Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol15.1995:

Tree Physiology 15, 791--798
© 1995 Heron Publishing----Victoria, Canada

Effects of light availability and tree size on the architecture of
assimilative surface in the canopy of Picea abies: variation in shoot
structure
ÜLO NIINEMETS1,2 and OLEVI KULL1
1

Institute of Ecology, Estonian Academy of Sciences, 40 Lai Street, EE2400 Tartu, Estonia

2

Present address: LS Pflanzenökologie, BITÖK, Universität Bayreuth, Postfach 10 12 51, 95448 Bayreuth, Germany

Received February 2, 1995

Summary Dependence of shoot morphology on relative irradiance (diffuse site factor, ad) and total tree height (TTH) was
studied in a natural canopy of Picea abies (L.) Karst. Surface
area of foliar elements was characterized by total needle area
(TLA, all-sided needle surface), projected needle area (PLA,

area of detached needles laid flat on a horizontal surface), and
vertical and horizontal silhouette shoot areas (SSA0 and SSA90,
defined as shadows cast by shoots with fixed horizontal inclinations of 0° and rotation angles of 0° and 90°, respectively).
With increasing irradiance and tree size, packing of needles
(needle number per unit shoot length, Ls) and packing of TLA
(TLA/Ls) increased, but packing of SSA0 (SSA0 /Ls) was invariant. Accordingly, the SSA0 to TLA ratio (STAR0) decreased,
signifying that the proportion of TLA exposed to direct solar
radiation declined, and thus the cost of SSA0 in terms of TLA
increased with increasing ad and TTH. Factors causing costlier
SSA0 at high irradiances and in tall trees included increases in
needle packing, changes in needle morphology (increases in
needle dry weight per TLA and decreases in TLA/PLA), and
changes in needle position and angle of needle inclination.
The weight of the shoot axis (Ma) was used as an estimate of
biomass costs for mechanical support of the needles and water
supply to the needles. Foliage-area-based needle-support costs
(NSCa), defined as Ma per unit foliage surface (TLA, PLA or
SSA0) increased with ad and were not related to TTH, whereas
foliage-weight-based needle-support costs (Ma/Mn ) decreased
with increasing TTH and were independent of ad.

Keywords: conifers, foliage area, LAI, leaf morphology, needle
packing, silhouette area, STAR.

Introduction
Because annual production of a stand quasi-linearly depends
on intercepted shortwave solar radiation (Jarvis and Leverenz
1983, Linder 1985), canopy attributes, such as leaf inclination
and clumping, which influence light absorption at constant
values of leaf area index (LAI, foliage area per ground area)
and thus determine the effectiveness of unit foliage area for
light interception, are important stand parameters.

If canopy foliage elements are distributed randomly, transmitted radiation (I) decreases exponentially with increasing
stand LAI according to Lambert-Beer’s law (e.g., Monsi and
Saeki 1953):
I = I0 e− k LAI /cos α ,

(1)

(where I0 is the irradiance above the stand, k is the extinction

coefficient, and α is the solar zenith angle), hence permitting
simultaneous estimation of canopy transmittance and LAI on
the basis of light measurements alone, provided that the mean
leaf inclination determining k is known. In coniferous trees,
however, needles are grouped on shoots, and canopy models
that assume random foliage distribution significantly underestimate stand LAI (Gower and Norman 1991, Chen and Black
1992). To account for needle clumping, a conifer shoot is
considered as the foliage element corresponding to a leaf of a
broad-leaved species (Oker-Blom 1986, Leverenz and Hinckley 1990). Accordingly, a detailed knowledge of shoot architecture and identification of patterns of variation are needed to
estimate foliage area and describe the light environment in a
coniferous canopy (Oker-Blom and Smolander 1988, Gower
and Norman 1991). Furthermore, dry matter production may
be directly related to shoot architecture, because the ability to
change shoot structure with respect to shading within the
canopy correlates closely with the efficiency of light-intercepting foliage display and the upper limit of LAI the species may
attain (Leverenz and Hinckley 1990, Leverenz 1992).
Several qualitative modifications in leaf morphology and
functioning along an irradiance gradient across the canopy
have been reported for leaves (e.g., Björkman 1981), but much
less is known about morphological acclimation in conifer

shoots with respect to irradiance. The ratio of shoot silhouette
to total needle surface area (STAR), which depends on several
shoot parameters, including needle orientation and inclination
(Carter and Smith 1985) and needle overlapping (Carter and
Smith 1985, Oker-Blom and Smolander 1988), has been used
to characterize shoot morphology and needle clumping (e.g.,
Oker-Blom and Smolander 1988). The STAR is equivalent to
the extinction coefficient in Equation 1 (Oker-Blom and Smo-

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NIINEMETS AND KULL

lander 1988). In Picea abies (L.) Karst., consideration of only
changes in needle structure and needle number per shoot
length predicted a linear decrease in STAR with increasing
irradiance (Niinemets and Kull 1995). We conclude, therefore,
that relative irradiance is a relevant determinant of shoot structure, and have undertaken to identify explicitly the patterns of
variation in shoot traits along a light gradient in the canopy.
In conifers, needle morphology is also affected by tree age

(Greenwood 1984, Steele et al. 1989) and dimensions (Niinemets and Kull 1995). Inasmuch as large environmental gradients and gradients of water potential exist in the crowns of tall
trees (Hellkvist et al. 1974) and the fraction of annual production allocated for supporting tissues increases with total tree
height (Givnish 1988), it is likely that shoot morphology as
well as partitioning of assimilative and supporting structures
within the shoot also change with changing tree size. Accordingly, we have examined variations in shoot structure and
partitioning of shoot biomass with respect to a natural gradient
of relative irradiance and to total tree height in a stand of
P. abies.

Material and methods
The study was conducted in a nemoral spruce forest, located
on a plateau-like crest of a drumlin with brown pseudopodzolic
soil, at Voore Ecological Station, Estonia (58°44′ N, 26°45′ E,
elevation 90 m above sea level), at the beginning of August
1989. Frey (1977) gives a thorough description of the study
site.
Current-year shoots at terminal branch positions were collected from the southern aspect of six variously exposed
P. abies trees. At two to five canopy heights per tree, four to
seven shoots per canopy height were taken, and means of all
shoot parameters for a given canopy height were determined.

Total tree height ranged from 1.6 to 35.5 m, and relative
sampling height (Rh), i.e., sampling height per total tree height,
ranged from 0.07 to 0.96, but the maximum Rh per tree was
never less than 0.78.
The hemispherical photographic technique (Anderson 1964,
Nilson and Ross 1979) was used to estimate relative irradiance
at the sample locations. The proportion of canopy gaps was
measured with respect to zenith angle, and the diffuse site
factor (ad, proportion of penetrating diffuse solar radiation)
was calculated. The value of ad is equal to unity above the
canopy and to zero in complete shade without any canopy
gaps. Further details about shoot sampling and estimation of
ad are given in Niinemets and Kull (1995).
Changing patterns of water relations and increasing gradients of environmental parameters with increasing tree size
were assumed to cause changes in shoot structure. Therefore,
total tree height (TTH), which was not significantly related to
ad (P > 0.2), was included in the statistical models as a second
independent variable.
Shoot silhouette area (SSA, shadow cast by a shoot) was
measured with an optical planimeter. The shoot axis was kept

perpendicular to the light source, and vertical (SSA0) and
horizontal (SSA90) silhouette areas (Boyce 1993, Figure 1)

were measured. There are an infinite number of silhouette
areas with respect to different sun elevations and shoot inclinations; however, we used a fixed angle of 90° between view
direction and shoot axis and only studied the variation in SSA
with rotation angle. A shoot with a horizontal inclination of 0°
has a silhouette area that is equal to SSA0 if the sun is in the
zenith (0°), and equal to SSA90 if the sun is at the horizon (90°)
and the azimuth angles of the shoot and sun are normal to each
other (Figure 1). Although these extreme conditions rarely
occur, various combinations of shoot and sun angles would
yield the situations depicted in Figure 1. In experimental studies, only SSA0 is usually measured (e.g., Carter and Smith
1985). Because measures of SSA also included the area of the
shoot axis, SSA was somewhat overestimated compared to the
silhouette area of needles only.
Ten needles were randomly selected from the central part of
a shoot, and mean total (TLAn) and projected (PLAn) needle
surface areas for a single needle calculated by means of a
geometric model that describes needle shape as a rhomboid

(Niinemets and Kull 1995). Total (TLA) and projected (PLA)
needle surface areas for a shoot were calculated from the
estimations of TLAn, PLAn and needle number per shoot (N).
The ratios of silhouette area to both total needle surface area
(STAR0) and projected surface area (SPAR0) were calculated
as the ratios of SSA0 to TLA and PLA, respectively. Needle
packing (NP) was calculated as the ratio of N to shoot length
(Ls, length of shoot axis) (Carter and Smith 1985, Boyce 1993).
Packing of TLA (TLAP), PLA (PLAP) and SSA (SSAP) was
defined as TLA, PLA and SSA0, respectively, per unit shoot
length. Shoots were oven-dried at 85 °C for 48 h to determine
dry weights of needles (Mn ) and shoot axis (Ma). Needle
weight per TLA (LWA) and per SSA0 (SWA), and packing of
needle dry weight (Mn /Ls) were calculated.
Because a balance exists between needle demand for water
and the capacity of conductive tissues to provide water, allometric relationships between foliar and sapwood area (Kaufmann and Troendle 1981), foliar biomass and sapwood area
(Grier and Waring 1974, Kaufmann and Troendle 1981) or
between foliar area and sapwood volume (Ryan 1989) are
often found. Thus the ability of the shoot axis to supply the
needles with water must scale with the amount of foliage on

the shoot, and hence Ma may serve as an estimate of biomass

Figure 1. Definition of vertical (SSA0) and horizontal (SSA90) shoot
silhouette areas (Boyce 1993). Axial view of a shoot with a fixed
horizontal inclination angle of 0°.

SHOOT STRUCTURE IN PICEA

costs for needle support (NSC). Moreover, the shoot axis also
provides needles with mechanical support, thus adding another
dimension to the term NSC. By using Ma as an estimate of
NSC, we assume that the costs for construction and maintenance (e.g., carbon costs for respiration) of the shoot axis
(Chazdon 1986) and for structures of the shoot axis that are not
directly related to water conduction and mechanical strength
(bark, pith, buds) are proportional to the weight of the shoot
axis. For comparative purposes, relative measures of NSC
were found: NSC per unit foliage weight (NSCm) was defined
as Ma/Mn, and NSC per unit foliage area (NSCa) as Ma/TLA
(NSCTLA ), Ma/PLA (NSCPLA ) and Ma/SSA0 (NSCSSA0).
Linear regression and correlation techniques were used, and

all relationships were considered significant at P < 0.05. Definitions and mean values (± SE) of all needle and shoot parameters are listed in Table 1.
Results
Packing of needles, needle surface and weight
Needle number per unit shoot length (NP) and total needle area
packing (TLAP) increased significantly with increasing total
tree height (TTH) (r 2 = 0.362, P < 0.01 and r 2 = 0.322, P < 0.02,
respectively) and diffusive site factor (ad) (r 2 = 0.708, P < 0.001
and r 2 = 0.497, P < 0.002, respectively) (Figure 2A and 2B).
Because TLAP = NP × TLAn, and mean TLA per needle
(TLAn) was not correlated with either ad or TTH (P < 0.05,
Niinemets and Kull 1995), the dependence of TLAP on ad and
TTH is mainly attributable to variation in NP.
Packing of PLA (PLAP) increased with TTH (r 2 = 0.293, P
< 0.05) and ad (r 2 = 0.238, P < 0.05). Inasmuch as PLAP is
equal to:
PLAP =

TLAP
TLA /PLA

,

(2)

793

Table. 1. Definitions and means (n = 86) for all studied shoot parameters.
Abbreviation

Definition

Mean ± SE

Ls
LWA
Ma
Mn
N
NP
NSC
NSCa
NSCm
NSCTLA
NSCPLA
NSCSSA0
PLA
PLAn
PLAP
SSA
SSA0
SSA90
SSAP
SSA0/SSA90
SPAR0
STAR0
SWA
TLA
TLAn
TLA/PLA
TLAP

Length of shoot axis
Needle dry weight per TLA
Weight of shoot axis
Needle dry weight per shoot
Needle number per shoot
Needle packing (N/Ls)
Needle-supporting costs
Area-based NSC
Weight-based NSC (Ma /Mn)
TLA-based NSCa (Ma /TLA)
PLA-based NSCa (Ma /PLA)
SSA0-based NSCa (Ma /SSA0)
PLAn × N
Projected needle area per needle
PLA packing (PLA/Ls)
Shoot silhouette area
SSA for sun in zenith
SSA for sun at horizon
SSA0 packing (SSA0 /Ls)
Ratio of SSA0 to SSA90
SSA0 to PLA ratio
SSA0 to TLA ratio
Needle weight per SSA0
TLAn × N
Total needle area per needle
Ratio of TLA to PLA
TLA packing (TLA/Ls)

5.85 ± 0.37 cm
62.4 ± 2.5 g m − 2
0.072 ± 0.011 g
0.226 ± 0.021 g
90.6 ± 6.1
15.40 ± 0.44 cm − 1

9.14 ± 0.74 cm2
7.21 ± 0.54 cm2
23.1 ± 1.5 cm2 cm − 1
1.29 ± 0.03 cm2 cm − 2
0.76 ± 0.02 cm2 cm − 2
0.27 ± 0.01 cm2 cm − 2
247 ± 12 g m − 2
35.2 ± 3.1 cm2
36.5 ± 1.1 mm2
2.84 ± 0.04 cm2 cm − 2
5.65 ± 0.23 cm2 cm − 1

Packing of SSA (SSAP) was not significantly correlated
with either ad or TTH (P > 0.05); therefore, SSA0 /TLA
(STAR0), which can be expressed as:
STAR0 =

and the ratio TLA/PLA increased linearly with ad (Niinemets
and Kull 1995), there are two opposing tendencies with increasing ad: (1) decreasing PLA at constant TLA, and (2)
increasing needle packing (Figure 2A) and consequently
TLAP (Figure 2B). As a result of (1) and (2), there was only a
poor correlation between PLAP and ad.

0.269 ± 0.011 g g − 1
16.7 ± 0.9 g m −2
48.8 ± 3.1 g m − 2
66.2 ± 4.2 g m − 2
12.17 ± 0.96 cm2
12.95 ± 0.39 mm2
16.6 ± 0.8 cm2 cm − 1

SSAP
,
TLAP

(3)

decreased significantly with increasing TTH (r 2 = 0.393, P <
0.01) and irradiance (r 2 = 0.586, P < 0.001, Figure 3A), as did
SPAR0 (r 2 = 0.430, P < 0.01 and r 2 = 0.366, P < 0.01 for TTH
and ad, respectively). The ratio SSA0 /SSA90, characterizing the
Figure 2. Effects of relative irradiance (diffuse site factor, ad) and
total tree height (TTH, m) on
packing of needles and needle surface area. (A) Needle number per
unit length of shoot axis (NP, needles cm −1) versus TTH and ad;
NP = 0.0876TTH + 12.2ad + 9.61
(r 2 = 0.819, P < 0.001, n = 17).
(B) Total needle surface area
(TLA) per unit shoot length
(TLAP, cm2 cm −1) versus TTH
and ad; TLAP = 0.0487TTH +
5.23ad + 3.06 (r 2 = 0.618, P <
0.01, n = 17).

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NIINEMETS AND KULL
Figure 3. Ratio of shoot silhouette
(SSA0) to total needle area
(STAR0), and of shoot silhouette
areas (SSA0/SSA90) with respect
to relative irradiance and total tree
height. Because both STAR0 and
SSA0 /SSA90 decrease with increasing ad and TTH, scales for
TTH and ad have been reversed to
facilitate reading the data. (A)
STAR0 = −0.00163TTH −
0.169ad + 0.356, (r 2 = 0.737, P <
0.001, n = 17). (B) SSA0 /SSA90 =
−0.00942TTH − 0.397ad + 1.61,
(r 2 = 0.672, P < 0.001, n = 17).

radial symmetry of a shoot, declined with increasing TTH (r 2
= 0.548, P < 0.001) and ad (r 2 = 0.342, P < 0.02, Figure 3B),
signifying that both the fraction of needles lying outside the
SSA0 plane and the symmetry of the shoot about its axis
increase with increasing ad and TTH. Both STAR0 (Figure 4)
and SPAR0 (data not shown) were dependent on changes in
needle morphology (TLA/PLA, Figure 4A) and shoot structure (SSA0/SSA90 and NP, Figure 4B and 4C).
Needle weight per SSA0 (SWA) increased with increasing
TTH (r 2 = 0.416, P < 0.01) and ad (r 2 = 0.674, P < 0.001,
Figure 5). Because SWA is equal to:
SWA =

LWA
,
STAR0

(4)

(where LWA is needle dry weight per TLA), changes in both
needle morphology, i.e., increasing LWA with ad and TTH
(Niinemets and Kull 1995), and shoot structure (STAR0, Figure 3A) are responsible for the variation in SWA. Similarly, an
increase in packing of needle dry weight (Mn /Ls) with increasing TTH (r 2 = 0.501, P < 0.002) and ad (r 2 = 0.559, P < 0.001)
can be ascribed to both increasing needle packing and increasing LWA (Mn /Ls = LWA × NP × TLAn).
Needle support
Needle-support costs per foliage area (NSCa, equal to NSCTLA
, NSCPLA and NSCSSA0) increased with increasing ad (P < 0.01,
Figure 6A), whereas NSCa was not significantly correlated

with TTH. Similarly, Ma/Ls increased with increasing ad (r 2 =
0.497, P < 0.01) but was independent of TTH. Because NSC
per unit foliage weight (NSCm) equals:
NSC m =

NSC TLA

LWA

(5)

,

and LWA increases with ad and TTH (Niinemets and Kull
1995), NSCm should be inversely related to TTH. Indeed,
NSCm decreased with increasing TTH (r 2 = 0.347, P < 0.02,
Figure 6B) but was not related to ad. Furthermore, NSCm (r 2 =
0.599, P < 0.001) and NSCa (P < 0.001, r 2 = 0.197, 0.172 and
0.131 for NSCTLA , NSCPLA and NSCSSA0, respectively) increased with increasing Ls (n = 86), but Ls was not related to
TTH, ad or to most indices of shoot structure (P > 0.05), except
for weak correlations with TLAP (r = 0.293, P < 0.01) and
PLAP (r = 0.266, P < 0.02).

Discussion
Packing of needles, needle surface and weight
Needle packing (NP) increases similarly (Figure 2A) with
increasing irradiance in Abies lasiocarpa (Hook.) Nutt., Picea
engelmannii Parry ex Engelm., Pinus contorta Dougl. ex
Loud. (Carter and Smith 1985, Smith and Carter 1988), Picea
sitchensis (Bong.) Carr. (Leverenz and Jarvis 1980b), Pinus
taeda L. (recalculation of data of Cregg et al. 1993) and
Figure 4. Dependencies of STAR0
on needle morphology
(TLA/PLA) and shoot structure
(NP, SSA0 /SSA90). (A) STAR0
versus TLA/PLA; STAR0 = 0.690
− 0.152TLA/PLA (r 2 = 0.546, P <
0.001, n = 17). (B) STAR0 versus
NP; STAR0 = 0.486 − 0.0141NP
(r 2 = 0.777, P < 0.001, n = 17).
(C) STAR0 versus SSA0/SSA90;
STAR0 = 0.024 +
0.186SSA0 /SSA90 (r 2 = 0.528, P
< 0.001, n = 17, intercept is not
significantly different from zero).

SHOOT STRUCTURE IN PICEA

Figure 5. Effects of TTH and ad on needle dry weight per SSA0 (SWA,
g m −2 ); SWA = 4.06TTH + 310ad + 50.9 (r2 = 0.880, P < 0.001, n =
17).

Pseudotsuga menziesii (Mirb.) Franco (Drew and Ferrell
1977), and with increasing canopy height in Abies balsamea
(L.) Mill. and Picea rubens Sarg. (Boyce 1993). However, in
Pinus sylvestris L., NP decreased with increasing canopy
height (Kellomäki and Oker-Blom 1983). High NP in tall trees
might be associated with increased water limitations in the
crowns of large trees, resulting in reduced water potentials and
retarded extension growth of shoots. For example, decreasing
values of NP with increasing Ls in Abies fraseri (Pursh) Poir.
(Brewer et al. 1992) and Tsuga canadensis (L.) Carr. (Powell
1992) were attributable to a decrease in overall plant vigor,
resulting in declining rates of shoot extension growth. However, in P. taeda (recalculation of data of Cregg et al. 1993) NP
increased with increasing Ls, and in our study, the decrease in
Ls with increasing TTH was not significant and there was no
relationship between Ls and NP, suggesting that other mechanisms may govern TTH-related variation in NP.
The amount of TLA that can be accommodated per unit Ls
(TLAP) is influenced by relative irradiance and TTH because
NP increases with increasing TTH and ad (Figure 2A and 2B).
However, as the complexity of foliage organization (TLA <
PLA < SSA0) increases, the effect of NP on surface area
packing gradually decreases (Equations 2 and 3), and the
shading effect of a unit shoot length (SSAP) becomes independent of ad and TTH. Also, increased needle packing is
counterbalanced by decreasing exposure of needle surface area
at a constant total needle area (TLA/PLA) (Niinemets and Kull
1995, Figure 4A) and increasing needle overlapping, needle
deviation from the SSA0 plane (Figure 3B and 4C), and angle

795

of needle inclination (Greis and Kellomäki 1981). Thus costs
for interception of direct radiation by a unit SSA0 are higher in
the upper crown and in taller trees than in the lower crown and
in smaller trees as illustrated by constant values of SSAP with
increasing NP, or decreasing values of STAR0 and SPAR0 (the
construction efficiencies of silhouette area in units of TLA and
PLA, respectively) with increasing ad and TTH (Figure 3A),
and NP (Figure 4B). Similar patterns have also been found for
other conifers. For example, STAR0 decreased with increasing
canopy height in P. rubens and A. balsamea (Boyce 1993), and
it was less in sun than in shade in P. engelmanni and A. lasiocarpa (Carter and Smith 1985). Tucker et al. (1987) reported
that SPAR0 decreased with increasing irradiance in Abies
amabilis Dougl. ex Forbes. However, because shoot asymmetry increases with decreasing ad and TTH, e.g., SSA0 /SSA90
(Figure 3B), the efficacy of various shoots depends on solar
elevation. Thus sun shoots and shoots of tall trees exhibiting
low efficiency in intercepting direct radiation at high solar
elevations, as indicated by low values of STAR0 and SPAR0,
may be more efficient at low solar elevations than shade shoots
and shoots of small trees. For broad-leaved species, canopy
photosynthesis is maximized when LWA follows the light
gradient (Gutschick and Wiegel 1988). Because needles at
various positions within a shoot have about the same photosynthetic capacity (Leverenz and Jarvis 1980a, Carter and Smith
1985), it can be advantageous to invest more photosynthetic
weight and area where ad is high, which would lead to a shoot
architecture characterized by high values of NP and SWA and
low values of STAR0 and SPAR0 (Figures 2--5).
In several species, it has been found that angles of leaf
inclination increase with increasing light availability (McMillen and McClendon 1979), allowing light to penetrate deeper
foliage layers. The extinction coefficient (Equation 1), which
determines the light absorption efficiency of foliage area, depends on foliage grouping and inclination angle (Anderson
1966), and values of STAR0 (if LAI is for TLA) and SPAR0 (if
LAI is for PLA) are close to the extinction coefficient if sun is
in the zenith (Oker-Blom 1986, Oker-Blom and Smolander
1988). Accordingly, increasing STAR0 and SPAR0 with decreasing ad may result in a situation where the extinction
coefficient is dependent on irradiance, and accordingly the
transmitted irradiance at each canopy height (Equation 1) is
influenced by both cumulative foliar area and the adaptation of
foliar architecture to incident irradiance. Though a mean exFigure 6. Dependence of needle support
costs (NSC) on relative irradiance and total tree height. (A) NSC per unit foliage
area (NSCa, g m −2) versus ad; s = NSC
per unit TLA, NSCTLA = 18.7ad + 9.26,
(r 2 = 0.370, P < 0.01, n = 17); d = NSC
per unit PLA, NSCPLA = 71.0ad + 19.9 (r 2
= 0.496, P < 0.01, n =17); n = NSC per
unit SSA0, NSCSSA0 = 127.4ad + 16.5 (r 2
= 0.730, P < 0.001, n = 17). (B) NSC per
unit foliage weight (NSCm, g g −1) versus
TTH; NSCm = 0.351 − 0.00408TTH, (r 2 =
0.347, P < 0.02, n = 17).

796

NIINEMETS AND KULL

tinction coefficient for the whole canopy may be derived from
the light measurements from above and below the canopy,
canopy models can be improved by the use of several extinction coefficients that take account of canopy structure (Baldocchi et al. 1984, Koppel and Oja 1984).
Variation in shoot structure also influences canopy energy
balance by affecting the convective energy exchange of shoots.
Overstory leaves might be expected to favor adaptations contributing to convective cooling because they are exposed to
high radiation loads (Vogel 1968). However, increased needle
packing at higher ad results in higher needle temperatures and
less effective convective cooling (Koppel 1982, Smith and
Carter 1988, Figure 2A). Furthermore, in Picea pungens
Engelm., up to 20% of the variation in needle temperature is
explained by differences in needle position with respect to
wind (Tibbals et al. 1964). Thus, increasing needle width with
increasing ad in P. abies (Niinemets and Kull 1995) is also
likely to cause significantly higher needle temperatures for
needles grown at high ad at the same radiation loads. Elevated
needle temperature may be advantageous if the air temperature
is lower than optimum for photosynthesis (Givnish 1987,
Smith and Carter 1988, Sprugel 1989, Smith and Brewer
1994). Because light reactions of photosynthesis are not very
temperature sensitive, overall shoot photosynthesis only depends on temperature when leaves are light-saturated (Sprugel
1989), and inasmuch as needles located deeper in the canopy
seldom reach light saturation, high needle temperature would
preferentially enhance photosynthetic rates at high irradiances.
Therefore, unlike many deciduous species, variation in evergreen shoot structure with ad may favor less efficient convective cooling at high solar radiation loads.
Increased needle packing at high relative irradiances may
also serve a protective function. After overstory removal, serious damage to photosynthetic apparatus of understory-grown
individuals of A. amabilis was related to elevated irradiance
(Tucker et al. 1987). In Macroptilium atropurpureum DC., the
damage was related to increased angle of leaf inclination,
diminished light interception, and decreased leaf photoinhibition (Ludlow and Björkman 1984). Accordingly, increasing
needle overlapping and inclination from the horizontal (i.e.,
higher cost of unit SSA0 in terms of TLA (Figure 3A)) with
increasing ad, or increasing shoot radial symmetry (i.e., lower
SSA0/SSA90 (Figure 3B)) with increasing ad are likely to
reduce the probability of photoinhibition at high ad, because all
of these modifications work in concert to decrease mean irradiance at the needle surface.
Needle support
In several understory palm species, NSCa increases with increasing plant age (Chazdon 1986). However, TTH did not
influence NSCa in P. abies, and NSCm decreased with increasing TTH (Figure 6B). Costs for needle support at different
relative irradiances scale with foliage weight rather than with
area, as indicated by the constant values of NSCm with increasing ad, and the finding that, with increasing ad, NSCa increased
in direct proportion with increasing foliage weight per area
(Figure 5, NSCSSA0 = NSCm × SWA).

As in P. abies, NSCm in P. taeda tended to decrease with age
of grafted scion (recalculation of data of Greenwood 1984).
Increasing NSCm with increasing Ls and the high supporting
efficiency (1/NSCm) of large trees (Figure 6B) may indicate
that young and small trees with relatively long and sparsely
needled shoots (Figure 2A) preferentially allocate resources to
extension growth rather than to diameter growth of stem and
branches as in large trees. Small trees may also have more
plagiotropic shoots than large trees, because a horizontal shoot
axis can bear less needle weight per unit twig weight than a
vertical shoot axis (Horn 1971, Givnish 1988), resulting in
higher NSCm. Furthermore, small trees must sustain higher
snow loads during the winter than large trees, because crown
weight increases more rapidly with TTH than does crown area,
resulting in relatively thicker stems in saplings than in large
trees (King 1991).
However, expenditures for mechanical support in terms of
biomass are usually much higher than actual requirements
(Chazdon 1986, King 1991) and lower NSCm in large trees
may be inadequate to meet the needs for water transport,
resulting in higher water stress in large than in small trees.
Decreasing photosynthetic rates with increasing plant age in
Chrysothamnus nauseosus (Pall.) Britt. (Donovan and Ehleringer 1992), P. contorta and Pinus ponderosa Dougl. (Yoder et
al. 1994) were not related to declining biochemical capacities
of photosynthetic apparatus but to increasing water limitation
in crowns of large trees.
Implications for canopy dynamics
Biomass investment for production of unit leaf area (LWA)
increased with tree age in Eucalyptus grandis W. Hill ex
Maiden. (Leuning et al. 1991) and P. sitchensis (Steele et al.
1989), and with TTH in P. abies (Niinemets and Kull 1995).
Moreover, because of increasing needle packing (Figure 2A)
and shoot radial symmetry (Figure 3B) with increasing TTH,
biomass requirements for construction of unit shoot area
(SWA) increased with increasing TTH in P. abies more rapidly
than the costs for the production of a unit TLA (Figure 5,
Equation 4). Because the ability of a species to produce unit
SSA0 with minimum structural requirements ultimately determines the LAI the species can attain (Leverenz and Hinckley
1990, Leverenz 1992), decreasing values of STAR0 and SPAR0
with increasing TTH (Figure 3A) may result in decreased
values of stand LAI. Furthermore, because total biomass production (Pta , annual biomass production per ground area, g
m −2) of a stand decreases after maximum LAI is reached
(Linder 1985), and relative allocation of annual production for
foliage construction (Pf/Pta, where Pf is annual foliage production per ground area, g m −2) decreases with TTH (Whittaker
and Woodwell 1968, Givnish 1988), it follows that stand LAI
should decline with increasing TTH after a threshold TTH has
been reached:
LAI =

Pta (Pf /Pta )
.
LWA

(6)

The product of LAI × STAR (shoot silhouette area per ground

SHOOT STRUCTURE IN PICEA

area), not LAI per se, scales with light interception, and therefore, the effect of TTH on light transmission by the canopy is
likely to be greater than indicated by the decrease in stand LAI
(Equations 4 and 6, Figures 3--5).
The amount of irradiance transmitted by the overstory is an
important ecological factor determining long-term dynamics
and productivity of the understory as well as self-regeneration
of canopy dominants. Thus there is a trade-off between high
stand LAI, resulting in enhanced light interception that is
advantageous in shading out possible competitors (Gutschick
and Wiegel 1988), and natural regeneration, benefiting from
high irradiances in the understory. Dispersal and habitat occupation by young trees may also be facilitated by the ability of
young trees to form extensive foliar displays that enable efficient light capture in the understory with minimum investment
in biomass (Figure 5).
Acknowledgments
We thank Kalle Sôber for skillful technical assistance.

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