Tree Physiology 22, 515–535
© 2002 Heron Publishing—Victoria, Canada
Stomatal conductance alone does not explain the decline in foliar
photosynthetic rates with increasing tree age and size in Picea abies
and Pinus sylvestris
ÜLO NIINEMETS
Department of Plant Physiology, Institute of Molecular and Cell Biology, University of Tartu, Riia 23, 51011 Tartu, Estonia ([email protected])
Received February 26, 2001; accepted November 30, 2001; published online May 1, 2002
Summary Foliar light-saturated net assimilation rates (A)
generally decrease with increasing tree height (H) and tree age
(Y), but it is unclear whether the decline in A is attributable to
size- and age-related modifications in foliage morphology
(needle dry mass per unit projected area; MA), nitrogen
concentration, stomatal conductance to water vapor (G), or
biochemical foliage potentials for photosynthesis (maximum
carboxylase activity of Rubisco; Vcmax). I studied the influences
of H and Y on foliage structure and function in a data set consisting of 114 published studies reporting observations on
more than 200 specimens of various height and age of Picea
abies (L.) Karst. and Pinus sylvestris L. In this data set, foliar
nitrogen concentrations were independent of H and Y, but net
assimilation rates per unit needle dry mass (AM) decreased
strongly with increasing H and Y. Although MA scaled positively with H and Y, net assimilation rates per unit area (AA =
MA × AM) were strongly and negatively related to H, indicating
that the structural adjustment of needles did not compensate for
the decline in mass-based needle photosynthetic rates. A relevant determinant of tree height- and age-dependent modifications of A was the decrease in G. This led to lower needle
intercellular CO2 concentrations and thereby to lower efficiency with which the biochemical photosynthetic apparatus
functioned. However, Vcmax per unit needle dry mass and area
strongly decreased with increasing H, indicating that foliar
photosynthetic potentials were lower in larger trees at a common intercellular CO2 concentration. Given the constancy of
foliar nitrogen concentrations, but the large decline in apparent
Vcmax with tree size and age, I hypothesize that the decline in
Vcmax results from increasing diffusive resistances between the
needle intercellular air space and carboxylation sites in chloroplasts. Increased diffusive limitations may be the inevitable
consequence of morphological adaptation (changes in MA and
needle density) to greater water stress in needles of larger trees.
Foliage structural and physiological variables were nonlinearly
related to H and Y, possibly because of hyperbolic decreases in
shoot hydraulic conductances with increasing tree height and
age. Although H and Y were correlated, foliar characteristics
were generally more strongly related to H than to Y, suggesting
that increases in height rather than age are responsible for declines in foliar net assimilation capacities.
Keywords: dry mass per unit area, foliar area, leaf structure,
nitrogen, photosynthetic capacity, photosynthetic electron
transport, Rubisco activity, stand age.
Introduction
Both single-leaf measurements (Miller et al. 1991, Donovan
and Ehleringer 1992, Grulke and Miller 1994, Schoettle 1994,
Yoder et al. 1994, Fredericksen et al. 1995, 1996, Hubbard et
al. 1999, but see Bauerle et al. 1999) and whole-plant water
flux estimations (Köstner et al. 1996, Hubbard et al. 1999,
Ryan et al. 2000, Schäfer et al. 2000) demonstrate that foliar
stomatal conductances are consistently lower in larger and
older trees than in smaller and younger trees in common environmental conditions. Lower stomatal conductance in taller
trees has been explained by greater water limitations as a consequence of a larger restriction to water flow from soil to
leaves because of increased path lengths in stems and branches
of taller trees (Ryan and Yoder 1997, Bond and Ryan 2000,
Mencuccini and Magnani 2000). There is evidence of age-related anatomical adjustments in xylem architecture, such as
increases in conduit diameter and length (Rumball 1963,
Pothier et al. 1989a, Mencuccini et al. 1997)—changes that
collectively improve the water transport capacity per unit
cross-sectional xylem area of constant length—as well as evidence of increases in cross-sectional xylem area per unit total
foliar area with increasing tree size (Becker et al. 2000b, Magnani et al. 2000, Schäfer et al. 2000, but see Coyea and Margolis 1992). However, there is also conclusive evidence that
whole-plant hydraulic conductances (total water flow rate per
unit of pressure difference in plants of various heights) are
generally lower in larger trees because of greater path lengths
(Pothier et al. 1989b, Mencuccini and Grace 1996a, 1996b,
Hubbard et al. 1999, Mencuccini and Magnani 2000). Thus,
homeostatic adjustments in xylem architecture and increases
in conductive area per unit transpiring foliar area are not sufficient to avoid greater water limitations in larger trees.
An important consequence of lower stomatal conductance
of taller trees is lower net assimilation rates because of lower
intercellular CO2 concentrations (Ci; Donovan and Ehleringer
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NIINEMETS
1992, Grulke and Miller 1994, Yoder et al. 1994, Fredericksen
et al. 1996, Hubbard et al. 1999). The decline in foliar photosynthesis resulting from lower Ci has been proposed (Ryan
and Yoder 1997, Bond 2000) as the primary cause of decreases
in forest net primary production with increasing stand height
and age (Gower et al. 1996, Ryan et al. 1997). However, studies demonstrating simultaneous decreases in foliar stomatal
conductance and net assimilation rate with increasing tree
height and age have not analyzed whether the observed decline
in stomatal conductance is sufficient to explain the decreases
in foliage photosynthesis and stand productivity. Such an analysis is called for, because there is evidence of tree height- and
age-related declines in foliage assimilative capacity at constant Ci (Kull and Koppel 1987, Miller et al. 1991, Grulke and
Miller 1994). When both stomatal conductance and photosynthetic capacity decline in parallel with increasing stand height
and age, decreases in stomatal conductances are not necessarily the cause of reduced foliar net assimilation rates.
Apart from physiological characteristics, foliage chemistry
and morphology also change with increasing tree size. Foliar
nitrogen concentrations are often lower in older and taller
stands (Peterson 1961, Höhne 1964, Schoettle 1994, Gower et
al. 1996, Niinemets 1997b). Such decreases in nitrogen concentrations may limit the formation of high-capacity photosynthetic apparatus in foliage of tall trees. In addition, leaves
of taller trees have a greater dry mass per unit area (Linder
1985, Chazdon 1986, Kull and Niinemets 1993, Schoettle
1994, Niinemets and Kull 1995, Niinemets 1997b), and may
be more lignified (Niinemets 1997c). These foliar modifications in taller trees may increase tolerance of low water potentials (Niklas 1989, 1991, Niinemets 2001), but they may also
decrease the CO2 diffusion conductance from the intercellular
air space to carboxylation sites in the chloroplasts (Parkhurst
1994, Syvertsen et al. 1995, Hanba et al. 1999). Thus, leaves of
taller trees may function at a lower chloroplast CO2 concentration than leaves of smaller trees.
In this study, foliage chemical, structural and photosynthetic data were analyzed in two conifer species, Picea abies
(L.) Karst. and Pinus sylvestris L. A large literature-based data
set covering 126 stands of various height and age was composed to: (1) generalize tree age- and height-related patterns in
foliar nitrogen concentrations and foliar structure; (2) gain
insight into mechanisms underlying variation in foliar net assimilation rates with increasing tree size, in particular, to distinguish between stomatal and biochemical limitations to photosynthesis; and (3) acquire conclusive evidence of whether
tree height or age controls the modification in foliage structure
and function. Finally, I studied whether the responses of foliar
structure and physiology to tree size and age differ qualitatively between species of contrasting ecological requirements,
and whether the kinetics of species responses differ. Picea
abies is a late-successional species that generally thrives only
on fertile soils (Brunner et al. 1999) with a large water-holding
capacity. Pinus sylvestris is an early-successional pioneer species growing over a wide range of habitats differing in soil fertility and water availability.
Data sources
The current synthesis of photosynthetic and morphological
data for P. abies and P. sylvestris is based on 114 published
studies that were conducted mainly in natural or planted stands
of varying tree age and size, although a few were conducted
with seedlings or saplings grown in growth chambers under
controlled conditions (see Appendix 1 for data sources). Data
for P. abies originated from 74 stands, and the data for P. sylvestris were from 52 stands. In addition, six growth chamber
studies with each species were considered (Appendix 1). Because in some stands a number of different tree age or size
classes were sampled, and the data were repeatedly collected
from the same stands in various years, the total number of data
points available was 125 for P. abies and 80 for P. sylvestris.
The availability of photosynthetic rates at saturating irradiance (measurement quantum flux density > 700 µmol m –2
s –1) and information on climatic conditions in the gas exchange cuvette during measurements (CO2 concentration,
temperature of needles) was the primary criterion for inclusion
of a study in the database. A few investigations providing information on foliar morphological variables and nutrient concentrations in stands of various ages were also incorporated. In
the case of experimental whole-plant studies, e.g., CO2, ozone,
temperature, and nutrient and water availability treatments,
only the control treatments were used.
Measurements of foliar gas exchange characteristics conducted at needle temperatures below 15 °C and above 30 °C
were excluded from the database. The included needle temperatures ranged from 15 to 27.5 °C (mean ± SD = 20.5 ± 2.6) in
P. abies and from 15 to 30 °C (mean ± SD = 21.8 ± 3.0) in
P. sylvestris. Because, at current ambient CO2 concentrations,
the net assimilation versus leaf temperature response curve
has a flat maximum around 15–30 °C in temperate species
(Berry and Björkman 1980), I suggest that the residual error in
foliar gas exchange versus tree size relationships resulting
from the variability in foliar temperatures is relatively minor.
Because large trees are generally exposed to higher light
availabilities than smaller trees, and such variability may lead
to confounding effects of size and light availability (Niinemets
and Kull 1995, Niinemets 1997b), I tried to keep the differences in long-term foliar light exposure between the trees of
varying size and age to a minimum. Thus, initially, only measurements from open-grown trees or from the upper unshaded
canopy were included in the database. However, few measurements had been taken from the full light-acclimated foliage
from the top of the trees. Given that relationships between
light availability and leaf morphology or physiology tend to be
curvilinear rather than linear, with changes in foliar characteristics progressively less at higher irradiances (e.g., Niinemets
and Kull 1998), the revised threshold for inclusion in the database was set equal to the light availability at the mid-canopy
level, i.e., 30% of daily integrated quantum flux density (Qint;
see Niinemets et al. 1998a) for the shade-tolerant species
P. abies and 50% for the shade-intolerant species P. sylvestris.
Nevertheless, more than 75% of all sample points received
more than 50% of above-canopy light in P. abies. Assuming
that the seasonal mean above-canopy Qint in temperate forests
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DECLINE IN PHOTOSYNTHETIC CAPACITY WITH TREE AGE AND SIZE
is 35–40 mol m –2 day –1 (Niinemets et al. 1998a, 1999a), the
corresponding threshold for above-plant Qint for the growth
chamber studies was taken to be 11 mol m –2 day –1 for P. abies
and 18 mol m –2 day –1 for P. sylvestris. Although there was a
weak positive correlation between total tree height and Qint
(r 2 = 0.14, P < 0.05) among the data for which exact measurements of Qint were available, Qint and tree age were not related
(r 2 = 0.02, P > 0.3). Given the weak correlations, I conclude
that covariation of tree dimensions and age with foliar exposure did not play a significant role in the relationships between
foliar structural or physiological variables and tree size or age.
Distribution of the stands
The P. abies and P. sylvestris stands were distributed over a
wide geographic gradient of more than 20 degrees of latitude
in the northern hemisphere (Appendix 1). The northernmost
stand of P. abies was at Åheden, Sweden (64°14 N, 19°46 E;
Bauer 1997) and the northernmost stand of P. sylvestris was at
Värriö, Finland (67°46 N, 29°35 E; Luoma 1997, Aalto
1998, Palmroth et al. 1999). In addition to a P. abies stand in
the southern hemisphere at Craigieburn, New Zealand (43°9
S, 171°43 E; Schulze et al. 1990, Zimmermann 1990), the
southernmost location of P. abies in the northern hemisphere
was at Monte di Mezzo, Italy (41°43 N, 14°18 E; Bauer
1997) and that of P. sylvestris was at Montesquíu, Spain (42°7
N, 2°12 E; Luoma 1997, Palmroth et al. 1999). Stands farther
south were generally also at greater altitudes, e.g., the altitude
of the stand in Monte di Mezzo was 950 m, whereas that in
Åheden was 350 m. The negative relationship between stand
altitude and latitude was significant for both species (for linear
regressions, r 2 = 0.34, P < 0.001 for P. abies, and r 2 = 0.27, P <
0.001 for P. sylvestris). Such elevational differences in northern versus southern locations moderate the gradient in climatic
conditions (i.e., temperature, precipitation) between stands at
various geographical locations. Although conifer morphology
and physiology may depend on long-term site climate, the
relationships observed thus far are weak (Luoma 1997, Niinemets 2001). Given the poor dependence of needle physiological and morphological variables on site climate, the possible
influences of long-term environmental conditions on foliage
structure and function are not considered here.
In this study, there was no correlation between tree height
and site latitude (r 2 = 0.02 for P. abies and r 2 = 0.04 for P. sylvestris) or longitude (r 2 = 0.05 for P. abies and r 2 = 0.02 for
P. sylvestris). Similarly, longitude and latitude were not correlated with tree age in either species (data not shown). Thus, the
observed relationships between foliar variables and tree size or
age are unlikely to be mediated by a bias in tree size and age
distributions with latitude or altitude.
Methods
Determination of tree height and age
In general, most studies provided values for both tree age and
height. Some studies reported estimates of either tree age or
height along with specific site quality indices (Daniel et al.
517
1979). Thus, the missing value of stand height or age was obtained by means of the site quality index from basic forestry
taxation tables (e.g., Krigul 1971 for the Russian stands).
In a few cases, the heights of 1- to 3-year-old seedlings were
calculated from their age using the data of Nilsson and Gemmel (1993; see also Mäkelä and Sievänen 1992) and assuming
an exponential growth phase and noncompetitive growth conditions.
Expression of foliar structural and photosynthetic variables
The literature provided either total- or projected-area based
values of needle dry mass and net assimilation rate. Generally,
in studies expressing the data per unit total needle area (S T),
projected needle area (SP) had actually been measured, and ST
was calculated from SP using a single literature-based S T /SP ratio for all needles investigated. However, the S T /SP ratio may
vary depending on the environmental conditions, especially in
P. abies (Niinemets and Kull 1995, Niinemets 1997b, Niinemets et al. 2001). Therefore, in the current study we expressed
all values of needle dry mass and net photosynthesis on a projected area basis, because SP was usually the measured variable. The same S T /SP ratio that was used in the original study
was employed to convert the values expressed on an S T basis
back to an SP basis. In P. abies, S T /SP ratios employed in various reports ranged from 2.38 (Schulze et al. 1977a, 1977b) to
2.68 (Keller and Wehrmann 1963) with the mode of 2.6 derived from the work of Oren et al. (1986). For P. sylvestris, the
S T /SP ratios varied from 2.18 (Keller and Wehrmann 1963,
Brunes et al. 1980) to 2.57 (Tirén 1926, Schulze and Küppers
1985, Lippu and Puttonen 1991, Luoma 1997), which was also
the value most frequently used. In a few cases, where ST was
measured directly, e.g., with the glass-bead method (Thompson and Leyton 1971, Koppel and Frey 1984), SP was computed from an S T/SP ratio of 2.6 for P. abies and 2.57 for
P. sylvestris.
Whenever needle dry mass per unit SP (MA) was available,
net assimilation rate and stomatal conductance to water vapor
could be computed both per unit dry mass and per unit projected needle area. Otherwise, either area- or mass-based values were available for the statistical analysis (Appendix 1).
Parameters of the needle photosynthesis model
Ribulose-1,5-bisphosphate (RUBP) carboxylation in photosynthesis is limited by either RUBP carboxylase/oxygenase
(Rubisco) activity, or the availability of RUBP (Farquhar et al.
1980, Farquhar and von Caemmerer 1982). The capacity of
Rubisco-limited photosynthesis is given by the maximum
carboxylase activity of Rubisco (Vcmax), and the RUBP-limited
photosynthesis is constrained by the maximum rate of photosynthetic electron transport (Jmax), which provides reductive
and energetic equivalents for RUBP regeneration. Both Vcmax
and Jmax are the key parameters that determine foliage photosynthetic rate at a certain Ci . At current ambient CO2 concentrations, net assimilation rates are generally limited by Vcmax at
high irradiance and by Jmax at low irradiance. Depending on
the data available, either Ci versus net photosynthesis (A) response curves, incident quantum flux density (Q) versus A
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curves, or single-point, light-saturated A values measured at
certain CO2 concentrations were used to derive estimates of
Vcmax or Jmax as described in Appendix 2. In all cases, Vcmax and
Jmax were standardized to a common temperature of 25 °C on
the basis of the shapes of the temperature dependencies of the
specific activity of Rubisco for Vcmax and the maximum rate of
chloroplastic electron transport per unit cytochrome f for Jmax,
as described in Niinemets and Tenhunen (1997).
Given that Vcmax and Jmax are strongly correlated in C3 plants
(Wullschleger 1993), and that considerably fewer values were
obtained for Jmax than for Vcmax, only the estimates of Vcmax are
reported here. Whenever a Jmax value was available, but Vcmax
was lacking, as in the measurements with an oxygen electrode
at saturating light and CO2 concentrations, the values of Jmax
were converted to Vcmax using mean ± SE Jmax/Vcmax ratios at
25 °C of 2.85 ± 0.14 mol mol –1 for P. abies and 2.38 ±
0.05 mol mol –1 for P. sylvestris. These Jmax /Vcmax ratios compare well with those observed in other C3 plants (Wullschleger
1993, Niinemets et al. 1998b).
Calculation of net assimilation rates from Vcmax values
A few studies reported only values of Vcmax, or initial slopes of
the CO2 response curve of net photosynthesis, which may be
used to calculate Vcmax (Equation A1). Because light-saturated
A is limited by Rubisco at current ambient CO2 concentrations, Vcmax may be used to compute an estimate of A at a certain Ci value (Equation A6) if the rate of mitochondrial
respiration in light (Rd; Equation A6, Figure A1) is known. In
addition to the correlation between A and Rd (Figure A1), the
mitochondrial respiration rate may be calculated as a fixed
proportion of Vcmax (Farquhar et al. 1980, Collatz et al. 1991,
Niinemets et al. 1998b). To find the scaling constant between
Rd and Vcmax (h) for P. abies and P. sylvestris in the current
study, I calculated a mean ratio of net assimilation rate at current ambient CO2 concentration to Vcmax (A/Vcmax) and used this
ratio to derive h from the regressions in Figure A1. Mean (±
SE) A/Vcmax ratios of 0.472 ± 0.021 and 0.309 ± 0.017 mol
mol –1 were obtained for P. abies and P. sylvestris, respectively,
giving h values of 0.0433 and 0.0229 mol mol –1 for P. abies
and P. sylvestris, respectively.
Net assimilation rates were calculated for Ci = 241 µmol
mol –1, which was the mean value over all data points. As the
regression analyses demonstrated, inclusion of these values of
A in the data set did not alter the conclusions of the statistical
significance of A versus tree age and height relations.
Photosynthetic nitrogen-use efficiency
The ratio of A to foliar nitrogen content was calculated as
an estimate of photosynthetic nitrogen-use efficiency (EN).
Among other determinants, the ratio characterizes the way that
leaves partition nitrogen to enhance light-saturated A. Photosynthetic nitrogen-use efficiency is high in leaves with high nitrogen investments in Rubisco and photosynthetic electron
transport components, and low in leaves with large nitrogen
investments in light-harvesting apparatus (Evans 1989, Evans
and Seemann 1989). However, EN is also dependent on stomatal constraints of photosynthesis, which may affect A by decreasing the CO2 concentration in the intercellular air space.
To characterize nitrogen investments in Rubisco (Niinemets
and Tenhunen 1997, Niinemets et al. 1998b), the ratio of Vcmax
to nitrogen content (Vcmax/N) was also computed. Like EN, the
Vcmax/N ratio indicates the efficiency with which foliar nitrogen is used to maximize A, but Vcmax/N is independent of stomatal limitations. Both EN and Vcmax/N could be calculated
only if data for N and A were available on the same basis of expression (nitrogen per unit dry mass if values of A were per
unit dry mass, and per unit projected area if values of A were
per unit projected area).
Consideration of needle age effects
Although I tried to include only measurements for currentyear needles (C) in the data set, some studies reported values
for foliar morphological and physiological characteristics for
1-year-old (C+1) or 2-year-old (C+2) needles only. Given that
needle age influences both foliar chemistry and structure
(Niinemets 1997a, Figures 1A and 1B) as well as photosynthetic potentials (Teskey et al. 1984, Figure 1C), the morphological and physiological characteristics of the C+1 and C+2
needles must be corrected for the age influences to reduce the
residual variance in the data set. To do this, studies reporting
foliar characteristics of various-aged needles of P. abies and
P. sylvestris were reanalyzed, and relative changes—i.e., the
Figure 1. Examples of the relationships between needle age
and the relative values of (A)
dry mass per unit area, (B) nitrogen concentration per unit
dry mass and (C) maximum
carboxylase activity of
ribulose-1,5-bisphosphate
carboxylase/oxygenase
(Rubisco) (Vcmax) per unit dry
mass and area (inset) in Picea
abies (䊉) and Pinus sylvestris (䊊). Foliage morphological and physiological variables of different-aged needles were standardized with respect to the values observed in current-year needles (needle age of zero). Error bars give ± SE for each needle age class. The data were derived
from the following studies: Schulze et al. 1977b, Aronsson and Elowson 1980, Zimmermann et al. 1988, Helmisaari 1990, Greve et al. 1992,
Rode 1992, Pfanz and Beyschlag 1993, Kellomäki and Wang 1997a.
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519
Table 1. Effects of tree height and age on foliar structural and physiological variables in Picea abies and Pinus sylvestris: explained variances (r 2)
of linear regressions (Figures 3–7). Both independent and dependent variables were log-transformed before the statistical analysis (see insets in
Figures 3–7). Statistical analysis: ns = not significant; * = P < 0.05; ** = P < 0.01; and *** = P < 0.001.
Dependent variable
Picea abies
Needle nitrogen concentration (%)
Dry mass per unit area (g m –2)
Needle dry mass (mg)
Needle length (cm)
Net assimilation rate (nmol g –1 s –1)
Net assimilation rate (µmol m –2 s –1)
Nitrogen use efficiency (mmol (mol N) –1 s –1)
Stomatal conductance (mmol g –1 s –1)
Stomatal conductance (mmol m –2 s –1)
Maximum carboxylase activity of Rubisco (nmol g –1 s –1)
Maximum carboxylase activity of Rubisco (µmol m –2 s –1)
Vcmax/N ratio (mmol (mol N) –1 s –1)
values of foliar characteristics measured at a certain year divided by the value for the current-year needles—were computed as means for all studies (see Figure 1 for reports
included as well as sample relations of foliar age versus needle
characteristics). These mean relative changes were used to
compute an appropriate estimate of the specific foliar variable
for current-year needles from the values measured in C+1
or C+2 needles. Although foliage longevity and age-related
changes in needle characteristics may depend on a number of
environmental factors, e.g., on light availability (Brooks et al.
1996, Niinemets 1997a), I consider the corrections obtained to
be the best that can currently be achieved.
Data analyses
Linear and nonlinear regression techniques (quasi-Newton
method; Wilkinson 1990) were employed in the data analyses.
Complex three-parameter equations are often used to describe
the age-related, nonlinear changes in needle characteristics
(e.g., Steele et al. 1989, 1990), but satisfactory fits to the nonlinear relationships among the data were also obtained by simple power functions of the form y = ax b. Given that the latter
can be linearized as log10y = log10 a + blog10 x, enabling demonstration of the initial changes in foliar characteristics with tree
height and age at better resolution, the data were also presented on log10–log10 axes in the insets (Figures 3–7). Both
nonlinear regressions with original data and linear regressions
with log-transformed data gave almost identical fractions of
explained variance. Because the log10 transformation of data
also essentially normalized the regression residuals such that
the requirements for the linear regression were fulfilled, I report the r 2 values with their significance estimates only for the
log-transformed data (Table 1).
Species differences in the log-transformed relationships of
foliar characteristics versus tree age and height were compared by means of covariation analysis. First, the separate
slope model with an interaction term was used to check for
possible differences in the slope. Whenever the interaction
Pinus sylvestris
Tree height
Tree age
Tree height
Tree age
0.00 ns
0.69***
0.61***
0.32*
0.64***
0.49***
0.58***
0.66***
0.63***
0.64***
0.59***
0.67***
0.00 ns
0.43***
0.38***
0.11 ns
0.48***
0.01 ns
0.01 ns
0.28*
0.51***
0.28**
0.00 ns
0.00 ns
0.00 ns
0.50***
0.46**
0.50**
0.76***
0.22*
0.52**
0.77***
0.33*
0.72***
0.34*
0.65***
0.08 ns
0.74***
0.48**
0.63***
0.75***
0.02 ns
0.37**
0.77***
0.25*
0.72***
0.19 ns
0.21 ns
term was insignificant, the data were analyzed by the common
slope model (Sokal and Rohlf 1995). All relationships were
considered significant at P < 0.05 (Wilkinson 1990).
Results
Variation in foliage nitrogen concentrations and structural
variables with tree height and age
Possibly because of differences in soil nutrient availability
among the stands, needle nitrogen concentrations (N) of current-year needles varied from 0.70 to 2.23% for the entire set
of data. Mean N (± SD) was 1.37 ± 0.36% for P. abies and
1.38 ± 0.33% for P. sylvestris, and the means were not statistically different according to a separate samples t-test (P > 0.8).
Needle nitrogen concentration was not correlated with tree
height (H) or age (Y ) in either species (Figure 2, Table 1).
Figure 2. Variability in needle nitrogen concentration in relation to
tree height in P. abies (䊉) and P. sylvestris (䊊). The linear correlation
was not significant in either P. abies (r = –0.06, P > 0.7) or P. sylvestris (r = –0.07, P > 0.7, see Table 1). The data sources are given in
Appendix 1.
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Overall, the correlations of foliar morphological variables
with H and Y were curvilinear, and were linearized by logarithmic transformation (Figure 3). Needle dry mass per unit projected needle area (MA) was strongly correlated with H and Y
in both species (Figures 3A and 3B, Table 1). This relationship
resulted primarily from increases in mean needle dry mass
with increasing H and Y (Figures 3C and 3D) in both species,
and from decreases in mean needle length (Figures 3E and 3F)
and area (data not shown) in P. sylvestris.
Because N was independent of H and Y, and MA increased
with increasing H and Y, the product N × MA (needle nitrogen
per unit projected area) scaled positively with both H (r 2 =
0.43, P < 0.001 for the linear regression with log–log transformed data) and Y (r 2 = 0.17, P < 0.01) in P. abies, and with Y
in P. sylvestris (r 2 = 0.53, P < 0.001).
assimilation rate per unit projected area (AA = AM × MA ) scaled
negatively with H (Figure 4C), but not with Y (Figure 4D), in
both species.
Given the independence of foliar N on H and Y, the photosynthetic nitrogen-use efficiency (EN) was, like AM, negatively
related to H in both species (Figure 4E), and to Y in P. sylvestris (Figure 4F).
Like needle morphological characteristics, A and EN decreased relatively more in younger and shorter plants than in
taller and older plants. Nevertheless, when trees shorter than
1 m were removed, AM still varied sixfold in P. abies and threefold in P. sylvestris, and AA varied fourfold in both species.
Thus, H and Y strongly altered needle photosynthetic characteristics not only in seedlings, but also in saplings and mature
trees.
Effects of tree height and age on foliar net assimilation rates
and nitrogen-use efficiency
Unravelling the stomatal and biochemical limitations of tree
size- and age-related decline in foliage assimilation rates
Net assimilation rate per unit needle dry mass (AM) decreased
with increasing H (Figure 4A) and Y (Figure 4B) in both species. Although MA increased strongly with both H and Y, net
The decline in A with increasing H and Y may arise either from
decreases in foliar stomatal conductance to water vapor (G) or
from decreases in biochemical foliage photosynthesis poten-
Figure 3. Correlation of needle dry
mass per unit projected area (A, B),
needle dry mass (C, D) and needle
length (E, F) with tree height (A, C, E)
and age (B, D, F) in P. abies (䊉, broken line) and P. sylvestris (䊊, solid
line). The data were fitted by power
functions of the form y = ax b by nonlinear regression in the main panels,
and by linear regressions in the insets,
which demonstrate the relationships on
log10–log10 axes. Table 1 reports the
explained variances (r 2) of the
linearized relationships, but r 2 was in
all cases similar for both nonlinear and
linear regressions (log10y = log10 a +
blog10 x). Only the regression lines of
the significant relationships (P < 0.05,
Table 1) are depicted. The data sources
are given in Appendix 1.
TREE PHYSIOLOGY VOLUME 22, 2002
DECLINE IN PHOTOSYNTHETIC CAPACITY WITH TREE AGE AND SIZE
521
Figure 4. Influences of tree height (A,
C, E) and age (B, D, F) on the rate of
net assimilation per unit dry mass (A,
B) and per unit projected area (C, D),
and on needle photosynthetic nitrogen-use efficiency (E, F). Data sources,
presentation and fitting as in Figure 3
(see Table 1 for the explained variances
of the linear fits in the insets).
tials (Vcmax) with increasing H and Y. In the current study, G per
unit needle dry mass (Figures 5A and 5B) and per unit projected area (Figures 5C and 5D) consistently decreased with
increasing H and Y in both species. However, H negatively affected Vcmax per unit needle dry mass (Figure 6A) and area
(Figure 6C) as well as the Vcmax/N ratio (Figure 7A) in both
species. Maximum carboxylase activity of Rubisco per unit
dry mass (Figure 6B) and the Vcmax/N ratio (Figure 7B) also
scaled negatively with Y. Thus, changes in both stomatal conductance and needle biochemical photosynthesis potentials
play a role in the decline in A with increasing H and Y in
P. abies and P. sylvestris.
Species differences in foliar structure and physiology
Covariation analysis with log-transformed data demonstrated
that at a common tree height and age, MA was larger in P. sylvestris than in P. abies (P < 0.001, Figures 3A and 3B). However, the slopes of the linearized MA versus H and MA versus Y
relationships were not significantly different between species,
indicating that the rate of age- and height-related changes in
MA is similar in both species.
The slopes of the linearized net assimilation rate (Fig-
ures 4A–D) and stomatal conductance (Figures 5A–D) versus
H and Y relationships were not significantly different between
species. However, P. sylvestris tended to possess greater AM at
common H (Figure 4A, P < 0.07) and Y (Figure 4B, P < 0.06)
than did P. abies. This, in combination with greater MA, led to
greater AA in P. sylvestris (Figures 4C and 4D, P < 0.005 for
the covariation analyses with both H and Y ). Similar foliar N
and somewhat larger AM in P. sylvestris implied a greater foliar
nitrogen-use efficiency in P. sylvestris than in P. abies (P <
0.02 for Figure 4E and P < 0.05 for Figure 4F).
Except for the relationship between stomatal conductance
per unit dry mass and H (Figure 5A, P > 0.1), G was higher in
P. abies than in P. sylvestris at common H and Y (Figure 5, P <
0.02). Because of the lower G and greater A (Figure 4), foliar
biochemical photosynthesis potentials were generally larger
in P. sylvestris than in P. abies (P < 0.01 for all comparisons in
Figures 6A–D). Furthermore, the slope of the relationship
between H and Vcmax per unit dry mass (Figure 6A) was more
negative in P. abies than in P. sylvestris (separate slope
ANCOVA model, P < 0.02). The latter difference indicates
that foliage biochemical photosynthetic capacity decreases
faster with increasing H in P. abies than in P. sylvestris.
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522
NIINEMETS
Figure 5. Stomatal conductance per
unit needle dry mass (A, B) and per
unit needle projected area (C, D) in relation to tree height and age. Data
sources, presentation and fitting as in
Figure 3. The r 2 values of the linearized relationships in the insets are
given in Table 1.
Evidence that tree size rather than age is responsible for
observed foliar modifications
Because Y and H were correlated (r 2 = 0.77 and 0.88 for
P. abies and P. sylvestris, respectively; linear regressions between the log-transformed variables, P < 0.001 for both regressions), tree age- and height-related adjustments in foliar
structure and function cannot be clearly distinguished in the
current data. However, the explained variances were generally
larger in the regressions with H (Figures 3–7, Table 1) than in
the regressions with Y, especially in P. abies. Furthermore, in
multiple linear regression analyses where both H and Y were
included as independent variables, Y was always insignificant
for P. abies, suggesting that tree height controls foliar structure
and function in this species. However, in P. sylvestris, Y rather
than H was significant in multiple regressions with MA and AM.
Nevertheless, other relationships (cf. Figures 4C, 4D and 6,
Table 1) provided evidence of greater control of foliage function by tree size in this species as well.
Figure 6. Relationships of the maximum carboxylase activity of Rubisco
(Vcmax) per unit needle dry mass (A, B)
and per unit needle projected area (C,
D) with tree height (A, C) and age (B,
D). Values of Vcmax were derived from
the data as described in Appendix 2,
and were standardized to 25 °C using
the temperature response of the specific activity of Rubisco given in
Niinemets and Tenhunen (1997). Data
sources, presentation and fitting as in
Figure 3. Table 1 reports the r 2 values
of the regressions in insets.
TREE PHYSIOLOGY VOLUME 22, 2002
DECLINE IN PHOTOSYNTHETIC CAPACITY WITH TREE AGE AND SIZE
523
Figure 7. Dependence of the Vcmax /N
ratio on (A) tree height and (B) tree
age. Data sources, presentation and fitting as in Figure 3. The explained variances of the linearized relations are
given in Table 1.
Discussion
Tree size- and age-related changes in foliage nitrogen
concentration
Increases in nitrogen-poor woody litter relative to N-rich foliar
litter, and resulting decreases in soil nitrogen turnover rates,
have been proposed as a general cause of declines in foliar nitrogen concentration (N) with age (Gower et al. 1996, Murty et
al. 1996). Alternatively, dilution of foliar nitrogen by other
leaf compounds such as carbohydrates and lignin, which accumulate in water-stressed needles, may explain the negative
association between foliage N and tree height (Niinemets
1997b). In the latter study, foliar lignin and nonstructural carbohydrate concentrations increased with increasing tree
height in P. abies, and this led to lower foliar N.
Despite the large body of evidence showing decreases in
foliar N with increasing H and Y (cf. Introduction), foliage N
apparently did not change during the course of stand development in other studies (Miller et al. 1991, Donovan and Ehleringer 1992, Yoder et al. 1994, Mencuccini and Grace 1996b,
Hubbard et al. 1999). The current work also demonstrates that
the relationship between foliar N and H and Y is not general
(Figure 2, Table 1). Possibly, the variation in nutrient availability across stands on various soils and at different geographical
locations plays a more important role than do tree height- and
age-related adjustments in foliar chemistry.
Although the needle N was independent of H and Y, foliar A
scaled negatively with tree size in the current study (Figure 4)
and in several other studies (Miller et al. 1991, Yoder et al.
1994, Hubbard et al. 1999). Thus, modification of foliar N
alone is apparently not responsible for the general decline in
photosynthetic rates with increasing stand height and age.
Changes in foliar structure with tree height and age
Higher foliar dry mass per unit projected area (MA ), as observed here (Figures 3A and 3B), is a general response to increases in tree height and age (see Introduction). In P. abies
and P. sylvestris, increases in MA resulted primarily from a
greater mean needle dry mass in larger and older trees (Figures 3C and 3D). Similarly, Höhne (1964) found that needle
dry mass increases hyperbolically with increasing Y in
P. abies.
Contrary to the monotonic increase in MA and needle dry
mass, foliar areas and lengths often initially increase with H
and Y to a maximum value, and decline thereafter (Montfort
and Müller 1951, Allsopp 1965, Kovalyev 1980, Steele et al.
1989, but see Greenwood 1984, Schoettle 1994 and P. abies in
Figures 3E and 3F for divergent patterns). The initial increase
in leaf size has been associated with the transition from the juvenile to the adult stage, but no physiological mechanism responsible for decreases in leaf size in mature plants has been
proposed. I suggest that greater water limitations in the crowns
of larger trees may be the cause of smaller leaves in tall and old
trees. Tissue expansion growth depends directly on tissue
turgor pressure, and is a water stress-sensitive process (Hanson and Hitz 1982, Dale 1988). Compatible with the hypothesis of limited expansion growth rates, foliar cells are smaller in
taller and older trees of Picea schrenkiana Fisch. & C. A. Mey.
(Baidavletova 1984). In addition, shoot growth rates are generally lower in larger than in smaller trees (Montfort and
Müller 1951, Maggs 1964, Schoettle 1994, Bond 2000), reinforcing the argument for a role of water stress in arresting
growth. Although determination of the exact mechanism of foliar area modification requires further study, I conclude that
decreases in mean needle surface area may be an important
factor responsible for larger MA in taller trees (P. sylvestris in
Figures 3E and 3F).
What is the adaptive value of leaves with greater needle dry
mass per unit area in taller trees?
Studies have shown that higher MA in taller conifer trees is related primarily to greater needle density (MA = thickness ×
density) rather than to greater needle thickness (Johnson et al.
1985, Niinemets and Kull 1995, Niinemets 1997b). Leaves of
greater density generally possess smaller and more tightly
packed cells (Cutler et al. 1977, Jones 1985, Niinemets 1999)
as well as thicker and more lignified cell walls (Niinemets
1997c, Niinemets et al. 1999b) than leaves of lower density.
Such foliar structural adjustments influence important foliar
hydraulic variables. A global analysis of the relationships between foliar structure and water relations (Niinemets 2001)
has demonstrated a strong positive correlation between leaf
density and leaf bulk elastic modulus (e; change in hydrostatic
pressure per unit change in leaf symplasmic water content)
across a wide range of woody species of contrasting ecology
and geographic distribution. Water potential changes more for
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524
NIINEMETS
a given change in tissue water content in leaves with greater e,
and thus, increases in e allow development of a larger gradient
of water potential between leaves and soil (DY) with lower tissue water loss (Bowman and Roberts 1985).
Although it has been hypothesized that trees regulate stomatal conductance to avoid critical foliar water potentials for
cavitation (Sperry et al. 1998), and that therefore the minimum
leaf water potentials should be similar in large and small trees
(Magnani et al. 2000), studies demonstrate that minimum water potentials are often lower in larger trees (Yoder et al. 1994,
Fredericksen et al. 1995, 1996, de Soyza et al. 1996, Bauerle et
al. 1999, Hubbard et al. 1999). Thus, DY values do change
with increasing tree size, and I conclude that adjustment of foliar elastic properties provides an important way for coping
with enhanced water limitations in the foliage of taller trees.
Decline in net assimilation rates with increasing tree size
and age: structural, stomatal and biochemical limitations
As observed previously in other species, net assimilation rates
(A) were generally lower in taller and older trees of both
P. abies and P. sylvestris (Figures 4A–D). Given that MA
scaled positively with tree size, this relationship was stronger
(cf. Figures 4A and 4B and Figures 4C and 4D) for net assimilation rates per unit of dry mass (AM) than for relationships per
unit of needle projected area (AA = MA × AM). In fact, foliar
nitrogen per unit area (Schoettle 1994, Rijkers et al. 2000, current study) and AA (Rijkers et al. 2000) may increase with increasing tree size, suggesting that increases in MA involve
accumulation of both support and assimilative compounds,
and may therefore partly counterbalance decreases in AM. In
the current study, there was evidence of moderately lower AA
values in the smallest seedlings compared with saplings (Figure 4C). However, as trees increased in height, AA decreased
monotonically, indicating that enhanced MA cannot fully compensate for decreases in AA.
Although foliar stomatal conductance (G) was consistently
lower in taller and older trees (Figure 5), photosynthetic capacities at constant intercellular CO2 concentrations (Vcmax)
also declined significantly with tree size (Figure 6). Thus, a
parallel decline in G and A with increasing tree size and height
does not necessarily mean that changes in G fully explain the
decreases in A. In a like manner, in Sequoiadendron giganteum (Lindl.) Buchh., both G and A were strongly affected by Y,
but the Ci was almost insensitive to Y, especially during the initial, most rapid phase of decline in A and G (Grulke and Miller
1994).
The relationships between foliage structural (Figure 3) and
physiological variables (Figures 4–7) were strongly nonlinear,
with the relative changes being highest in smaller trees and
progressively less in larger trees. Similar nonlinear responses
in foliage morphology and function have been observed in
several other studies (Höhne 1964, Steele et al. 1989, Grulke
and Miller 1994). Despite the nonlinear scaling of foliar characteristics with H and Y, foliage photosynthetic variables also
varied several-fold for a height range of 5–20 m (Figures 4–7),
indicating that the height- and age-related changes in photosynthetic capacity are also important in mature trees.
Although the way in which hydraulic resistance to water
flow changes with increasing length of the water-conducting
pathway depends on the taper of xylem conduits (Becker et al.
2000a), experimental data suggest that hydraulic resistance increases in a nearly linear manner with increasing tree height
(Mencuccini and Grace 1996a, 1996b, Magnani et al. 2000).
However, the conductance, rather than resistance, scales linearly with plant transpirational water loss, and accordingly
with potential water stress in the upper canopy. Given that a
linear increase in hydraulic resistance is compatible with a hyperbolic decline in hydraulic conductance, with the decreases
in conductance progressively less at higher values of resistance, I conclude that the observed nonlinear responses of hydraulic conductance with tree height and age (Mencuccini and
Grace 1996a, 1996b) provide an explanation of the asymptotic
scaling of foliage photosynthetic characteristics.
Interspecific differences in foliar response to tree size and
age
Foliar attributes changed similarly with increasing tree size in
both species (Figures 3–7, Table 1). However, there was evidence of a greater decline in Vcmax per unit needle dry mass in
P. abies than in P. sylvestris with increasing H. This may indicate that water limitations in crowns of equal-sized trees were
more severe in P. abies than in P. sylvestris. Because the needle
longevity of P. abies (> 10 years) is considerably greater than
that of P. sylvestris (up to 5 years), total canopy foliar area is
generally more extensive in P. abies. Given the larger stomatal
conductance (Figure 5) and foliar area, P. abies should be
more prone to water stress unless interspecific differences in
whole-plant hydraulic characteristics compensate for differences in foliar area and stomatal conductance. In fact, available stem hydraulic and xylem architectural data do not
support the assumption of a more efficient water conducting
system in P. abies. Mean specific hydraulic conductivity at the
trunk base of tall (about 15 m) open-grown P. abies trees was
1.75 × 10 –12 m2 (Sellin 1993), but 3.41 × 10 –12 m2 in similarsized P. sylvestris trees (Mencuccini et al. 1997), and mean
tracheid diameters were also larger in P. sylvestris than in
P. abies at common H and Y (Sellin 1990, 1993, Mencuccini et
al. 1997). In addition, the relative fraction of sapwood in stemwood of trees of common age and size was greater in P. sylvestris than in P. abies (cf. Sellin 1991, 1994, Mencuccini and
Grace 1996b).
Evidence of larger mesophyll diffusion resistance in older
and larger trees
The values of Vcmax and the maximum rate of photosynthetic
electron transport, calculated as described in Appendix 2
(Equations A1–A6) from Ci as a substitute for chloroplast CO2
concentration (Cc), provide a useful estimate of foliar photosynthetic capacity independent of stomatal limitations, and
also allow reliable simulation of observed rates of net assimilation. The use of Ci instead of Cc for computation of the parameters of the biochemical leaf photosynthesis model is
common in plant ecophysiological research, because Cc cannot be estimated from foliar gas exchange data alone (Loreto
TREE PHYSIOLOGY VOLUME 22, 2002
DECLINE IN PHOTOSYNTHETIC CAPACITY WITH TREE AGE AND SIZE
et al. 1992, Evans and von Caemmerer 1996). However, there
is generally also a diffusion resistance between leaf intercellular air space and carboxylation sites in the chloroplasts
(Ri) that is not taken into account by substituting Ci for Cc
(Epron et al. 1995, Syvertsen et al. 1995, Evans and Loreto
2000). Thus, foliar biochemical photosynthesis capacities
may actually be larger than estimated from Equations A1–A6.
Studies indicate that foliar anatomical structure is an important factor affecting Ri (Evans et al. 1994, Syvertsen et al.
1995). In particular, greater foliar density (lower volume of
intercellular air space, and longer diffusion path lengths from
intercellular air space to the outer surfaces of cell walls as well
as through the cell walls) is compatible with greater R i
(Syvertsen et al. 1995). Given the constant foliar N, declines in
Vcmax (Figure 6) and the Vcmax/N ratio (Figure 7) may arise from
modifications in foliar density. Higher foliar lignin concentrations in larger trees (Niinemets 1997c) further suggest that Ri
is greater in taller trees, because lignification dramatically decreases the permeability of cell walls to both water and CO2
(Brett and Waldron 1996).
Greater enrichment of foliar carbon by the heavier stable
isotope (13C) with increasing tree height or age has been interpreted exclusively as indicative of stronger stomatal control in
larger trees (Donovan and Ehleringer 1992, Yoder et al. 1994,
Bauerle et al. 1999, Hubbard et al. 1999). However, in many
cases (see above) the variation in foliar Ci is only moderate in
response to large tree height-related changes in foliar G. In
fact, the fractionation of carbon isotopes may occur along the
entire diffusion pathway from the outside air to the CO2 fixation sites within the chloroplasts. In addition to stomatal closure, large diffusion resistances from sub-stomatal cavities to
the carboxylation sites in chloroplasts may also effectively reduce the isotopic effect of CO2 fixation (Vitousek et al. 1990).
In the study of Bauerle et al. (1999), there was no evidence of
lower G in taller trees, but taller trees fixed a greater fraction of
13
C, possibly because of larger mesophyll transfer resistances.
Thus, the available data on foliar carbon isotope composition
in different-sized trees may need to be reconsidered in light of
possible changes in Ri with tree size.
Does leaf structure and function respond to tree age or size?
Difficulties in attributing modifications in foliage characteristics to changes in height or age have been addressed in several
contributions (Ryan et al. 1997, Becker et al. 2000b, Bond
2000). Foliar variables change continuously throughout plant
development (Doorenbos 1965, Borchert 1976, Clark 1983),
but tree dimensions increase simultaneously. Nevertheless, as
studies with various-aged scions grafted on juvenile rootstocks of the same size demonstrate, a number of important foliar modifications, e.g., increases in mean needle dry mass
(Greenwood 1984), and in MA (Hutchison et al. 1990), do occur with increasing age. However, contrary to the observations
of greater density in mature, tall forest trees, larger MA of older
scions in Larix laricina (Du Roi) C. Koch (Hutchison et al.
1990) arose from greater thickness (MA = density × thickness).
This is an important difference, because increases in foliar
thickness allow accumulation of photosynthetic biomass per
525
unit area, thereby enhancing foliar AA, but should not necessarily increase mesophyll diffusion limitations (see Niinemets
1999 for a review). Unlike the decline in A and G in taller and
older trees (Figures 4–7), age of grafted scions positively affected foliar net photosynthesis and did not influence foliar
stomatal conductance in L. laricina (Hutchison et al. 1990).
Hence, experimental evidence suggests that observed increases in foliar density, and declines in G (Figure 5) and photosynthetic capacity (Figure 6), are primarily responses to increases in tree height rather than age. Although H and Y were
correlated in the current study, the correlations of foliar structural and physiological variables were generally stronger with
H, and Y was mostly insignificant in multiple regressions.
Thus, based on the outlined experimental and statistical evidence, I conclude that decreases in foliar net assimilation rates
throughout stand development are primarily responses to increases in stand stature.
Conclusions
This study demonstrates that modification of foliar G and foliar N with increasing tree size and age is insufficient to explain the decline in foliar A in two temperate conifer species.
Changes in MA with increasing tree size are likely to bring
about enhanced diffusive resistances between sub-stomatal
cavities and carboxylation sites in the chloroplasts, thereby reducing foliar photosynthesis at a common Ci in larger trees. Increases in MA with increasing H likely result in higher needle
elastic moduli, and thereby allow development of a larger water potential gradient between soil and needles with lower tissue water loss. Thus, a greater capacity for water extraction
from drying soil inevitably leads to a lower photosynthetic capacity.
The tree size-related increases in MA and decreases in A are
strongly nonlinear and parallel the nonlinear decreases in tree
hydraulic conductance. This simultaneous modification in foliar structural, physiological and stem hydraulic characteristics suggests that the enhanced water limitations in taller trees
may be the ultimate cause of adjustments in foliage structure
and function. Although the changes in A are progressively less
with increasing tree size, larger trees also have lower fractional
allocation of total biomass to foliage (Whittaker and Woodwell 1968, Ryan et al. 1997). Thus, decreases in whole-canopy
photosynthesis rather than in the assimilative capacity of single leaves are likely to provide an explanation for the strong
monotonic decreases in forest net primary productivity with
increasing stand age (Ryan et al. 1997).
Acknowledgments
The study was supported by the Estonian Science Foundation (Grant
3235) and the Estonian Minister of Education (Grants 0280341s98,
0180517s98).
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Appendix 1
Table A1. Data sources, stand locations, height and age of studied trees and available variables.
No.
Study
Picea abies
1
Bauer 1997
2
Schulze et al. 1990, Zimmermann 1990
3
Zimmermann 1990
4
Grassi and Minotta 2000, Grassi et al. 2001
52
Dixon et al. 1995, Le Thiec and Dixon 1996
6
Bavcon et al. 1996
7
Koike et al. 1994
8
Grassi and Bagnaresi 2001
9
Hättenschwiler and Körner 1996
10
Benecke 1972
11
Bauer et al. 2000
12 3
Benecke 1972, Havranek et al. 1989
13 3
Benecke 1972, Perterer and Körner 1990
14 2
Havranek and Wieser 1994, Weih et al. 1994,
Wieser and Havranek 1994
15
Keller and Wehrmann 1963
16
Falge et al. 1996
17
Rennenberg et al. 1990
18
Egli et al. 1998
19
Mehne-Jakobs 1995, 1996
20
Bauer 1997
21
Hager and Sterba 1985
22
Le Thiec et al. 1994
23 3
Alekseyev 1975
24
Wieser and Havranek 1993
25
Zimmermann 1990
26
Schulze et al. 1985
27 2, 3
Marek et al. 1991, 1992, 1995, 1997,
Medlyn et al. 1999, Šprtová et al. 1999
28
Benner et al. 1988
29
Lange et al. 1986
30
Bauer 1997
31
Bauer 1997
32 4
Lange et al. 1986, Zimmermann et al. 1988,
Weikert et al. 1989, Zimmermann 1990,
Wedler 1991, Niinemets 1997b
33
Zimmermann et al. 1988, Zimmermann 1990
34 3
Alsheimer 1996
35
Pfanz and Beyschlag 1993
36
Pfanz and Beyschlag 1993
37
Benner et al. 1988
38
Pfanz et al. 1994
39
Höhne 1963
Wedler 1991, Wedler et al. 1995
40 2
Stand coordinates
Mean tree height (m)
Age (year)
Available variables1
41°43′ N, 14°18′ E
43°09′ S, 171°43′ E
43°22′ N, 00°21′ W
44°30′ N, 11°20′ E
45°39′ N, 03°15′ E
46°03′ N, 14°30′ E
46°34′ N, 08°01′ E
46°38′ N, 12°32′ E
47°02′ N, 08°00′ E
47°11′ N, 10°46′ E
47°12′ N, 11°28′ E
47°13′ N, 11°25′ E
47°17′ N, 11°24′ E
47°21′ N, 11°52′ E
20.9
38
22
3
4
7–8
1.6
26
23
6
3
3
3, 60
3–12
62–67
N, MA
N, AA, Vcmax;A
N, AA, Vcmax;A
N, MA, A, Vcmax
MA, G, A, Vcmax
AM
N, AA, Vcmax;A
N, MA, Vcmax
N, AM, O
N, AM
N, AA, Vcmax;A
N, GA, AM
N, MA
MA, G, A, Vcmax
25
1.4–16
0.33
130
6
5.7
6
100
21
8
120
80
2
72
7–30
N, MA, A
GA, AA, Vcmax;A
GA, AA, Vcmax;A
MA, G, A, Vcmax, O
GA, AA, Vcmax;A
N
M A, O
GA, AA, Vcmax;A
MA
MA, G, A, Vcmax
N, AA, Vcmax;A
GA, AA, Vcmax;A
N, AA, Vcmax;A
49°42′ N, 07°05′ E
49°43′ N, 09°43′ E
50°04′ N, 11°50′ E
50°08′ N, 11°54′ E
50°00′ N, 11°49′ E
10
5.7
25.3
26.7
2.7–16.7
22.5
19
120
142
9–32
MA, G, A, Vcmax
MA, A, Vcmax
N
N, MA
N, MA, G, A, Vcmax, O
50°05′ N, 11°42′ E
50°08′ N, 11°52′ E
50°24′ N, 12°57′ E
50°36′ N, 13°27′ E
50°38′ N, 07°22′ E
50°38′ N, 13°33′ E
51°01′ N, 13°19′ E
51°04′ N, 00°49′ W
10.0
16.1–25.2
30
40–140
140
65
18
15
15
5, 6
N, MA, G, A, Vcmax
N, MA
N, AM, Vcmax;M
N, AM, Vcmax;M
MA, A, Vcmax
N, AM, Vcmax;M
N, O
N, GM, AM, Vcmax;M
47°21′ N, 08°26′ E
47°21′ N, 08°26′ E
47°29′ N, 11°05′ E
47°33′ N, 07°35′ E
47°59′ N, 07°51′ E
48°12′ N, 07°11′ E
48°20′ N, 15°20′ E
48°29′ N, 07°05′ E
48°37′ N, 24°22′ E
48°42′ N, 14°00′ E
48°45′ N, 06°21′ E
49°25′ N, 16°36′ E
49°30′ N, 18°32′ E
0.9–1.0
0.36, 0.45
1.55
0.7
30
0.35
29.6
6
1
19.0–23.4
7
2
9
0.8, 0.9
Continued on facing page.
TREE PHYSIOLOGY VOLUME 22, 2002
DECLINE IN PHOTOSYNTHETIC CAPACITY WITH TREE AGE AND SIZE
533
Table A1 Cont’d. Data sources, stand locations, height and age of studied trees and available variables.
No.
Study
Picea abies
41
Schulze et al. 1977a, 1977b
Eamus et al. 1990,
42 2
Mikkelsen and Ro-Poulsen 1994
43
Alekseyev 1975
44
Ingerslev 1999
45
Bauer 1997
46
Bauer 1997
47a
Karlsson et al. 1997
47b 2
Wallin et al. 1990, 1992a, 1992b,
Wallin and Skärby 1992
Alekseyev 1975
48 3
49 3,4
Arvisto 1971, Kull 1986, Kull and Koppel 1987,
Niinemets and Kull 1995
Gulidova 1959
50 3,4
Alekseyev 1975
51 3
52
Troeng 1991
53
Vapaavuori et al. 1992
54 3
Roberntz and Stockfors 1998, Roberntz 1999
55
Bauer 1997
56
¯elawski et al. 1973
57
Kronfuß et al. 1998, Wieser et al. 1998
58
Szaniawski and Wierzbicki 1978
59
Lippert et al. 1996, 1997
60
Lippert et al. 1997
61
Dube and Bornman 1992
Pinus sylvestris
1
Luoma 1997, Palmroth et al. 1999
2
Luoma 1997, Palmroth et al. 1999
3
Perterer and Körner 1990
4
Keller and Wehrmann 1963
5
Auclair 1977
6
Luoma 1997, Sturm 1998, Palmroth et al. 1999
7
Schulze and Küppers 1985
82
Jach and Ceulemans 1999, 2000
9
Farrar et al. 1977
10
Reich et al. 1994
11
¯elawski et al. 1968
van Hees and Bartelink 1993
12 3
13
Beadle et al. 1985a, 1985b
14
Greve et al. 1992, Rode 1992,
Greve and Terborg 1993
15
Luoma 1997, Palmroth et al. 1999
16 4
Ovington and Madgwick 1959
Malkina 1982
17 3
18
Sandford and Jarvis 1986
19
Molchanov 1983
20
Luoma 1997, Palmroth et al. 1999
21
Troeng 1991
22 3
Bengtson 1980, Hellkvist et al. 1980,
Linder and Axelsson 1982,
Troeng and Linder 1982a, 1982b
23
Raitio 1990
24
Raitio 1990
25
Raitio 1990
26
Raitio 1990
27
Raitio 1990
Available variables1
Stand coordinates
Mean tree height (m)
Age (year)
51°34′ N, 09°52′ E
55°41′ N, 12°06′ E
25.6
1
89
5, 8
M A, A
GA, AA, Vcmax;A
55°45′ N, 37°55′ E
56°27′ N, 08°27′ E
56°33′ N, 13°13′ E
56°58′ N, 08°24′ E
57°40′ N, 11°90′ E
57°40′ N, 11°90′ E
23.6
16
15
20
0.125
85
59
30
80
1.5
7, 8
MA
N
N, MA
N, MA
GA, AA, Vcmax;A
N, MA, G, A, Vcmax
57°45′ N, 36°27′ E
58°44′ N, 26°45′ E
12.7–26.5
1.5–38
100–120
5–107
MA
N, MA, G, A, Vcmax, O
59°36′ N, 40°18′ E
60°00′ N, 38°31′ E
60°19′ N, 16°12′ E
62°37′ N, 26°06′ E
64°07′ N, 19°27′ E
64°14′ N, 19°46′ E
Growth chamber 5
Growth chamber
Growth chamber
Growth chamber
Growth chamber
Growth chamber
0.3–25
16.4, 17.7
1–100
105, 130
0.55
1.7
36
145
0.27
5
0.21
5
4
0.31
M A, O
MA
GA, AA, Vcmax;A
N
N, G, A, Vcmax
N, MA
AM
GA, AA, Vcmax;A
M A, A
N, GM, AM, Vcmax;M
N, GM, AM, Vcmax;M
O, AM
42°07′ N, 02°12′ E
42°37′ N, 02°06′ E
47°17′ N, 11°24′ E
47°21′ N, 08°26′ E
47°47′ N, 01°52′ E
47°56′ N, 07°38′ E
49°45′ N, 11°56′ E
51°13′ N, 04°24′ E
51°24′ N, 00°40′ E
52°15′ N, 17°03′ E
52°15′ N, 21°00′ E
52°18′ N, 05°42′ E
52°25′ N, 00°44′ E
53°00′ N, 10°21′ E
12.2
7.9
26
6.5
0.33
2
24–32
7
3, 4
3.19
9
0.5
9–38
45
32
N, MA, G, A, Vcmax
N, MA, G, A, Vcmax
MA
N, MA, A
AM
N, MA, G, A, Vcmax
N, MA, G, A, O
N, MA, A, O, Vcmax
M A, O
N, AM
M A, O
MA
AA, Vcmax;A
N, AA, O
N, MA, G, A, Vcmax
N
AM, Vcmax;M
G A, A A
M A, A
N, MA, G, A, Vcmax
GA
N, MA, GA, A, Vcmax, O
N, O
N, O
N, O
N, O
N, O
4.9, 7.2
22
0.325
0.5
11.9–12.9
1.8
0.63, 1.05
1
3.4–16.5
16.5
12
53°08′ N, 13°04′ E
55°28′ N, 02°34′ W
55°45′ N, 37°55′ E
55°57′ N, 03°12′ W
57°40′ N, 38°34′ E
56°42′ N, 13°05′ E
60°19′ N, 16°12′ E
60°49′ N, 16°30′ E
11.2
9.5–13.2
1.5–25
17.2
9.1
0.4
2.1–15.6
25
33
5–90
3
38
18
0.55
20, 120
61°43′ N, 22°54′ E
61°45′ N, 22°40′ E
61°46′ N, 22°33′ E
61°46′ N, 22°44′ E
61°47′ N, 22°30′ E
3.2
3.6
6.6
5.2
4.8
25
27
25
27
25
Continued on overleaf.
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534
NIINEMETS
Table A1 Cont’d. Data sources, stand locations, height and age of studied trees and available variables.
No.
Study
Stand coordinates
Pinus sylvestris
28
Korpilahti 1990
29
Raitio 1990
30
Vapaavuori et al. 1995
31a 2
Wang et al. 1996, Kellomäki and Wang 1997a,
1997b, Medlyn et al. 1999
Helmisaari 1990, 1992
31b 3
32
Luoma 1997, Palmroth et al. 1999
33 2
Norgren 1996
34
Lundmark et al. 1988, Hällgren et al. 1990
35
Öquist and Malmberg 1989
36
Luoma 1997, Aalto 1998, Palmroth et al. 1999
37
¯elawski et al. 1973
38
Brunes et al. 1980
39
Lippu and Puttonen 1991
40 2
Szaniawski and Wierzbicki 1978
41
Vapaavuori et al. 1995
42
Gowin et al. 1980
1
2
3
4
5
Mean tree height (m)
61°51′ N, 24°17′ E
62°04′ N, 22°14′ E
62°39′ N, 27°05′ E
62°47′ N, 30°58′ E
3.7
2.5, 2.8
62°47′ N, 30°58′ E
61°48′ N, 24°28′ E
63°49′ N, 20°19′ E
64°14′ N, 19°46′ E
65°17′ N, 16°43′ E
67°46′ N, 29°35′ E
Growth chamber
Growth chamber
Growth chamber
Growth chamber
Growth chamber
Growth chamber
2.03–20.0
10.5
0.4–1.3
6.3–7.0
0.18
0.22
0.48
0.10–0.24
Age (year)
Available variables1
20
25
13.5
22.5, 27.5
AA, Vcmax;A
N, O
N, AM
N, MA, G, A, Vcmax
15–100
27
3.7
2.5
2.5
36–45
0.096
0.14
1
0.03–0.14
0.58
0.18
N, O
N, MA, G, A, Vcmax
M A, O
AA, Vcmax;A
AA, Vcmax;A
N, MA, G, A, Vcmax
AM
MA, G, A, Vcmax
GA
AM
N, AM
AM
Abbreviations: N = needle nitrogen concentration (%); MA = dry mass per unit projected area (g m –2); G = stomatal conductance to water vapor
per unit projected area (mmol m –2 s –1) and per unit dry mass (mmol g –1 s –1); A = needle net assimilation rate per unit projected area (µmol m –2
s –1) and per unit dry mass (nmol g –1 s –1); Vcmax = maximum carboxylase activity of Rubisco per unit projected area (µmol m –2 s –1) and per unit
dry mass (nmol g –1 s –1); and O = other needle morphological characteristics (dry mass (mg), needle length (cm)). In the case of missing MA values, stomatal conductance, net assimilation rate and maximum carboxylase activity of Rubisco were expressed either per unit projected area
(GA, AA, Vcmax;A) or per unit dry mass (GM, AM, Vcmax;M).
Trees from the same stand or experiment sampled at various times.
Different stands of varying age and height in close vicinity.
Several trees of various age and size from the same stand.
Plants grown in growth chambers under controlled conditions.
Appendix 2
Derivation of parameters of the needle photosynthesis model
Intercellular CO2 (Ci) versus net photosynthesis (A) response
curves are generally used to calculate estimates of the maximum carboxylase activity of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) (Vcmax) and the maximum rate
of photosynthetic electron transport (Jmax), assuming that A is
limited by low CO2 concentration in the initial part of the
curve and by the photosynthetic electron transport rate in the
saturating part of the curve. Whenever A versus Ci response
curves were available, an estimate of Vcmax and mitochondrial
respiration (Rd ; CO2 evolution from non-photorespiratory processes continuing in the light) was derived from the initial portion (Ci ~ 50–180 µmol mol –1) of an A versus Ci curve. First,
the slope and intercept (A = kCi + i) were calculated for each
combination of points in the Rubisco-limited part of the A versus Ci curve. Because the slope is equivalent to the first derivative of the equation of leaf photosynthesis when Rubisco limits carboxylation (Farquhar and von Caemmerer 1982), Vcmax
was calculated for each slope as:
Vcmax = k
(C i + Kc (1 + O / K o )) 2
,
Γ* + K c (1 + O / K o )
(A1)
where Kc and Ko are the Michaelis-Menten constants for carboxylation and oxygenation, respectively, O is the intercellular oxygen concentration and Γ ∗ is the CO2 compensation
concentration in the absence of mitochondrial respiration
(Laisk 1977). Parameters Kc, Ko and Γ ∗ were calculated for
each specific temperature as described in Niinemets and Tenhunen (1997). From CO2 response curves, Rd was determined
as:
Rd =
Vcmax (C i − Γ* )
− ( kC i + i).
C i + K c (1 + O / K c )
(A2)
The mean of the two highest values of Vcmax with their mean
Rd was used in the following calculations. The values of k (carboxylation efficiency), which were reported in many studies,
were also converted to estimates of Vcmax with Equation A1.
The data points measured at intercellular CO2 concentrations larger than 300 µmol mol –1 were used to derive the capacity for photosynthetic electron transport. Assuming that
the rate of ribulose-1,5-bisphosphate (RUBP) regeneration is
NADPH-limited, the rate of photosynthetic electron transport,
(J) was determined as (Farquhar and von Caemmerer 1982):
J=
( A + Rd )( 4C i + 8Γ* )
,
C i − Γ*
TREE PHYSIOLOGY VOLUME 22, 2002
(A3)
DECLINE IN PHOTOSYNTHETIC CAPACITY WITH TREE AGE AND SIZE
and Jmax from the Smith’s equation (Tenhunen et al. 1976):
αQJ
Jmax =
α Q2 − J 2
2
(A4)
,
where α (mol electrons (mol quanta) –1) is the apparent initial
quantum yield at saturating CO2 and for an incident quantum
flux density (Q). Whenever available, the initial slope (Q <
100 µmol m –2 s –1) of the light-response curve of net photosynthesis (φ) measured at a specific Ci was used to calculate an estimate of α according to Kellomäki and Wang 1997a:
φ=
∂A
Q →0
∂Q
=α
1 − Γ*/ C i
φ ( 4 + 8Γ*/ C i )
α
.
⇔
=
1 − Γ */ C i
4 + 8Γ*/ C i
(A5)
For studies lacking the information necessary for φ calculations, representative estimates of α were derived, accounting
for the light field heterogeneity at needle surfaces during the
photosynthesis measurements. Although the quantum yields
for an absorbed irradiance are conservative in C3 species
(Ehleringer and Björkman 1977), α varies as a result of
changes in the fraction of incident light that is absorbed. Apart
from the dependence on leaf optical properties, α depends on
shoot structure in conifers, especially when the shoot illumination is unidirectional, leading to the highest within-shoot
shading. In the current study, a value of α of 0.12 mol mol –1
was obtained for the measurements with unidirectional irradiance as an average of all available estimates calculated
with Equation A5. For the measurements with bidirectional
irradiance or diffuse light, or for artificially thinned shoots
(e.g., ¯elawski et al. 1973, Szaniawski and Wierzbicki 1978,
Luoma 1997), a mean estimate of 0.25 mol mol –1 was determined in the same manner.
Assuming that at current ambient CO2 concentrations A at
light saturation is limited by Vcmax, and at lower quantum flux
densities by Jmax, Vcmax and Jmax may also be obtained from the
light-response curves of A (Niinemets and Tenhunen 1997,
Niinemets et al. 1999c, 1999d). The value of A measured at the
lowest Q, along with the information about quantum yield,
was used to compute Rd. The rate of photosynthetic electron
transport was calculated with Equation A3 for each A value
exhibiting light-sensitivity, and Jmax with Equation A4. Maximum carboxylase activity of Rubisco was computed from the
saturated part of the light curve as (Farquhar et al. 1980,
Farquhar and von Caemmerer 1982):
Vcmax =
( A + Rd )(C i + K c (1 + O / K c ))
.
C i − Γ*
(A6)
535
Finally, when only single-point, light-saturated rates of A at
certain CO2 concentrations were available, either an estimate
of Vcmax from Equation A6 (measurements with non-saturating
CO2 concentrations) or Jmax from Equation A3 (saturating CO2
concentrations) could be computed (Niinemets and Tenhunen
1997, Niinemets et al. 1999d). An estimate of Rd in this case
was calculated from linear regressions between net assimilation and dark mitochondrial respiration rates derived from the
whole set of available data (Figure A1). We assumed that mitochondrial respiration is suppressed by roughly 50% in light
as compared to dark (see Niinemets and Tenhunen 1997 for a
discussion).
The maximum carboxylase activity of Rubisco and Jmax
could be estimated by the routines outlined only if the Ci value
was available. For photosynthesis measurements at high CO2
concentrations (between 1 × 10 4 and 5 × 10 4 µmol mol –1) with
either an infrared CO2 analyzer or an oxygen electrode, lack of
Ci was remedied by using a constant ratio of intercellular to
ambient CO2 concentrations of 0.7. As CO2 concentrations increase, rates of photorespiration progressively decrease, photosynthesis becomes limited by Jmax, and the overall sensitivity
of photosynthesis to stomatal conductance decreases. Thus, I
consider the approximation employed to be reasonable (see
also Evans 1987).
Figure A1. Needle mitochondrial respiration versus needle light-saturated net photosynthesis rates per unit projected needle area in Picea
abies (䊉) and Pinus sylvestris (䊊). The linear regression lines were
forced through zero. Carbon dioxide concentrations in the gas-exchange cuvette were about 330–350 µmol mol –1, and needle temperatures varied from 15 to 27.5 °C with means ± SD of 22.1 ± 3.2 °C for
P. abies and 20.9 ± 3.9 °C for P. sylvestris. The data were derived from
the following studies: Szaniawski and Wierzbicki 1978, Brunes et al.
1980, Troeng and Linder 1982b, Schulze et al. 1985, Weikert et al.
1989, Hällgren et al. 1990, Korpilahti 1990, Wallin et al. 1990, 1992b,
Wedler 1991, Weih et al. 1994, Falge et al. 1996, Luoma 1997, Wieser
et al. 1998, Grassi and Minotta 2000, Jach and Ceulemans 2000,
Grassi et al. 2001.
The maximum rate of photosynthetic electron transport and
Vcmax were defined as the means of the three highest estimates.
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