7.9 ± 1.4 a
6.9 ± 0.5 a
663.7 ± 190.7 b
659.3 ± 134.7 b
396.5 ± 61.6 ab
244.9 ± 42.0 a
143.0 ± 24.0 a
113.1 ± 26.2 a
1139.3 ± 435.0 c
855.6 ± 175.3 b
560.2 ± 93.1 ab
308.4 ± 60.5 a
217.2 ± 28.9 a
152.1 ± 34.5 a
110.5 ± 31.3 b
190.3 ± 36.6 c
87.1 ± 15.7 b
78.6 ± 22.9 b
15.9 ± 3.6 a
10.9 ± 2.1 a
123.3 ± 37.1 cd
201.9 ± 39.2 d
91.9 ± 16.6 bc
82.7 ± 24.3 bc
18.1 ± 4.4 ab
11.7 ± 2.2 a
–
0.53 ± 0.09 a
–
0.40 ± 0.13 a
–
0.29 ± 0.09 a
1.88 ± 0.85 b
2.01 ± 0.46 b
1.36 ± 0.29 ab
0.89 ± 0.22 ab
0.41 ± 0.096 a
0.24 ± 0.047 a
2.05 ± 0.95 b
2.09 ± 0.47 b
1.43 ± 0.31 ab
0.92 ± 0.23 ab
0.43 ± 0.10 a
0.26 ± 0.051 a
153.5 ± 44.5 b
230.0 ± 33.1 c
102.0 ± 17.5 ab
93.1 ± 17.4 ab
37.3 ± 7.6 a
35.0 ± 10.4 a
73.0 ± 37.9 bc
81.6 ± 22.4 c
30.4 ± 5.9 ab
23.4 ± 7.2 ab
3.8 ± 0.9 a
2.3 ± 0.6 a
136.6 ± 53.8 cd
149.7 ± 44.2 d
100.1 ± 16.2 bcd
65.7 ± 14.0 abc
12.7 ± 3.9 ab
7.6 ± 1.7 a
143.8 ± 26.4 abc
125.7 ± 5.8 abc
95.4 ± 9.2 a
154.3 ± 16.0 c
144.6 ± 11.9 bc
99.8 ± 11.3 ab
260.4 ± 19.3 d
231.4 ± 23.8 d
220.3 ± 23.0 d
0.73 ± 0.09 ab
0.96 ± 0.08 b
0.70 ± 0.04 a
0.87 ± 0.05 b
1.18 ± 0.10 c
1.25 ± 0.13 c
1.48 ± 0.30 a
1.13 ± 0.19 a
1.78 ± 0.23 a
2.51 ± 0.47 a
9.08 ± 1.62 b
10.86 ± 1.56 b
93.4 ± 33.4 bc
101.0 ± 14.7 c
65.1 ± 10.5 abc
50.3 ± 9.1 ab
35.7 ± 4.5 a
27.1 ± 3.3 a
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Table 2. Mainstem node of vegetative phase change from juvenile to
transitional leaf form for Wilsons Prom. Eucalyptus globulus ssp.
globulus saplings grown in different irradiances. Mean values are
given with standard error of the mean.
Light availability (%)
100
50
10
Mainstem node of change (weeks)
Mean
Minimum
Maximum
25.9 ± 1.4
24.8 ± 2.0
24.8 ± 2.6
16
15
15
34
36
32
ontogenetic development from the juvenile to adult leaf form
(Figure 1B). Leaf area increased as irradiance decreased from
full sunlight to 50% sunlight, but declined with a further reduction in light availability (Figure 1C). Juvenile Wilsons
Prom. leaves, however, increased in area with decreasing
irradiance. Petiole length increased significantly with ontogenetic development from the juvenile to adult leaf form (Figure 1D). Tasmanian juvenile leaves lacked a petiole irrespective of light treatment. Petiole length of transitional and adult
leaves decreased with decreasing light availability, reflecting
the more horizontal orientation of these leaves under shaded
conditions.
Within each light treatment, juvenile leaves of both provenances were dorsiventral in structure, and adult leaves of
Wilsons Prom. were isobilateral. Transitional leaves typically
had an isobilateral structure, but with a greater volume of airspace within the abaxial palisade mesophyll. All leaf forms
had increased bundle-sheath and vascular development with
increasing light availability.
Each leaf form increased in thickness with ontogenetic development and increasing light availability (Figure 2A) as a
result of increases in mesophyll and palisade cell number and
thickness (Figure 2B). Juvenile leaves of both provenances
had two adaxial palisade cell layers that were reduced to a single layer under low-light conditions. Three palisade layers on
the adaxial surface of adult leaves of Wilsons Prom. were reduced to less than two layers in low light.
The ratio of palisade to spongy mesophyll thickness declined significantly with decreasing irradiance from full sun to
10% sunlight for both transitional and adult leaves of Wilsons
Prom. (Figure 2C). In contrast, juvenile leaves retained the
same ratio of palisade to spongy mesophyll in all treatments.
Adaxial and abaxial palisade mesophyll cell length declined
significantly with light availability for all ontogenetic leaf
forms (Figure 2D). Within each light treatment, adaxial palisade mesophyll cells were significantly longer than abaxial
palisade mesophyll cells (Figure 2D).
Cuticle thickness increased with ontogenetic development
(Figure 3A). Adult leaves had the thickest cuticle in each light
treatment. With the exception of the juvenile leaf form, cuticle
thickness declined significantly with decreasing irradiance
(Figure 3A). Epidermal thickness was similar among the leaf
forms, treatments and leaf surfaces (Figure 3B). The epidermis of adult leaves produced in 10% sunlight was significantly
Figure 1. Leaf dimensions of juvenile Tasmanian (Jt ) and juvenile
(JW), transitional (T), and adult (A) Wilsons Prom. Eucalyptus
globulus ssp. globulus leaves developed in 100 (full), 50 and 10%
sunlight. (A) Leaf length (solid bars) and maximum width (open
bars), (B) ratio of leaf length to width, (C) leaf area, and (D) petiole
length. Bars are the mean, and error bars the standard error of the
mean. Bars with the same letter are not significantly different at P =
0.05.
thicker than the epidermis of other leaf forms in all treatments.
Adaxial stomatal density was significantly lower than abaxial stomatal density for all leaf forms in all light treatments
(Figure 4A). With decreasing irradiance, adaxial stomatal
density of transitional and adult leaf forms declined, whereas
abaxial stomatal density increased significantly. In contrast,
abaxial stomatal density of juvenile leaves declined with decreasing irradiance. Total stomatal density per unit juvenile
leaf area declined significantly with decreasing irradiance
from full sunlight to 10% sunlight (Figure 4B). Total stomatal
density of transitional leaves was not influenced by irradiance,
and adult leaves had a greater stomatal density in 50% sunlight
than in the other light treatments. Leaves became more
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JAMES AND BELL
Figure 3. (A) Adaxial (solid bars) and (B) abaxial (open bars) cuticle
and epidermal thickness of juvenile Tasmanian (Jt ) and juvenile (JW),
transitional (T), and adult (A) Wilsons Prom. Eucalyptus globulus
ssp. globulus leaves developed in 100, 50 and 10% sunlight. Bars are
the mean, and error bars the standard error of the mean. Bars with the
same letter are not significantly different at P = 0.05.
Figure 2. Leaf thickness and palisade characteristics of juvenile
Tasmanian (Jt ) and juvenile (JW), transitional (T), and adult (A)
Wilsons Prom. Eucalyptus globulus ssp. globulus leaves developed in
100, 50 and 10% sunlight. (A) Leaf thickness, (B) total number of
mesophyll cell layers (solid bars) and adaxial palisade cell layers
(open bars), (C) ratio of palisade to spongy mesophyll thickness, and
(D) adaxial (solid bars) and abaxial (open bars) cell length of the first
palisade cell layer. Bars are the mean, and error bars the standard error
of the mean. Bars with the same letter are not significantly different at
P = 0.05.
hypostomatous with decreasing light availability. With the exception of the Tasmanian juvenile leaf form, which produced
no adaxial stomata, the ratio of adaxial to total stomatal density declined with decreasing irradiance (Figure 4C). In all
treatments, adult leaves produced the largest stomata and juvenile leaves had the smallest stomata (Figure 4D). Adaxial and
abaxial stomatal pore lengths were greatest for leaves produced in full sunlight, and least for leaves produced in 10%
sunlight.
Adaxial oil gland density was unaffected by light treatment
or ontogenetic leaf form (Figure 5). Abaxial oil gland density,
however, was significantly greater for leaves developed in
10% sunlight than for leaves developed in full or 50% sunlight.
The DCA ordination of mean values of all leaf characteristics highlighted the gradual structural changes in leaves that
occurred in response to ontogenetic development and
irradiance (Figure 6). Eigenvalues indicated that most of the
variability was contained within axes one (0.31) and two
(0.06). Petiole length, cuticle thickness, abaxial oil gland density, palisade characteristics and stomatal density were the
characteristics most strongly distinguishing the leaf forms
within each light treatment.
Discussion
Growth, architecture and leaf structure of Tasmanian and
Wilsons Prom. Eucalyptus globulus ssp. globulus saplings
were strongly influenced by light availability. The rate of vegetative phase change, however, was not affected by irradiance.
The two provenances had a similar biomass allocation to
stems and leaves during growth, even though the late-maturing Tasmanian saplings have a faster absolute growth rate
(James 1998). Saplings of both provenances maintained
growth throughout the experimental period in all light treatments, with maximum growth and biomass production occurring in full sunlight (cf. Rao and Singh 1989). Plant components of most eucalypts decline in dry weight with decreasing
irradiance (Brittain and Cameron 1973, Ashton and Turner
1979, Withers 1979, Bowman and Kirkpatrick 1986b, Rao
and Singh 1989, Stoneman and Dell 1993), and the same was
found for the two provenances studied here. An increased allo-
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Figure 5. Adaxial (closed bars) and abaxial (open bars) oil gland density of juvenile Tasmanian (Jt ) and juvenile (JW), transitional (T), and
adult (A) Wilsons Prom. Eucalyptus globulus ssp. globulus leaves developed in 100, 50 and 10% sunlight. Bars are the mean, and error
bars the standard error of the mean. Bars with the same letter are not
significantly different at P = 0.05.
Figure 4. Stomatal characteristics of juvenile Tasmanian (Jt ) and juvenile (JW), transitional (T), and adult (A) Wilsons Prom. Eucalyptus
globulus ssp. globulus leaves developed in 100, 50 and 10% sunlight.
(A) Adaxial (solid bars) and abaxial (open bars) stomatal density, (B)
total stomatal density per unit leaf area, (C) ratio of adaxial to total
stomatal density, and (D) adaxial (solid bars) and abaxial (open bars)
stomatal pore length. Bars are the mean, and error bars the standard
error of the mean. Bars with the same letter are not significantly different at P = 0.05.
cation of biomass to leaves at the expense of non-photosynthetic stems and roots in low light maximizes light interception and growth rates (Björkman 1981, Lambers and Poorter
1992). For many Eucalyptus species, irradiance has little effect on allocation of dry matter among leaves, stems and roots
(Doley 1978, Küppers et al. 1988, Rao and Singh 1989,
Fownes and Harrington 1992, Stoneman and Dell 1993). Instantaneous measurements of E. globulus characteristics indicated a greater allocation of biomass to leaves than stems by
seedlings in 10% sunlight. However, when ontogenetic effects
were taken into account, saplings in 50% sunlight allocated
more biomass to leaves than to stems, and saplings in full and
10% sunlight allocated more biomass to stems than to leaves.
Saplings in full sunlight apparently had an adequate carbon resource that could be allocated to structural components, such
as basal diameter and number of branches, whereas saplings in
50% sunlight preferentially invested available carbon into
leaves for increased sunlight capture. Saplings in 10% sunlight allocated biomass preferentially to stems, but allocated
more biomass to leaves than full sunlight saplings. The allocation pattern in saplings in 10% sunlight reflects their high specific leaf area and the requirement for a structural component
for maximal leaf display and light capture in low-light conditions. Similar allocation of resources to height growth by
low-light saplings and to stem diameter and branch production
by high-light saplings has been found for other Eucalyptus
species (Cameron 1970, Ashton 1975, Doley 1978, Ashton
and Turner 1979, Withers 1979, Bowman and Kirkpatrick
1986a, Rao and Singh 1989).
Leaf size increased with decreasing irradiance from full
sunlight to 50% sunlight, and then declined with further reductions in light availability. Similar trends have been found for
individual leaf areas and total plant leaf area (Cameron 1970,
Ashton and Turner 1979, Withers 1979, Stoneman and Dell
1993) for a range of eucalypt species. A decrease in leaf size in
full sunlight reduces leaf temperature, potential water loss and
damage to leaf photosystems. The increased leaf size in 50%
sunlight would increase light interception. The cost of producing a larger leaf in 10% sunlight may outweigh the benefit of
increased light capture and carbon gain. Specific leaf area increased for each ontogenetic leaf form with decreasing light
availability, as shown for other eucalypt species (Doley 1978,
Ashton and Turner 1979, Withers 1979, Stoneman and Dell
1993). Greater specific leaf area of leaves in low light increases the potential photosynthetic leaf area relative to leaf
biomass.
Heteroblastic development and vegetative phase change occur even under constant environmental conditions (Wareing
and Phillips 1981). Factors that retard growth and reduce car-
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1014
JAMES AND BELL
Figure 6. Ordination of mean leaf characteristic values for juvenile
Tasmanian (Jt ) and juvenile (JW), transitional (T), and adult (A) Wilsons
Prom. Eucalyptus globulus ssp.
globulus leaves in 100, 50, and 10%
sunlight. Characteristics influencing
the distribution of the leaf types in the
ordination hyperspace are indicated.
Lines join the Wilsons Prom.
ontogenetic leaf forms. The influence
of light treatment and ontogeny on the
separation of leaf forms is indicated.
bohydrate concentrations, such as low light, can prolong the
juvenile phase (Hackett 1985, Poethig 1990). The duration of
the juvenile leaf form of Eucalyptus fastigata H. Deane &
Maiden (Cameron 1970) and E. regnans F.J. Muell. (Ashton
and Turner 1979) seedlings increased with decreasing sunlight. We observed that the change from the juvenile to the
transitional and adult foliage was strongly inherent, but the
chronological time taken was similarly delayed by shading.
However, light availability had no effect on the number of
nodes acquired before phase change.
Leaf structure is strongly influenced by light availability
during development (see Boardman 1977, Björkman 1981,
Lichtenthaler 1985, Abrams and Kubiske 1990). Leaf thickness increased with both ontogenetic development and light
availability, corresponding to an increase in palisade mesophyll cell length and number of layers, as reported by others
(Boardman 1977, Björkman 1981, Hoflacher and Bauer 1982,
Lichtenthaler 1985, Dengler 1994). Extensive palisade mesophyll development of juvenile and adult leaves in high light increases Ames /A (mesophyll cell surface area per unit leaf
surface area) and photosynthetic capacity while limiting the
effect on transpirational water loss (Nobel et al. 1975,
Björkman 1981, Smith and Longstreth 1994, Smith et al.
1997, James et al. 1999). The ratio of the thickness of palisade
to spongy mesophyll gives an indication of light exposure during the development of a leaf (Lichtenthaler 1985). This ratio
is high in sun leaves with extensive palisade development
(1.5), and decreases with increasing shade (< 0.7). The ratio of
palisade to spongy mesophyll declined with decreasing
irradiance for the transitional and adult leaves of Wilsons
Prom. saplings as a result of reduced palisade mesophyll development and increased spongy mesophyll differentiation.
The lack of change in the ratio for juvenile leaves of both provenances may indicate a reduced structural plasticity of these
leaves compared with adult leaves.
Stomatal frequency is usually higher in full sunlight plants
than in shade plants (Boardman 1977, Björkman 1981, Ticha
1982, Lichtenthaler 1985, Abrams and Kubiske 1990, Willmer and Fricker 1996). Only juvenile leaves showed an increase in stomatal frequency with increasing irradiance. Hypostomy increased with decreasing irradiance for all ontogenetic leaf forms. It has often been reported that hypostomy
is favored by low light (Björkman 1981, Jones 1985, Mott and
Michaelson 1991), whereas amphistomatous species are more
successful in high-light habitats (Mott et al. 1982, Smith et al.
1998). The presence of stomata on the adaxial leaf surface improves diffusion characteristics, particularly for thicker leaves
(Beerling and Kelly 1996). Increased hypostomy in low
irradiance may be related to reduced leaf thickness and the reduced light potential for CO2 utilization. Smaller guard cells
have been associated with plants from xeric habitats (Lichtenthaler 1985, Abrams and Kubiske 1990, Willmer and
Fricker 1996). Other studies have reported larger guard cells
in sun leaves than in shade leaves, or no significant trends in
guard-cell length between sun and shade leaves (Boardman
1977, Abrams and Kubiske 1990). In our study, stomatal pore
length decreased with decreasing irradiance for Wilsons
Prom. transitional and adult leaves. Stomata of Eucalyptus
fastigata leaves also decline in size with decreasing irradiance
(Cameron 1970). Larger stomata in high light may indicate
TREE PHYSIOLOGY VOLUME 20, 2000
LIGHT AVAILABILITY AFFECTS EUCALYPT LEAF STRUCTURE
that Eucalyptus globulus ssp. globulus leaves, especially adult
leaves, rely on transpirational water loss for leaf cooling in
high light (cf. Ducrey 1992). The numerous small stomata of
juvenile leaves would allow greater potential water loss under
conditions of high water availability than the adult leaf form
which, in turn, would maximize nutrient uptake. The absence
of an effect of irradiance on stomatal pore size of juvenile
leaves further suggests limited structural plasticity.
Reduced density of starch grains, decreased cuticle thickness, and a greater number of oil glands in the low-light leaves
1015
of Eucalyptus globulus ssp. globulus suggests an altered leaf
metabolism in low-light conditions (Lichtenthaler 1985,
Thompson et al. 1992, Larcher 1995). The cuticle of Wilsons
Prom. leaves in full sunlight was 2.5 times thicker than the cuticle of leaves in 10% sunlight, as was also found for Eucalyptus regnans (Ashton and Turner 1979). Increased cuticle
thickness in high light would assist in reducing water loss and
protecting the leaves from ultraviolet light penetration. Epidermal cells of adult leaves developed in 10% sunlight were
significantly thicker than epidermal cells developed in high
Table 3. Sun, shade and xeromorphic morphological and anatomical leaf characteristics compiled from several studies (Bauer and Bauer 1980,
Givnish 1988, Hart 1988, Bolhár-Nordenkampf and Draxler 1993, Larcher 1995). An indication has been given as to whether the juvenile Eucalyptus globulus ssp. globulus leaves conform to a shade leaf form, and the adult leaves conform to a sun or xeromorphic leaf form based on data
presented here and in James (1998) and James and Bell (2000).
Characteristic
Leaf orientation
Phyllotaxis
Leaf area index of plant
Leaf area
Dry matter
Water content (by mass)
Leaf mass:leaf area
Leaf thickness
Stomatal frequency
Stomatal size
Sunken stomata
Sclerification
Number of lateral veins
Bundle-sheath extensions
Intercellular airspace
Internal surface area (Ames /A)
Thickness of mesophyll parenchyma
Thickness of palisade mesophyll
Palisade cell length
Palisade/spongy parenchyma ratio
Thickness of epidermal outer wall and cuticle
Lens-shaped epidermal cells
Waxiness
Light-saturated photosynthetic rate
Light-limited photosynthetic rate
Photosynthetic compensation point
Light saturation for photosynthesis
Dark respiration
Starch content
N, Rubisco and soluble protein content (by mass)
Chlorophyll a/b ratio
Chlorophyll/xanthophyll ratio
1
2
3
4
5
High light
Sun leaves
Low light
Shade leaves
Xeromorphic
leaves
Adult
Juvenile
Adult
Vertical
Spiral
High-low
–2
+
–
+
+
+
–
Horizontal
Distichous
Low
–
–
+
–
–
–
+
Vertical
+
–
+
–
+
+
+
+
+
+
None
+
+
–
+
+
+
+
+
+
–
–
+
–
+
–
–
–
–
–
–
Rare
–
–
+
–
–
–
–
–
–
+
High?
Yes
+ (Succulent)
+
+
+
–/+
+/–
+
+
+
–
+
+
+
–
+
+
None?
+
+
–?
+?
+?
+?
Conform?
Yes
Yes
No 1
No
No
Yes
Yes
No
No
Both sunken 3
Yes
Yes 4
Yes
Yes
Yes
Yes
Yes
No/yes 5
Yes
Yes
No
No
Yes
Yes?
Yes?
Yes?
Yes?
No
No?
No
No
Not measured for the provenances studied here, but provenances of Eucalyptus nitens (Deane & Maiden) Maiden with a juvenile-persistent leaf
form have been reported to have a greater leaf area index than early-maturing provenances with a canopy of leaves of the adult leaf type
(Turnbull et al. 1988, Beadle et al. 1989). Leaf area to stem height ratio was also greater for late maturing Tasmanian saplings than for early maturing Wilsons Prom. saplings (James 1998).
Abbreviations: + indicates an increase, high rates or large amounts; – indicates a decrease, low rates or small amounts.
Stomata are over-arched by extensions of the cuticle and slightly sunken.
According to Ito and Suzaki (1990).
Adult leaves have shorter adaxial palisade cells than juvenile leaves, which conforms to the xeromorphic leaf type, but not to the sun leaf type.
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1016
JAMES AND BELL
light. Increased epidermal thickness may assist in the capture
of diffuse light, with the abaxial epidermis assisting in the internal reflection of light (James 1998).
Many of the observed leaf structural differences between
sun and shade leaves were consistent with differences between
xeric and mesic leaves (Abrams et al. 1990, Bolhár-Nordenkampf and Draxler 1993, Rundel and Gibson 1996). Leaf
characteristics of xeromorphic species are a result of enhanced
radiation loads, with high irradiance resulting in greater evaporative demand and desiccation stress. Juvenile Eucalyptus
leaves generally have shade leaf morphology and anatomy,
whereas adult leaves have sun leaf characteristics (see Table 3;
Johnson 1926, Cameron 1970, Ito and Suzaki 1990, BolhárNordenkampf and Draxler 1993). Adult Eucalyptus globulus
ssp. globulus leaves exhibited many characteristics typical of
xeromorphic sun leaves found in arid, high-light conditions
(Table 3). Juvenile leaves had some characteristics typical of
mesomorphic shade leaves. However, E. globulus leaves did
not conform exactly to the sun xeromorphic and shade
mesomorphic leaf types (Table 3). One discrepancy arising
from the assumption that juvenile leaves are of the shade-leaf
form and adult leaves are of sun-leaf form is that both
E. globulus leaf forms develop in full sunlight within the canopy, and the species requires fire, or an open canopy, for regeneration (Kirkpatrick 1975, Stoneman 1994). This is also
true for heteroblastic Eucalyptus fastigata (Cameron 1970)
and Eucalyptus regnans (Ashton and Turner 1979). Compared
with juvenile leaves of Eucalyptus globulus ssp. globulus,
adult leaves have a significantly greater Ames /A and Vmes /V
(mesophyll volume per unit leaf volume) (James et al. 1999), a
greater photosynthetic capacity per unit leaf area, and a similar
leaf conductance (James 1998). These results indicate that
adult leaves have a greater water-use efficiency than juvenile
leaves (see Nobel 1980). The vertical leaf orientation of adult
leaves further assists in water conservation by reducing radiation load during summer. Furthermore, adult E. globulus
leaves have greater desiccation tolerance than juvenile leaves
(Ito and Suzaki 1990). The thinner, larger and horizontal juvenile leaves are advantageous in increasing light interception,
carbon accumulation, and growth of saplings. Juvenile leaves
have a greater total chlorophyll content per unit leaf volume
and ratio of chlorophyll a/b than adult leaves (James et al.
1999), indicating that juvenile leaves may be more
sun-adapted than adult leaves.
In conclusion, the structure of the ontogenetic leaf forms of
the Tasmanian and Wilsons Prom. provenances is influenced
by light availability. The structure of the juvenile leaf form
was altered less by a reduction in light availability than that of
the adult leaf form. Although this might indicate that the juvenile leaf is structurally adapted to shaded conditions, the juvenile leaf is able to tolerate high-light conditions. However, the
distribution and orientation of leaves within the juvenile leaf
canopy may result in most leaves receiving an irradiance below that required to saturate photosynthesis (Wong and Dunin
1987, Honeysett et al. 1992). Juvenile foliage would promote
growth and establishment in favorable conditions, such as the
greater light, nutrient and water availabilities after fire. Shade
intolerance of adult leaves may result from their greater vertical leaf orientation and reduced light interception (James and
Bell 2000). We conclude that the adult leaf form has a high
plasticity, and can persist in heavily shaded conditions by adjusting leaf structure and orientation to compensate for ambient light conditions.
Acknowledgments
This research was supported by an Australian Postgraduate Award
(SAJ). The authors thank Professor Ian James for his statistical advice
and Mr. Steven Mole for technical assistance.
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