Functional
E C O ~ O1989,
~
3, 53-62
Canopy organization and foliage photosynthetic
capacity in a broad-leaved evergreen montane
forest
D . Y . HOLLINGER
Forest Research Institute, New Zealand Ministry
of Forestry, PO Box 31-01I , Christchurch, New
Zealand
Abstract. The spatial and physical characteristics
of foliage varied systematically with canopy
height in a broad-leaved evergreen forest of
Nothofagus solandri var. clifforfioides (H0ok.f.)
Poole (mountain beech) in the Craigieburn Range,
South Island, New Zealand. Leaf inclination angle,
leaf weight per unit area, leaf nitrogen concentration, leaf photosynthetic capacity and leaf reflectance of photosynthetically active radiation all
decreased with depth in the canopy. These
changes will result in a more uniform distribution
of photosynthetically active radiation through the
canopy and a greater canopy carbon gain than
possible in canopies composed of randomly oriented leaves with constant physical properties.
The mean leaf area index of the Nothofagus
solandri var. cliffortioides foliage was 6.7 and
mean branch silhouette area index was 1.4. Mistletoe (Alepisflavida [Hook.f.] Tiegh) was present in
the canopy and had a leaf area index of 0.14, and a
stem silhouette area index of 0.02. Total beech and
mistletoe foliage biomass was 1183 and 36g m-2
respectively and total beech and mistletoe foliage
nitrogen mass was 12.3 and 0.37g m-'.
Key-words Leaf orientation, leaf area ~ n d e x ,leaf nitrogen, Nothofagus, photosynthetic capacity, mistletoe
Introduction
How are the canopies of trees and other plants
organized? The null hypothesis is that there is no
organization; that canopies consist of uniform
leaves randomly displayed in angle and orientation. Although many researchers implicitly
reject this hypothesis, the null hypothesis has not
been rigorously tested in broadleaf trees. Instead,
in many simulation models, physical or physiological properties are constant but leaf angles and
orientation follow some a priori distribution such
as that on the surface of a sphere.
A third hypothesis is that plant canopies are in
some way optimal. Many researchers have considered how canopies may display foliage to
maximize space filling, light interception, or
photosynthetic carbon gain (e.g. Monsi & Saeki,
1953; Verhaggen, Wilson & Britten, 1963; de Wit,
1965; Duncan, 1971; Horn, 1971; Fisher & Honda,
1979; Miller & Stoner, 1979; Oker-Blom & Kellomaki, 1982; Oker-Blom, 1984). These analyses are
hindered by the enormous complexity of calculating the canopy radiation field (Ross, 1981) and
the unknown significance of the simplifying
assumptions. In canopies composed of leaves with
constant physical properties, photosynthetic gain
is maximized when all leaves are receiving an
identical photon flux (Verhaggen et al., 1963).
Thus carbon assimilation by a canopy is increased
by characteristics which lead to a uniform light
distribution through the canopy by enhancing
light penetration at the top of the canopy and
increasing interception at lower levels. Examples
include vertically orientated leaves at the top of
dense canopies with horizontal leaves lower down
(Duncan, 1971) and small leaves at the top of
multilayered canopies (Horn. 1971; Oker-Blom,
1984). Similarly. other analyses have investigated
how nitrogen, a resource known to be directly
related to leaf photosynthetic capacity (e.g. Field &
Mooney, 1986). might be allocated amongst foliage
in different microsites to maximize canopy carbon
gain (Field, 1983: Hirose & Werger. 1987). Results
from Field (1983) suggest that canopy carbon gain
is increased when greater amounts of nitrogen are
allocated to leaves in brighter microsites.
Together, these studies suggest that canopy carbon
gain of an individual plant will be increased if leaf
spatial and physical properties vary through the
canopy so that (1) light will be more uniformly
intercepted through the canopy than would be
expected with a random arrangement of foliage
and (2) leaf nitrogen will be continuously apportioned with the greatest amount in the brightest
canopy sites (i.e, the top).
54
A final alternative considers the competitive
D. Y. Hollinger environment of plants, and suggests that the
canopy architecture of a plant must represent an
evolutionarily stable strategy (ESS) according to
the criteria of Maynard Smith (1976). To be an ESS
there must exist no other alternative architecture
that increases fitness over the common architecture. A tree architecture representing an ESS, for
example, may not maximize light interception or
carbon gain in isolation but will (assuming these
are related to fitness) i n the competitive forest
environment. It is unlikely that Duncan's optimum architecture of vertical leaves at the top of a
canopy and horizontal leaves at the bottom is
evolutionarily stable (Duncan, 1971). A competitor could arrange its foliage more horizontally high
in the canopy and increase its light interception
and carbon gain to the detriment of a n adjacent
individual with Duncan's architecture.
This study considers these hypotheses concerning canopy organization with reference to the
architecture of undisturbed, monospecific Nothofagus solandri var. cliffortioides (H0ok.f.) Poole
forest, although data from other forest types are
also discussed. The Nothofagus solandri var, cliffortioides system is suited to investigations on
whether a canopy might be organized to increase
carbon gain because the crown of each tree generally extends from the top to the bottom of the
canopy (important as any trade-off at one level can
be recovered at a lower one) and because the
canopy is monospecific; there being a high probability that neighbouring trees will be related
(important in any inclusive fitness arguments).
Data on the size, location, and optical properties
of leaves, and orientation of leaves and stems in a
forest canopy are also critical prerequisites in
efforts to model the canopy radiation regime or
carbon gain. Data presented here may cause
modellers to question some of the assumptions
they build into their models and provide a starting
point for further modelling efforts of our own to
assess the consequences of canopy organization on
carbon gain and fitness in N. solandri var. cliffortioides.
Materials and methods
Components of the canopy architecture were
measured in a stand of monospecific New Zealand
mountain beech (Nothofagus solandri var. cliffortioides [Hook.f.] Poole) growing on a level site at
an elevation of 900m in the Craigieburn Range
(Lat. 43O08'S, Long. 171°41'E), South Island, New
Zealand. Basal area of the stand was approximately 72mZ ha-' and trees were relatively even
aged, most being 70-90 years old. Canopy height
ranged between 15 and 17m.
Mean annual rainfall at this montane maritime
site is approximately 1450mm. and the mean
annual air temperature (1964-1980) is 8.0°C
(McCracken, 1980). Daytime temperatures rarely
exceed 25°C or remain below zero. Frosts are
common throughout the year, with the average
frost-free period at this site being 41 days.
Mountain beech retains much of its foliage into a
second year. Foliage loss occurs gradually during
the second summer after budbreak (Wardle, 1970).
The canopy was sampled in mid-March (1987)
after the current foliage had fully expanded and
much of the previous season's growth had been
lost.
Samples of foliage for determining the leaf area
distribution were obtained from 18 randomly
located square columns (0-5m on a side) that
extended from the ground to the top of the canopy
within the 42 m2 confines of a 21 m tall scaffolding
tower. Areas where such a vertical column would
meet a tower walkway or ladder were not sampled.
Columns were delineated by stretching four nylon
cords from a frame fixed at the top of the tower to
one located just above ground level. All of the
foliage and the branches with a diameter <I cm
within the column were removed in l m increments from the ground up by hand clipping, giving
(with a maximum tree height of 17m) 17 samples,
each 0.25m3 volume, for each column. About
one-half of the sample volumes did not contain
foliage. Leaf sub-samples (approximately 100
leaves) were taken from each sample for nitrogen
analysis and for area and weight determinations.
These sub-samples were sealed in plastic bags and
kept cool until the area determinations were made
(within 3 h of sampling). The area of the fresh
foliage and twig samples was determined with a
video leaf-area meter (model AMS-Basic, Delta-T
Devices, Cambridge, England). Nitrogen concentrations were determined by automated colorimetric analysis of Kjeldahl digests of ground (20
mesh) leaf material. Accuracy of the digestions
and system were checked by analysis of standard
foliage (Pinus radiata D. Don needles, batch FRI
2976).
Harvested twigs were dried at 70°C for 24 h in a
forced draft oven, leaves were separated from
stems, redried and then weighed. Leaf areas for
each sample were calculated based on the arealdry
weight relationship of each fresh sub-sample and
the total leaf dry weight of the associated sample.
55
Canopy
organization
The projected area of branches was measured in
eight of the sample columns. For branches and
twigs with diameters larger than l c m in each
sample volume, measurements were made of
branch length and diameter. For twigs with
diameters < I cm, projected area was estimated
from the area to weight ratio of a bulked twig
sub-sample and the dry weight of twigs in each
increment.
Leaf inclination angle from the horizontal and
azimuth angle were measured with an inclinometer and compass at the top of the canopy
(15-16m), mid-canopy (11-12m) and at the
bottom of the canopy (7-8m). All the leaves on a
number of randomly selected twigs were
measured, giving a total of approximately 175
leaves for each canopy level. N. solandri var.
cliffortioides leaves are predominantly planar and
few problems were encountered with the inclinometer measurements. The azimuth data were
averaged according to Batshelet (1981).
Photosynthetic measurements were made on
mature foliage in the spring prior to growth of new
foliage with the system described by Schulze et al.
(1982). Each twig sample was illuminated with a
photosynthetically active photon flux density
l
s-' supplied by a
(PFD) of 1000-1500 ~ m o mP2
400-watt metal arc lamp. Projected leaf areas were
measured with a video leaf area meter (model
AMS-Basic, Delta-T Devices, Cambridge,
England).
Reflectance and transmittance characteristics
were measured for seven leaves randomly selected
from each of the three canopy levels in midsummer 1986. Measurements of leaf optical properties between 400 and 1100nm were made with
an external integrating sphere (model 1800-12,
Li-Cor, Inc., Lincoln, Nebraska, USA) and scanning spectroradiometer (model Li-1800, Li-Cor).
Adaxial and abaxial surfaces were measured separately. The average of two scans of each leaf surface
(2nm wavelength intervals) was used for the
calculations of leaf transmittance and reflectance.
Results
Foliage distribution and leaf characteristics
The mean leaf area index (LAI) of the N. solandri
var. cliffortioides foliage was 6.7 f 1.2 (values in
text given as mean and 95% confidence interval).
The silhouette area index of twigs and branches
was 1.4 f 0.7. Foliage was concentrated at the top
of the canopy (15-16m), with a second apparent
peak in the mid-canopy (10m) (Fig. 1). Little
Nothofagus solandrl
var. clltfortlo1d.s
I 1
Leaf area index by tier
Fig. 1. Leaf area index by 1m tier and relative height (A)
in a Nothofagus solandri var. cliffortioides stand. Error
bars signify one standard error. Sample size for each
tier shown on figure. Total LA1 = 6.7for beech, 0.14 for
mistletoe. On Figs 1-5, the verticaI positions of the
observations are given both as (left ordinate) height
above the ground an? (right ordinate) in the dimensionless form f i where H = 1-HIHwhere H = height above
ground and H = maximum tree height in the stand, to
facilitate comparison with results from other forests (e.g.
Rauner, 1976).
+
foliage was found in the 2-5m strata; foliage at the
l m height was N. solandri var, cliffortioides
seedlings. Two species of mistletoe, Peraxilla
tetrapetala (Murr.) Tiegh. and Alepis flavida
(H0ok.f.)Tiegh., grew in the canopy, although only
Alepis flavida was encountered in the actual
harvests (present in 8.6% [13] of the 151 samples
containing foliage). The mean LA1 of Alepis flavida was 0.14 0.17 and the mean stem silhouette
area index (SAI) was 0.02. Foliage biomass of N.
solandri var. cliffortioides was 1183 241g m-2
and of A. flavida 36 54g m-'.
Foliage occurred in fewer of the sample volumes
at the top of the canopy than at lower layers (P <
0.01, X2 = 9.5, d.f. = 2). Foliage in the top third of
the canopy by LA1 (>=15m), was found in 48% of
the samples in this region. In the middle third of
the canopy (11-15 m), foliage was present in 61%
of the samples, and in the bottom third (7-llm),
75%. The foliage area densities (calculated only
from samples containing foliage) for the top,
middle and bottom third of the green canopy were
1.6, 1.0 and 0.6 m2 m-3. The foliage area densities
calculated from all samples at these levels were
0.8, 0.6 and 0.4m2 m-3.
+
+
+
56
higher than in any of the canopy above (Fig. 4).
Because of the concurrent decrease in leaf weight
per unit area, the decrease in leaf N per unit area (g
mP2)with depth into the canopy was greater than
the decrease in N concentration (Fig. 4). The N
weight per unit area of foliage at the bottom of the
canopy at 1.05g m-2 was about 41% of the canopy
top value of 2.54g m-'.
Beech and mistletoe foliage N concentrations
were not significantly different. There was no
trend of N concentration or N weight per unit area
with height in the mistletoe. N per unit area was
high in the mistletoe at about 2.7g m-'. Total
canopy nitrogen mass for the beech and mistletoe
was 12.3 2.0 and 0.37 f 0.48g m-'.
Leaf photosynthetic capacity (photosynthesis at
18-23 O C , leaf-air vapour concentration difference
5-10 mmol H20mol-' air, PFD 1000-1500 kmol
m-2 s -1 ) declined with depth into the canopy (Fig.
D. Y. Hollinger
+
Mean leaf size (ern2)
Fig. 2. Mean leaf size as a function of canopy position.
Error bars signify -t one standard error, sample size of
each tier shown on Fig. 1.
5), reflecting the decline in leaf nitrogen. Photosynthetic capacity varied with leaf N concentration and hence location in the canopy. Leaf N
content or weight N per unit leaf area accounted
for most of the variance (r2 > 0.85) in photosynthetic capacity. Photosynthetic capacity at the top
of the canopy at approximately 5 kmol mP2 s-'
was 2-3 times greater than at the bottom of the
Mean leaf size in N. solandri var. cliffortioides
reached a maximum of 0.83 cmZin the mid-canopy
(Fig. 2). Leaves at the 10-11m level of the canopy
were about 36% larger than those at the top of the
canopy and 93O/0 larger than those at the bottom.
Mean leaf size in A. flavida was 3.0cmZ and did
not vary with height (data not shown).
The mean leaf weight per unit area of beech
foliage decreased continuously from the top of the
canopy (Fig. 3) and values at the bottom of the
canopy (6m) were only about half of those at the
top (16m). The leaf weight per unit area of the
seedling (1m) strata was only about 25% of that at
the top of the canopy. Mean mistletoe leaf weight
per unit area at 263 k 31g m-2 was similar to that
of beech leaves from the top of the canopy, but did
not vary systematically with height.
Beech
A
Nitrogen distribution and leaf photosynthetic
capacity
Leaf nitrogen concentrations were significantly
higher in the mid- and upper canopy than at the
bottom (P < 0-01, F test), where the mean concentration was about 85% of that at the top (Fig. 4).
However, seedling foliage N concentration was
0
1 ,
loo
Mislk10~
I
300
200
Leaf weight per unit area (g
II-~)
Fig. 3. Leaf weight per unit area of Nothofagus solandri
var. cliffortioides and Alepis flovida as a function of
canopy position. Error bars signi@ f one standard error,
sample size of each tier shown on Fig. 1.
Canopy position:
Bottom
Middle
D. Y. Hollinger
Inclination angle class (degrees)
Fig. 6. Leaf inclination angle distributions at three
heights within a Nothofagus solandri var. cliffortioides
canopy.
12.6% for the random distribution, 11.8% for the
best fit elliptical distribution (ratio of horizontal to
vertical semi-axes of 2.1) and 26.2% for the spherical distribution. The 95% confidence intervals for
'G' values calculated from these distributions on
the summer solstice are 12.6% (random), 13.6%
(elliptical 2.1) and 32.5O/0 (spherical) of the 'G'
value calculated for the N. solandri var. cliffortioides canopy.
0-001, F test). PAR reflectance from the adaxial
surface of leaves was relatively constant with
canopy depth at about 0.06 (Table 2 and Fig. 9) but
that of the abaxial surface was 2-4 times this value
and decreased significantly at the bottom of the
canopy (P < 0.001, F test). The abaxial surfaces of
leaves at the top of the canopy were densely
pubescent. This pubescence decreased at lower
levels in the canopy. The spectral reflectance of
the abaxial (pubescent) surfaces in the PAR band
decreased below about 450nm but was otherwise
quite uniform (Fig. 9). The PAR reflected from both
leaf surfaces at the bottom of the canopy was
enhanced in the 500-600nm region. The reflectance of NIR from both leaf surfaces and at all levels
was relatively constant at about 45% (Table 2). The
pubescence on the abaxial leaf surface had no
significant effect on NIR reflectance.
Discussion
The LA1 of 6.7 for this stand (beech and mistletoe)
is between that of two N. solandri var. cliffortioides pole stands measured by a different
Optical characteristics of leaves
The mean leaf transmittance of photosynthetically
active radiation (PAR) increased significantly
down from the top of the canopy (P < 0.001, F test)
and was not significantly different for adaxial or
abaxial surfaces (Table 2). Most of the increased
transmittance of PAR with depth was in the
500-600nm region (Fig. 8). Leaves at the bottom of
the canopy also transmitted significantly more
near infrared radiation (NIR) than those higher up
in the canopy (P< 0.001, F test). The transmittance
of NIR is not symmetrical; more NIR was transmitted through the leaf from the abaxial than from
the adaxial side (P < 0-001, F test).
The reflectance of PAR from the adaxial and
abaxial surfaces was significantly different (P <
........
- - -01:
I
0800
N. solandrl var.
c1111or11e1dos
R.",om
Sph.rlc.1
Elllp8otdml (2.1)
I
I
I
I
I
1
0800
1000
1200
1400
1800
1800
Solar time
Fig. 7. Projection of foliage area in the direction of the
solar beam ('G')of Nothofagus solandri var. cliffortioides
foliage from top of canopy and three hypothetical foliage
distributions at the spring and autumn equinox.
Table 1. Mean leaf angles at different levels in a Nothofagus solandri var, cliffortioides canopy (mean and standard
deviation).
Canopy level
Inclination (O)
Orientation (0)
Top (15-16m)
Middle (11-12 m)
Lower (7-8m)
43.3 (22.4)a
22.1 (15.6)"
17.0 (14.3)a
345 (77)b
355 (74)C
315 (75Ib
--
-
" Significantly different from a spherical distribution ( P< 0.01,Kolmogorov-Smirnov one-sample test.
Not significantly different from a mean direction of 360" ( P< 0.05,V test, Batschelet, 1981).
Not significantly different from a mean direction of 360" ( P< 0.005,V test).
59
Canopy
organization
;60
. .
S
-
Bottom
-. ....
. ...
_ .....................
Middle
.'
. L.
Wavelength (nm)
Middle
Fig. 8. Mean Nothofagus solandri var. cliffortioides
foliage transmittance (adaxial surface) at three heights
within the canopy. Error bars represent the maximum
standard error in the 400-700nm wave band (n = 7).
+
"'a
abaxial
S
20
0400
technique (Nordmeyer, 1980a) and is typical of
values from broad-leaved temperate evergreen
forests (e.g. Kira, Shinozaki & Hozumi, 1969).
Values from deciduous forests tend to range somewhat lower, from about 3-6 (Miller, 1967; Ford &
Newbould, 1971; Miller & Lin, 1985; Hutchison et
al., 1986). The distribution of foliage area within
the canopy observed here is bimodal. Hutchison et
al. (1986) reported a bi- or even tri-modal distribution of foliage in a deciduous oak-hickory forest.
The mean N concentrations of N. solandri var.
cliffortioides and A. flavida foliage are very low.
However, the Craigieburn data are consistent with
530
600
adaxlal
800
700
900
1000
1100
lL!dx
40
abaxial
20
0400
500
adaxial
600 Wavelength
700
800
(nm) 900
lo00
1100
Fig. 9. Mean reflectance of abaxial and adaxial surfaces of
Nothofagus solandri var. cliffortioides foliage at three
heights within the canopy. Error bars represent 2 the
maximum standard error in the 400-700nm wave band.
Table 2. Mean leaf optical properties by height in a mountain beech canopy (mean and standard deviation).
Transmittance
-
Canopy level
-
-
400-7OOnm
-
702-1100 nm
adaxial
abaxial
adaxial
abaxial
Top (15-16m)
0.029 (0.008)
0.026 (0.005)
0.281 (0.030)
0.314 (0.034)
Middle (11-1 2 m)
0.031 (0.009)
0.033 (0.008)
0.287 (0.045)
0.349 (0.027)
Bottom (7-8m)
0.056 (0.008)
0.060 (0.006)
0.416 (0.025)
0.465 (0.024)
Tukey's critical
difference (P < 0.05)
0.011
0.051
Reflectance
Canopy level
400-700 nm
702-1100 nm
adaxial
abaxial
adaxial
abaxial
Top (15-16m)
0.060 (0.006)
0.233 (0.036)
0.442 (0.071)
0.495 (0.060)
Middle (11-12m)
0.059 (0.005)
0.199 (0.027)
0.427 (0.069)
0.477 (0.050)
Bottom (7-8m)
0.066 (0.006)
0.127 (0.018)
0.428 (0.026)
0.427 (0.052)
Tukey's critical
difference (P < 0.05)
0.032
0.091
60
previously reported values for Nothofagus sol-
D.Y. Hollinger andri var. cliffortioides (Adams, 1976; Nordmeyer, 1980b).
Trends i n spatial and physical properties of
leaves
Many of the trends found in this study seem to be
generally characteristic of forests. Leaf weight per
unit area decreased with increasing depth, as also
found by Miller (1967), Kira et al. (1969), Ford &
Newbould (1971) and Hutchison et al. (1986) and
is probably a general feature of plants which
produce leaves simultaneously throughout a
canopy.
The pattern of a mid-canopy maximum in mean
leaf size is identical to that reported for a deciduous forest canopy (Hutchison et aJ., 1986). The
small size of N. solandri var. cliffortioides leaves
and the windy but otherwise moderate habitat
suggest that the size trends observed in the Nothofagus solandri var. cliffortioides canopy are not
associated with thermoregulation or water-useefficiency (e.g. Parkhurst & Loucks, 1972; Givnish,
1979).
Leaf inclination angle seems to decrease with
increasing depth in the canopy in many forests and
has been observed in aspen, oak, pines and oakhickory canopies (Miller, 1967; Ford & Newbould,
1971; Norman & Jarvis, 1974; Hutchison et al.,
1986). Horizontally inclined leaves will be more
efficient collectors of the isotropic diffuse radiation that makes up anincreasing proportion of the
total radiation with increasing depth into the
canopy. The general model of a spherical foliage
angle distribution that has proved useful for many
crop species (e.g. Ross, 1981)may be inappropriate
for broad-leaved forest canopies. Either random or
ellipsoidal foliage angle distributions better model
the true distribution at the top of the canopy and
increasingly horizontal distributions are necessary lower in the canopy. Most observers have
assumed that foliage orientation angles are
random. However, the subtle non-random azimuthal orientation observed in the N. solandri var.
cliffortioides canopy may be widespread. Miller &
Lin (1985) also presented data showing forest leaf
orientation angles biased toward the equator. The
azimuthal asymmetries in a canopy may perhaps
be best addressed in simulation models by directly
calculating the 'G' value (or k, the related extinction coefficient where k = Gfsin 0 , 8 = the solar
altitude) from measured foliage orientations by the
method of Lemeur (1973).
The high leaf reflectance at the top of the canopy
attributed to leaf abaxial surface pubescence will
increase photosynthetically active photon flux
densities in the lower canopy. The increased
reflectivity at the top of the canopy will tend to
re-direct light reflected from the lower layers of the
canopy. Alternative hypotheses for the change in
reflectance with height including more favourable
energy balance eonsiderations associated with
either increased reflectance or an increased
boundary layer, are not supported by the constant
low reflectance of the adaxial surfaces, the moderate temperatures at the site, or the broad photosynthetic temperature optima in N. solandri var.
cliffortioides (Hollinger, unpublished data).
Similar profiles in leaf reflectance might also be
expected in other dense canopies where light
intensities at the top of the canopy are well above
saturating levels for leaf photosynthesis.
The change in many leaf characteristics (e.g. leaf
weight per unit area, N concentration, photosynthetic capacity) through the canopy suggests
that any separation into 'sun' and 'shade' foliage
classes is arbitrary. Instead, foliage characteristics
appear to change continuously - presumably in
response to a continuous change in the light
micro-environment.
Canopy architecture - moving towards optimal
carbon gain
We can reject the hypothesis that leaf angles in N.
solandri var. cliffortioides and several other tree
species are random and that leaf physical properties are constant. We can also reject the hypothesis that leaf orientations are consistent with a
spherical model. However, are the observed leaf
angles and characteristics consistent with an optimization of some factor, or does the canopy
architecture represent an evolutionarily stable
strategy?
Leaf angles in the canopy were not consistent
with maximizing carbon gain according to the
results of Duncan (1971), although the deviations
from random (e.g. more horizontal angles lower in
the canopy) are in the direction that would increase rather than decrease carbon gain. Other
deviations in leaf properties from constant values
were also in the direction that would increase
carbon gain. Smaller leaves at the top of the canopy
result in greater penumbral effects (Horn, 1971;
Oker-Blom, 1984) and leaf absorptance (l-reflectance-transmittance) is lowest at the top of the
canopy. Both of these changes serve to increase
photosynthetically active photon flux densities in
the lower canopy which increases carbon gain in
61
Canopy
organization
canopies consisting of leaves with constant physiological properties (Verhaggen et al., 1963).
Nitrogen (and consequently additional photosynthetic capacity) in N. solandri var, cliffortioides is also aUocated in the direction that
enhances overall canopy carbon gain (e.g. more at
the top) (Field, 1983). Consistent with a hypothesis that these variations maximize canopy
carbon gain and are not just a result of canopy
position, leaf size and N content in mistletoe show
no variation with height in the canopy.
The data presented here show that canopy
properties are not constant with depth, so that the
results of Verhaggen et al. (1963) and Duncan
(1971) may not apply. Explicitly to specify the
optimization function with the additional freedom
of varying foliage is far born trivial. The 'optimum'
architecture for carbon gain will depend upon a
myriad of factors, only some of which are presented in this study. Some of the more important
additional factors are the photosynthesis-light and
photosynthesis-nitrogen relationships, general
climate of the site (relating both to the ratio of
direct to diffuse radiation and the timing of favourable photosynthetic periods) as well as any costs
(e.g. herbivory) associated with various architectures. To consider the evolutionary stability of an
architecture requires additional data about how
architecture of adjacent individuals may interact,
the relatedness of these individuals and about the
heritability of architecture. Simulation models
provide a powerful method of testing some of these
ideas. Natural systems provide other avenues of
investigation. Both the natural variation within a
species and that existing between species can be
used to test these hypotheses. For example, the
investigations of Miller (1967), Ford & Newbould
(1971), Hutchison et al. (1986) and this current
study show a very consistent pattern in broadleaved tree architecture. Is this because it is an
ESS? How does the architecture differ between
species in a mixed species forest? An ESS may
result in canopy architecture converging when
species exist as stable mixtures but diverging
where one species competitively replaces another.
Conclusions
Many canopy models have, in the interests of
simplicity and economy, considered randomly
located and orientated leaves of constant physical
and physiological properties. The data from
Nothofagus solandri var. cliffortioides, the oakhickory forest of Hutchison et al. (1986) and other
previous studies of canopy architecture suggest
that these simplifications are unrealistic. The field
data instead lend support to a hypothesis that
canopy architecture and canopy nitrogen distribution are optimized for maximum carbon gain in
the particular habitat of the plant. Additional
modelling should give us a better understanding of
the trade-offs between leaf and canopy characteristics for maximizing carbon gain both with and
without competitors. However, for simulations of
actual stand production a renewed emphasis on
measurements of canopy architecture would probably be appropriate.
Acknowledgments
Thanks to J. Hunt, A. Allan, J. Byers, T. McSeveny
and G. Rogers for expert technical assistance and
A. Greene for the loan of the spectroradiometer.
My appreciation also to J. Hunt, U. Benecke and A.
Nordmeyer for their helpful discussions and to U.
Benecke and J. Orwin for their comments on the
manuscript.
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Received 27 January 1988; revised 16 June; accepted 28
June 1988