Directory UMM :Data Elmu:jurnal:T:Tree Physiology:vol17.1997:

Tree Physiology 17, 723--732
© 1997 Heron Publishing----Victoria, Canada

Acclimation to low irradiance in Picea abies: influences of past and
present light climate on foliage structure and function
ÜLO NIINEMETS
Institute of Ecology, Estonian Academy of Sciences, Riia 181, Tartu EE 2400, Estonia

Received May 2, 1996

Summary Leaf retention time increases with decreasing irradiance, providing an effective way of amortizing the costs of
foliage construction over time. To elucidate the physiological
mechanisms underlying this dependence, I studied needle life
span, morphology, and concentrations of carbon, nitrogen and
nonstructural carbohydrates along a gradient of relative irradiance in understory trees of Picea abies (L.) Karst. Maximum
needle life span was greater in shaded trees than in sun-exposed
trees. However, irrespective of irradiance, needles with maximum longevity were situated in the middle rather than the
bottom of the canopy, suggesting that needle life span is
determined by the irradiance to which needles are exposed
during their primary growth. Morphology and chemistry of
current-year needles were adapted to prevailing light conditions. Current-year needles exposed to high irradiances had

greater packing of foliar biomass per unit area than shaded
needles, whereas shaded needles maximized foliar area to
capture more light. Nitrogen concentrations were higher in
shaded needles than in sun-exposed needles. This nitrogen
distribution pattern was related to the high nitrogen cost of light
interception and was assumed to improve light absorptance per
needle mass of shaded needles. In contrast, in both 1- and
2-year-old needles, morphology was independent of prevailing
light conditions; however, needle nitrogen concentrations were
adjusted toward more effective light interception in 2-year-old
foliage but not in 1-year-old foliage, indicating that acclimation
of sun-adapted needles to shading takes more than one year. At
the same time, needle aging was accompanied by accumulation
of nonstructural carbohydrates (NSC), and increasing concentrations of needle carbon, suggesting a shift in the balance
between photosynthesis and photosynthate export. The accumulation of NSC and carbon resulted in a dilution of the
concentrations of other needle chemicals and explained the
decline in needle nitrogen concentrations with increasing age.
Thus, although morphological inadequacy to low light availabilities may partly be compensated for by modifications in
needle chemistry, age-related changes in needle stoichiometric
composition progressively lessen the potential for acclimation

to low irradiance. A conceptual model, advanced to explain
how environmental factors and age-related changes in the
activities of needle xylem and phloem transport affect needle
longevity, predicted that adaptation of needle morphology to
irradiance during the primary growth period largely determines

the fate of needles during subsequent tree growth and development.
Keywords: aging, carbon balance, needle longevity, needle
morphology, nitrogen content, nonstructural carbohydrates,
Norway spruce, shade tolerance.

Introduction
Plants acclimate to low irradiances in forest understories by
enhancement of light capture as a result of plastic modifications of foliar and canopy architecture and biomass allocation
patterns (Givnish 1988, Pearcy and Sims 1994). Although
increased assimilate investment in leaf area formation improves light interception (Pearcy and Sims 1994), the high
carbon cost of this investment seriously limits enhanced foliage production. Therefore, an increase in leaf longevity, resulting in greater foliar biomass accumulation (Schulze et al.
1977, Reich et al. 1992), provides an effective way of amortizing the costs of leaf construction over the long-term and enables construction of an efficient foliar display for light
absorption in low-light environments. A wide range of species,
including the herb Fragaria virginiana Duchesne (Jurik et al.

1979), the shrubs Rhododendron maximum L. (Nilsen et al.
1987), Daphniphyllum macropodum var. humile Rosenthal
and Pachysandra terminalis Sieb. et Zucc. (Kikuzawa 1988),
several tropical woody Piper species (Williams et al. 1989) and
the conifers Abies mariesii Mast. (Kohyama 1980), Picea
abies (L.) Karst. and Pinus cembra L. (Koike et al. 1994) are
able to extend foliar retention time in response to increased
habitat shading. Additionally, leaf life span may adjust to
differences in irradiance across the canopy (e.g., Pinus contorta Engelm.; Schoettle 1989). However, apart from phenomenological observations, little is known about the
physiological mechanisms underlying adjustments in foliage
life span.
Several studies on the acclimation of current-year needles of
evergreen woody species to within-canopy light gradients have
recently been described (Niinemets and Kull 1995b, Sprugel
et al. 1996, Niinemets 1997a). In conifers, needle thickness
generally increases with increasing irradiance (Aussenac
1973, Tucker and Emmingham 1977, Sprugel et al. 1996),
resulting in a positive relationship between needle dry mass

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NIINEMETS

per area (LMA) and irradiance. Plastic modifications in needle
morphology also appear to underlie the frequently observed
strong linear relationship between needle nitrogen per area
(Na) and irradiance (Brooks et al. 1996, Niinemets 1997a).
Although changes in needle anatomy are associated with increases in Na with increasing irradiance in P. abies, needle
nitrogen per dry mass (Nm) increases with decreasing irradiance in this species (Niinemets 1997a). This preferential allocation of nitrogen to needles at low irradiances improves the
efficiency of light interception, which is expensive in terms of
nitrogen (Evans and Seemann 1989).
Recent studies on the acclimation of older sun foliage to
shading have demonstrated that morphological adjustments in
leaf structure, which optimize carbon assimilation of currentyear needles, are not reversible (Brooks et al. 1994, 1996). As
a tree canopy gains size, needles developed in a particular light
regime will be increasingly shaded by newly expanding
branches and foliage. Therefore, the morphological structure
of needles that are ≥ 1-year-old will almost always be more or
less unmatched to the prevailing irradiance. Although these
architectural insufficiencies may partly be compensated for by

changes in needle biochemical machinery----e.g., chlorophyll
concentration in older needles responds to increased shading
on a time-scale of months (Brooks et al. 1994)----needle acclimation to shading is likely to require reallocation of nitrogen
to thylakoid proteins within the needle as well as enhanced
nitrogen concentrations in foliage. However, with increasing
age, needle nitrogen content becomes progressively decoupled
from shading and the concentration of needle nitrogen decreases (Gower et al. 1989, Schoettle 1989, Everett and Thran
1992, Helmisaari 1992). The age-dependent decline in needle
nitrogen may seriously limit the potential of older sun-adapted
needles to acclimate to shade conditions.
To gain insight into the interrelationships between needle
life span and the adaptive modifications in needle structure to
past and current light conditions, I studied the demography of
needles, and their morphology and chemical composition in
the evergreen conifer, P. abies. The following hypotheses were
tested: (1) needle longevity is related to light conditions;
(2) older foliage responds to decreased irradiance in the same
manner as young foliage; and (3) needle morphology and life
expectancy depend on the irradiance conditions prevailing
when the needles were formed.

Material and methods
Characteristics of the study trees
The research was conducted in a planted 33-year-old P. abies
stand located on a plateau-like crest of a hill with podzolic and
brown pseudopodzolic soils formed on phyllite at Oberwarmensteinach (49°59′ N, 11°47′ E; elevation about 760 m above
sea level), Fichtelgebirge, Germany (Hantschel 1987, Türk
1992) in September--October 1991. The study was carried out
in an unthinned part of the stand. The 0.25-ha plot had a
density of about 8000 stems ha −1 with tree heights ranging
from 1 to 8 m. Additional shading was provided by neighboring P. abies trees, about 100 years old and 25 m high, and

several Fagus sylvatica L. trees, about 40 years old and 15 m
high, so that relative irradiance (proportion of open sky) above
the tree crowns was rarely greater than 0.3.
Thirty trees that differed in vigor and exposure to sun were
selected. Although tree size generally alters foliar structure
(e.g., Niinemets and Kull 1995a, 1995b, Niinemets 1997a), the
effect was not significant in the current study (P > 0.05),
probably because all of the sampled trees were within a height
range of only 2.4 to 4.9 m (mean ± SE = 3.39 ± 0.14).

Estimation of irradiance conditions
Variation in relative irradiance (RI) among trees and among
sampling locations was quantified by a hemispherical photographic technique (Anderson 1964). The photographs were
analyzed according to Nilson and Ross (1979). Relative
amount of penetrating diffuse solar radiation (RI) was calculated for uniformally overcast sky conditions from the relative
area of canopy gaps measured from hemispheric photographs
and corrected for cosine of incidence effects. The RI is an
index that varies from 0 to 1. An RI of 1.0 corresponds to the
diffuse irradiance of open sky, and an RI of zero corresponds
to complete shade with no penetrating canopy gaps (cf. Salminen et al. 1983).
Demographic study
Because maximum foliage age may be a good estimate of
mean foliage age (Kohyama 1980, Koike et al. 1994), I studied
variability in maximum needle age (NAmax ) across tree crowns.
Picea abies has a deterministic growth pattern and produces
only one flush of needles annually, so that it was possible to
follow the growth history of a branch in a given whorl by
examining the bud scale scars on branch axes. However, to
convert these observations to an absolute time-scale, it was
necessary to identify the chronological age of whorls. Thus,

the first step in foliage census was to determine the year of
formation of every whorl of each tree. From every needled
whorl, one to four representative branches were further chosen
for determination of NAmax . The NAmax for a given whorl,
NAmax (W), was calculated as the mean of the estimates of all
sampled branches on the whorl. Only green and securely
attached needles were included in estimations of NAmax . Altogether over 1000 branches were examined in 30 trees. Currentyear needles were assigned an age of 0.
There was a common tendency for all needle-age classes to
be present in the upper canopy. The distribution of NAmax (W)
leveled off in the mid-canopy and decreased with canopy depth
thereafter (see Figure 1). The distribution of maximum needle
age was fitted with the Weibull function (Mori and Hagihara
1991, Niinemets 1996):
u × m  (W c+1) − W 
NAmax (W ) =


α 
α


m−1

 (W c + 1) − W 

e− 
α


m

,

(1)

where Wc is the year of formation of the current-year whorl, W
is whorl number (year of formation), α, m and u are constants.
A nonlinear least-square fit of Equation 1 to the measured
values gave r 2 from 0.907 to 0.997 (averaging 0.971; Figure 1).

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725

ences in irradiance between whorls were accounted for (oneway ANCOVA), but W was occasionally more strongly correlated with foliar parameters than RI in older needles.
Foliage structure and chemical composition

Figure 1. Sample fit of the distribution of maximum needle age at a
given whorl, NAmax (W), in P. abies. Distribution of NAmax (W) was
fitted by a Weibull function (Equation 1) using a nonlinear least
squares routine. Maximum needle age for the tree was estimated by
Equation 1 using the age distribution maximum.

To obtain an estimate of maximum needle age for the tree, the
distribution maximum (NAmax ′(W) = 0, solved for W, see also
Figure 1) was derived as:
1

Wmax

1 m

= (Wc + 1) − α 1 −  .
m



Total needle surface area (TLA) and needle volume (V ) were
calculated from measurements of needle thickness (D1), width
(D2) and length (L) according to Niinemets and Kull (1995b).
Needles were weighed after drying the samples at 70 °C for at
least 48 h, and needle dry mass per TLA (LMA) was calculated. The LMA was further expressed as the product of
V/ TLA and needle density (ND, dry mass per volume)
(Witkowski and Lamont 1991, Niinemets and Kull 1995b,
Niinemets 1997a):
LMA =

V
ND .
TLA

(3)

Foliar carbon (Cm) and nitrogen (Nm) concentrations were
determined with a C/N analyzer (Model 1500, Carlo Erba,
Italy). Concentrations of ethanol-soluble carbohydrates (ESC)
and starch (SC) were determined by anthrone reaction as
described previously (Niinemets 1995, 1997a).
Parameters for nonstructural carbohydrate-free dry mass

(2)

Substitution of Wmax into Equation 1 gave NAmax for the whole
tree. Maximum needle age calculated by Equations 1 and 2
was correlated with highest needle age for all sampled
branches per tree (r 2 = 0.68, P < 0.001).
An estimate of relative irradiance (RI) for each tree was
obtained from RI measurements just above the canopy (RIa)
and below the canopy at distances of 0.1 m and 1.2 m from the
stem in both the north and south compass directions (RIb0.1 and
RIb1.2 , respectively). The RIb0.1 (0.136 ± 0.011) was significantly lower (paired t-test, P < 0.01) than either RIa (0.169 ±
0.015) or RIb1.2 (0.157 ± 0.011); however, RIa and RIb1.2 were
not statistically different (P > 0.5). Relative irradiance for the
tree was computed as [RI a + (RIb0.1 + RIb1.2 ) /2]/2 .
Needle sampling for examination of foliage structure and
chemical composition
Foliar samples of current-year and 1- and 2-year-old needles,
consisting of 10--20 needles per age-class, were taken from the
southern aspect of terminal branch positions from the fourth
whorl from the top. To allow needle expansion to reach completion and needle mineral content to stabilize (Weikert et al.
1989, author’s unpublished observations), sampling was conducted between 1500 and 1600 h on cloudy days during
3 weeks in October 1991. Hemispheric photographs were
taken immediately after foliage sampling. To get a more extensive gradient in RI, needle samples were in several cases
collected also across the crown from different whorls. There
were no consistent effects of whorl age on foliage morphology
and chemical composition in current-year needles when differ-

There is evidence that the size of the foliar nonstructural
carbohydrate (NSC, ethanol-soluble carbohydrates plus starch)
pool varies with needle age in P. abies (Einig and Hampp
1990), resulting in a parallel variation in foliar mass per area
(e.g., Chatterton et al. 1972) and the concentrations of other
leaf components (Plhák 1984). Therefore, LMA, ND and the
concentrations of leaf chemicals were also expressed on the
basis of NSC-free dry mass (Wong 1990). Needle dry mass
per area and ND were multiplied by 1 − TNC (where
TNC = ESC + SC , expressed here as the proportion of dry
matter) to obtain LMA and ND on the basis of NSC-free dry
mass (LMAc and NDc, respectively). Leaf nitrogen content
expresssed on an NSC-free dry mass (Ncm) was obtained by
dividing Nm by 1 − TNC. Foliar carbon content expressed on
the basis of NSC-free dry mass was calculated as:
C cm =

C m − NCC
,
1 − TNC

(4)

where NCC is the proportion of leaf carbon in NSC.
Statistical analysis
Linear correlation and regression techniques were used to
analyze the relationships between needle morphological and
structural parameters as well as the dependencies of these
parameters on irradiance within an age-class. Differences between age-classes were separated by the Bonferroni test after
one-way analysis of variance. If RI significantly affected the
dependent variable, it was included as a covariate in the statistical model. All effects were considered significant at P < 0.05
(Wilkinson 1990).

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NIINEMETS

distribution maximum, Wmax , and NAmax were also correlated
(r = −0.76, P < 0.001).

Results
Demographic study
The oldest needles were generally located in the middle of the
living canopy (Figure 1), but maximum needle age was greater
in shaded trees than in sun-exposed trees (Figure 2). Light
availability also influenced maximum longevity of needles in
different whorls. The age distribution maximum (Wmax , Equation 2) tended to shift upward with increasing irradiance
(r 2 = 0.27), indicating that progressively younger annual shoot
segments were defoliated at greater RIs (cf. Figure 1). The age

Relationships of needle morphology and chemical
composition with irradiance in current-year needles
Because ND was independent of RI (P > 0.3), the increase in
LMA with increasing RI was attributable to increases in needle
width (P < 0.001) and volume to total area ratio (Figure 3).
The concentrations of ethanol-soluble carbohydrates and
starch were weakly correlated with relative irradiance
(r 2 = 0.09, P < 0.01 for ESC and r 2 = 0.06, P < 0.05 for SC,
n = 105). These positive relations were more significant with
LMA (r 2 = 0.52, P < 0.001 for ESC and r 2 = 0.08, P < 0.01 for
SC). Needle nitrogen concentration was negatively correlated
with RI (r 2 = 0.12, P < 0.001) and LMA (Figure 4). Despite
this, nitrogen content expressed on a TLA basis (Na) was
positively correlated with both RI (r 2 = 0.19, P < 0.01) and
LMA (Figure 4), signifying the overwhelming importance of
modifications in foliar morphology (Na = NmLMA) for the
adjustment of foliar resources toward efficient use of different
light microclimatic conditions. Expression of the variables on
an NSC-free dry mass did not alter the conclusions qualitatively (data not shown).
Dependencies of needle morphology and chemical
composition on irradiance in 1- and 2-year-old foliage

Figure 2. Dependence of maximum needle age per tree (NAmax ) on
relative irradiance. Relative irradiance was calculated from estimates
of relative irradiance above and below the tree canopy.

Needle age affected the relationships between morphological
variables and irradiance qualitatively. In contrast to currentyear foliage, neither needle width (P > 0.3), V/TLA (Figure 3)

Figure 3. Relationships between needle dry mass per total area (LMA), volume to total area ratio (V/TLA) and relative irradiance. The V/TLA
ratio describes the needle morphology-related variation in LMA (Equation 3). s = current-year needles, d = 1-year-old needles, and m =
2-year-old needles.

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IRRADIANCE, NEEDLE AGE AND NEEDLE STRUCTURE IN PICEA

727

Figure 4. Correlations between LMA and amounts of needle nitrogen per needle dry mass (N m), and per total surface area (Na). Coefficients for
the hyperbolic relationships between Nm and LMA were obtained from the linear relationships between N a and LMA (Na = aLMA + b,
Nm = b/LMA + a). The intercept denoted by the asterisk did not differ significantly from zero.

nor LMA (Figure 3) was related to irradiance in 1- and 2-yearold needles. Despite the independence of RI and LMA in 1and 2-year-old needles, whorl number and LMA were positively correlated in older needles (r 2 = 0.25, P < 0.001 for
1-year-old and r 2 = 0.15, P < 0.02 for 2-year-old needles),
indicating that previous rather than actual light climate determined LMA in older needles. Needle density was not dependent on irradiance in old foliage (P > 0.7).
The concentrations of ethanol-soluble carbohydrates and
starch were not correlated with irradiance in 1-year-old needles (P > 0.3 for both), but they were positively influenced by
RI in 2-year-old needles (r 2 = 0.24, P < 0.005 for ESC and
r 2 = 0.21, P < 0.005 for SC). Both ESC and SC were positively
correlated with LMA in 1-year-old needles (r 2 = 0.21, P < 0.01
for ESC and r 2 = 0.10, P < 0.05 for SC), but not in 2-year-old
needles (P > 0.05). In 1-year-old needles, Nm was negatively
related to LMA (Figure 4) and independent of RI (P > 0.4), but
it was dependent on RI (Figure 5) and independent of LMA in
2-year-old needles (Figure 4). The conclusions were not qualitatively altered by using the parameters for NSC-free dry mass.
Age effects on needle structure
Needle dry mass per TLA increased with increasing needle age
(Table 1). This was attributable to greater needle density,
needle thickness and needle width in older needles (Table 1).
The increase in NSC content with needle age paralleled the
increase in ND. Therefore, when ND was calculated per NSCfree dry mass (NDc ), it did not differ between the age-classes
(Table 1). However, as a result of contrasting needle morphol-

Figure 5. Effect of relative irradiance on needle nitrogen content per
total dry mass, Nm (%), in 2-year-old needles.

ogy, both LMA and LMAc were greater in older needles than
in current-year needles (Table 1).
Analysis of the increase in NSC with needle age indicated
that ESC varied little between age-classes, whereas starch
concentration increased with needle age in parallel with the
increase in NSC (Table 1). Although NSC did not only alter
needle density, it diluted other leaf compounds, and most of the
decline in needle nitrogen concentration during aging was
atttributable to the accumulation of NSC (Table 1). Inasmuch
as needle carbon concentration increased with increasing age,
a larger fraction of carbon-rich compounds in older needles
may also have diluted other leaf chemicals, in particular leaf
nitrogen (Table 1). For the whole material, Nm was negatively

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NIINEMETS

Table 1. Needle chemical composition and morphology in relation to needle age 1.
Variable

Mean ± SE

Definition (unit)

Current-year needles
Cm
C cm
D1
D2
ESC
L
LMA
LMAc
Na
Nm
Ncm
ND
NDc
SC
TNC
TLA
V
V/TLA
1
2

Carbon per total dry mass (%)
Carbon per NSC2-free dry mass (%)
Thickness (mm)
Width (mm)
Ethanol-soluble carbohydrates per
total dry mass (%)
Length (mm)
Total dry mass per TLA (g m −2)
NSC-free dry mass per TLA (g m −2)
Nitrogen per NSC-free dry mass (g m −2)
Nitrogen per total dry mass (%)
Nitrogen per NSC-free dry mass (%)
Density (total dry mass per V, g cm −3)
NSC-free dry mass per V (g cm −3)
Starch per total dry mass (%)
ESC + SC (%)
Total area (mm2)
Volume (mm3)
V to TLA ratio (mm3 mm −2)

1-Year-old needles

2-Year-old needles

47.79 ± 0.14 a
48.57 ± 0.19 a
0.948 ± 0.022 a
0.446 ± 0.014 a
4.86 ± 0.24 a

48.17 ± 0.15 ab
49.04 ± 0.21 a
0.995 ± 0.019 a
0.480 ± 0.011 a
5.53 ± 0.27 b

48.56 ± 0.16 b
49.75 ± 0.19 b
1.080 ± 0.016 b
0.570 ± 0.013 b
6.17 ± 0.29 b

13.16 ± 0.24 a
36.3 ± 0.9 a
33.3 ± 0.8 a
0.705 ± 0.018 a
1.866 ± 0.030 a
2.105 ± 0.034 a
0.365 ± 0.005 a
0.324 ± 0.005 a
6.72 ± 0.36 a
11.61 ± 0.48 a
27.9 ± 1.0 a
2.88 ± 0.19 a
0.1002 ± 0.0027 a

13.34 ± 0.31 a
41.2 ± 0.8 b
36.1 ± 0.7 a
0.704 ± 0.013 a
1.773 ± 0.023 b
2.037 ± 0.033 a
0.377 ± 0.005 a
0.328 ± 0.004 a
8.10 ± 0.23 b
13.82 ± 0.42 b
29.7 ± 1.0 ab
3.26 ± 0.15 a
0.1077 ± 0.0022 a

13.22 ± 0.30 a
48.3 ± 1.1 c
40.5 ± 0.8 b
0.817 ± 0.019 b
1.726 ± 0.026 b
2.029 ± 0.034 a
0.385 ± 0.006 b
0.322 ± 0.005 a
10.20 ± 0.33 c
16.30 ± 0.46 c
32.5 ± 1.0 b
4.13 ± 0.18 b
0.1255 ± 0.0026 b

Means designated by the same letter are not significantly different (P > 0.05). Data were subjected to ANOVA and the means separated by the
Bonferroni test. An ANCOVA (common slope model) was used if relative irradiance significantly altered the model at P < 0.05.
NSC = Nonstructural carbohydrates (ethanol-soluble carbohydrates + starch).

correlated with both carbon (r 2 = 0.15, P < 0.001) and nonstructural carbohydrate concentrations (r 2 = 0.13, P < 0.001).

Discussion
Changes in needle structure, composition and life span in
relation to irradiance
The finding of increased needle longevity in P. abies growing
in environments with low irradiance (Figure 2) is in agreement
with other studies showing that stressful environments, e.g.,
high altitude (Schoettle 1990, Reich et al. 1996) or low-light
habitats, result in an increase in leaf life span. Chabot and
Hicks (1982) hypothesized that leaf longevity should adjust to
amortize the costs of leaf construction. Although Williams
et al. (1989) rejected this hypothesis, they demonstrated a
positive relationship between leaf life span and its payback
time. Inasmuch as lower carbon gain under limited irradiances
results in a longer payback time, leaf life span should be
greater at low irradiance. Although this relationship appears to
hold in P. abies (Figure 2), the correlation between longevity
and payback time alone provides no insight into why sunadapted needles abscise earlier than shade-adapted needles.
The explanation may lie in the light acclimation process itself.
There are two components of the needle’s response to its light
environment: acclimation to irradiance during its primary
growth, and its ability to adjust as the light environment
changes. Many adaptations of leaf structure and function to
irradiance are irreversible (Brooks et al. 1994, 1996). Furthermore, the light environment for needles that developed in a

high-light regime changes more quickly than that for needles
that developed in shade. Therefore, the lower life expectancy
of sun needles compared with shade needles may largely
depend on their low potential to adjust to shade and on the time
constraints imposed on the acclimation process.
Generally, needle thickness increases with increasing irradiance in conifers (Aussenac 1973, Tucker and Emmingham
1977, Sprugel et al. 1996, Niinemets 1997a); however, in
P. abies, needle width is considerably more responsive to irradiance than needle thickness (Aussenac 1973, Greis and Kellomäki 1981, Niinemets and Kull 1995b, Niinemets 1997a).
Because needle density is not correlated with irradiance in
P. abies (Niinemets and Kull 1995b, Niinemets 1997a), the
light-induced changes in needle width underlie the correlation
between V/TLA and LMA in current-year needles (Figure 3,
Equation 3). Adaptation to low irradiance seems also to involve
modifications in leaf chemical composition as indicated by the
increases in foliar nitrogen concentrations with decreasing
irradiance (Figures 4 and 5, Niinemets 1997a).
Because the nitrogen requirement increases disproportionately with increasing leaf absorptance (Evans and Seemann
1989), it has been hypothesized that this pattern of nitrogen
distribution represents an investment strategy inherent to
shade-tolerant species (Kull and Niinemets 1993, Niinemets
1995, 1997a, 1997b). Because chlorophyll concentrations
(Heinze and Fiedler 1976) and photosynthetic capacity per
needle dry mass (Schulze et al. 1977) increase with decreasing
relative irradiances in P. abies, I postulate that the extra nitrogen is invested in compounds that improve light interception
of incident irradiance as well as in needle compounds that

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IRRADIANCE, NEEDLE AGE AND NEEDLE STRUCTURE IN PICEA

improve the utilization of intercepted light. High concentrations of NSC concentration at high irradiances is compatible
with earlier results for this species (Einig and Hampp 1990,
Niinemets 1997a) and other conifers (Gholz and Cropper
1991). A positive relationship between NSC and irradiance
probably results from increased daily photosynthetic production at high irradiances (Hendrix and Huber 1986, Niinemets
1995).
Changes in needle morphology with aging
Increasing LMA with increasing needle age (Tucker and Emmingham 1977, Benecke 1979, Borghetti et al. 1986, Ohmart
and Thomas 1986, Oren et al. 1986, Gower et al. 1989, Gilmore et al. 1995) is a central modification in needle structure.
Expression of LMA as the product of needle density and
V/ TLA ratio (Equation 3) appears useful for a mechanistic
understanding of the causes and effects of the age-related
changes in LMA. In most cases, changes in needle density
(Beets 1977, Tucker and Emmingham 1977, Shelton and
Switzer 1984, Whitehead et al. 1994) underlie the increase in
LMA with aging in conifers. However, in the current study,
changes in needle width and thickness (Table 1) also contributed toward the increase in LMA with increasing needle age.
Because LMA of older needles was significantly larger in
whorls that were previously exposed to higher irradiance, the
lack of correlation between LMA and irradiance in older
needles (Figure 3) may be associated with the adaptation of
needle morphology to preceding rather than to prevailing light
climate. Similarly, LMA in Pinus radiata D. Don was independent of depth in the canopy for needles ≥ 2 years old,
whereas it was related to canopy position in younger needles
(Ohmart and Thomas 1986). However, in many conifers, e.g.,
Pinus radiata (Benecke 1979) and Pinus sylvestris L. (van
Hees and Bartelink 1993), LMA of older needles is related to
depth in the canopy. By the same token, LMA of older needles
is dependent on irradiance in Pseudotsuga menziesii (Mirb.)
Franco (Del Rio and Berg 1979) and P. abies (Koppel and Frey
1984). These data suggest either that the location of needles in
the crown is a poor estimate of actual light climate, or that the
lack of correlation between needle structure and irradiance in
the present study (Figure 3) was a consequence of the limited
range of irradiances examined.
Because the morphology of needles acclimated to high-irradiances has developed toward high photosynthesizing mass
per unit surface area in current-year needles (Figure 3; Niinemets and Kull 1995b, Niinemets 1997a) rather than to high
efficiency of light interception, the structure of sun-adapted
older needles becomes increasingly less advantageous as they
become shaded. Moreover, needle thickness and width increase with needle age (Table 1), probably as a result of
secondary phloem growth (Ewers 1982, Gilmore et al. 1995).
Because secondary growth does not affect needle length, it
leads to further reductions in the effectiveness of light interception, which is inversely related to needle thickness to length
ratio (Takenaka 1994).

729

Age effects on nitrogen partitioning
The priority of increasing efficiency of light interception gains
in relevance with aging and shading. Despite little flexibility
in adjusting sun-adapted needle architecture to shade conditions, the stoichiometry of needle chemicals can be modified
fairly rapidly in response to low irradiances (Brooks et al.
1994, Brooks et al. 1996). Thus, needle chlorophyll concentrations increase with increasing needle age (Linder 1972, Brooks
et al. 1994, Mandre and Tuulmets 1995), resulting in enhanced
light utilization efficiency (Teskey et al. 1984). Similarly, the
observed alterations in needle nitrogen partitioning with age
demonstrate (Figures 4 and 5, and Table 1) the potential for
acclimation of needle function toward lower quantum availabilities. Nitrogen allocation within leaves can be related to
lowered irradiance within a season (Brooks et al. 1994), however, as is suggested by the close association between nitrogen
in 1-year-old needles and previous light climate (cf. Figure 4),
the redistribution of foliar resources among needles occurs
over longer periods.
Aging and the stoichiometry of needle carbon constituents
Increases in nonstructural carbohydrates with increasing needle age (Table 1) have been observed in P. abies (Einig and
Hampp 1990, Egger et al. 1996) and Pinus elliottii Engelm.
(Gholz and Cropper 1991). Generally, a balance exists between carbon acquisition in photosynthesis and carbohydrate
export from leaves (Hendrix and Huber 1986). Thus, increasing concentrations of NSC with needle aging (Table 1) may be
related to decreasing activities of enzymes responsible for
carbon translocation (e.g., sucrose phosphate synthase; Hendrix and Huber 1986, Egger et al. 1996), or to a decreasing
ability of the phloem to export photosynthates from the needles. There is evidence that the increment of secondary growth
of phloem declines as needles age (Ewers 1982).
Because of the close correlation between foliage carbon and
energy contents (Walton et al. 1990), increasing needle carbon
content with increasing needle age (Table 1) agrees with previously observed greater heat of combustion of old foliage than
of young foliage in P. abies (Ivask 1983, Bobkova 1987), Pinus
contorta (Gower et al. 1989) and Pinus sylvestris (Bobkova
1987). According to Frey (1981), lignification of the needle
hypodermis proceeds until at least the third year of development. Given the high carbon concentration of lignin (65.4%,
calculated according to Freudenberg 1965), continued lignification may account for the increased carbon concentrations
during needle aging. If the accumulation of lignin is the cause
for the observed changes in Cm, its concentration should increase by 2.6% to explain the difference in carbon concentration between 0- and 2-year-old needles. Correcting for NSC
deposition, lignin concentration should increase by 3.6%.
There may be a feedback link between NSC accumulation and
increased Cm, because limited usage of nonstructural carbohydrates promotes the production of carbon-rich secondary metabolites such as lignin or terpenes (Chapin 1991).

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730

NIINEMETS

Interactive effects of current and past light climate on needle
function
Age-related changes in the concentration of needle chemicals,
which are responsible for light capture and photosynthetic
function, indicate that aging may be a crucial factor in setting
constraints on subsequent shade acclimation. Besides lesions
that accumulate over time (cf. Sutinen 1987), availability of
needle chemicals for acclimation to shade also decreases with
aging. In this respect, it may be the initial adaptation state,
rather than needle chronological age, that is the primary factor
influencing needle acclimation and longevity.
Preferential abscission of the most shaded needles may
improve the capacity for light interception of the remaining
needles, especially in sun shoots that not only have more
needles per unit stem length than shade shoots (Niinemets and
Kull 1995a) but also have higher self-shading within the shoot.
The observed age-related changes in shoot morphology are in
good agreement with the hypothesis that needles in unfavorable positions in terms of light interception become selectively
abscised (Norman and Jarvis 1974, Oker-Blom and Smolander
1988).
Acknowledgments
The study was supported by a scholarship from the German Academic
Exchange Service (DAAD) and by the German Federal Minister of
Research and Technology (BMFT) under Grant BEO 51-0339476A
(BITÖK, University of Bayreuth). I am grateful to Riho Kôiveer
(Department of Plant Biochemistry, University of Tartu, Estonia) for
providing facilities for carbohydrate analysis.
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