Tree Physiology 21, 925–929
© 2001 Heron Publishing—Victoria, Canada
Photosynthesis and light-use efficiency by plants in a Canadian boreal
forest ecosystem
DAVID WHITEHEAD1 and STITH T. GOWER2
1
Landcare Research, P.O. Box 69, Lincoln 8152, New Zealand
2
Department of Forestry Ecology and Management, University of Wisconsin, Madison, WI 53706, USA
Received August 18, 2000
Summary Measurements of the photosynthetic response to
midsummer irradiance were made for 11 species representing
the dominant trees, understory shrubs, herbaceous plants and
moss species in an old black spruce (Picea mariana (Mill.)
B.S.P.) boreal forest ecosystem. Maximum rates of photosynthesis per unit foliage area at saturating irradiance, Amax, were
highest for aspen (Populus tremuloides Michx.), reaching
16 µmol m –2 s –1. For tamarack (Larix laricina (Du Roi)
K. Kock) and P. mariana, Amax was only 2.6 and 1.8 µmol m –2
s –1, respectively. Values of Amax for understory shrubs and herbaceous plants were clustered between 9 and 11 µmol m –2 s –1,
whereas Amax of feather moss (Pleurozium schreberi (Brid.)
Mitt.) reached only 1.9 µmol m –2 s –1. No corrections were
made for differences in shoot structure, but values of photosynthetic light-use efficiency were similar for most species
(70–80 mmol CO2 mol –1); however, they were much lower for
L. laricina and P. mariana (15 mmol CO2 mol –1) and much
higher for P. schreberi (102 mmol CO2 mol –1). There was a linear relationship between Amax and foliage nitrogen concentration on an area basis for the broad-leaved species in the canopy
and understory, but the data for P. mariana, L. laricina and
P. schreberi fell well below this line. We conclude that it is not
possible to scale photosynthesis from leaves to the canopy in
this ecosystem based on a single relationship between photosynthetic rate and foliage nitrogen concentration.
multi-layered canopies and to develop procedures for scaling
processes of CO2 exchange from leaves to canopies.
At a southern old black spruce site (Gower et al. 1997), a
comprehensive program of field measurements of photosynthesis at the leaf scale for the major tree species (Brooks et al.
1997, Dang et al. 1997a, Flanagan et al. 1997, Middleton et al.
1997, Sullivan et al. 1997) and moss understory (Goulden and
Crill 1997) provided the parameters appropriate for scaling
photosynthesis from leaves to canopies (Dang et al. 1997b).
However, there was little effort to compare rates of photosynthesis of trees and moss with those of understory shrubs and
herbaceous plants to estimate their contribution to canopy
photosynthesis.
Experimental evidence for a wide range of species (Field
and Mooney 1986), for the same species growing at different
sites (Dang et al. 1997b) and for leaves within a canopy
(Leuning et al. 1991) supports a linear relationship between
foliar nitrogen concentration and photosynthetic capacity,
which is useful for scaling photosynthesis from leaves to canopies (Leuning et al. 1995). However, it has not been determined if a linear relationship exists for all component species
within a stand. Thus, the objective of this study was to test the
hypothesis that foliar nitrogen concentration provides a means
of scaling photosynthesis for the plant components to provide
an estimate of canopy photosynthesis.
Keywords: foliar nitrogen concentration, irradiance, Larix
laricina, Picea mariana, Populus tremuloides, scaling.
Materials and methods
Site description
Introduction
To estimate global carbon balance, it is important to understand the processes regulating the exchange of CO2 between
vegetation and the atmosphere in boreal forests, because this
biome occupies about 17% of the vegetated surface of the
globe. From 1993 to 1996, detailed investigation of these processes at a wide range of scales in the boreal forests of Saskatchewan and Manitoba, Canada, was undertaken under the
auspices of a large international program (Sellers et al. 1997,
Margolis and Ryan 1997). Major objectives of this program
were to determine the contributions to ecosystem carbon balance made by components of the vegetation in mixed species,
Measurements were made at the southern boreal old black
spruce site near Candle Lake in the Prince Albert National
Park, Saskatchewan, Canada (53°53′ N, 104°53′ W, elevation
600 m). The forest is dominated by black spruce (Picea
mariana (Mill.) B.S.P.) and, in better drained areas, tamarack
(Larix laricina (Du Roi) K. Kock). Trembling aspen (Populus
tremuloides Michx.) occurs as isolated individual trees. Tree
leaf area index was between 4 and 5 (Gower et al. 1997). The
understory consists of a wide range of shrubs and herbaceous
species, but is dominated by Labrador tea (Ledum groenlandicum Oeder) and wild rose (Rosa spp.). Ground cover consists
of feather moss (Pleurozium schreberi (Brid.) Mitt.). The site
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WHITEHEAD AND GOWER
is poorly drained and the soil consists of a 200–300-mm deep
layer of peat over a coarse-textured mineral soil.
Measurements were made on 11 species comprising dominant representatives of overstory trees, understory shrubs, herbaceous plants and moss. The species and mean heights are
shown in Table 1.
Photosynthesis measurements
The response of photosynthesis, A, to incident irradiance, Q,
was measured in the field during dry, summer conditions for
the 11 species by placing leaves or shoots in a cuvette of a portable photosynthesis system (Model LI-6400, Li-Cor, Inc.,
Lincoln, NE) with an artificial light source. The temperature
of the cuvette was controlled at 20 °C and measurements were
made at ambient CO2 concentration and humidity. For the
dominant tree species, the shoots were equilibrated at an incident quantum flux (400–700 nm) of 2000 µmol m –2 s –1 and
measurements of photosynthesis were made as the irradiance
was reduced in 12 steps to darkness. The same procedure was
followed for the understory and moss species, but the initial
quantum flux was set at 500 µmol m –2 s –1.
After completing the curves, leaf area in the cuvette was
measured with a Li-Cor leaf area meter (Model LI-3000). For
the leaf area measurements, individual needles from the
P. mariana and L. laricina shoots were separated and held flat
between two plastic sheets. Calculations of one-sided leaf area
were made based on the shape of the needles. All results in this
paper are expressed on a one-sided leaf area basis. The leaves
were dried at 70 °C, weighed, then finely ground for analysis
of total nitrogen concentration with a CNS analyzer (Carlo
Erba Ltd., Italy).
The response of A to Q was fitted to the non-rectangular hy-
Table 1. List of study species. Measurements of height for the tree
species are taken from Gower et al. (1997) and heights of the understory shrubs and herbaceous plants are means (± standard error) of
30 measurements.
Species
Common name
Height (m)
Dominant trees
Larix laricina
Populus tremuloides
Picea mariana
Tamarack
Trembling aspen
Black spruce
10–16
20.1
7.2
Understory shrubs
Betula glandulosa Michx.
Salix serissima (Bailey) Fern.
Potentilla fruticosa L.
Rosa acicularis Lindl.
Ledum groenlandicum
Bog birch
Autumn willow
Shrubby cinquefoil
Prickly rose
Labrador tea
0.82 ± 0.03
0.67 ± 0.04
0.52 ± 0.03
0.20 ± 0.02
0.38 ± 0.02
Herbaceous plants
Anemone quinquefoia
Cornus canadensis
Wood anemone
Bunch berry
0.09 ± 0.005
0.10 ± 0.003
Moss
Pleurozium schreberi
Feather moss
0.02
perbolic function (Farquhar and Wong 1984) described by:
θ ( A + Rd )2 − (ε Q + Amax )( A + R d ) + εQAmax = 0,
(1)
where Amax is maximum rate of photosynthesis at saturating
irradiance, Rd is rate of respiration in the dark, θ defines the
convexity of the response curve, and ε, the initial slope of the
curve, is the photosynthetic light-use efficiency.
Results
For the study species, Amax varied between 1.8 and 20 µmol
m –2 s –1. The responses of A to Q for the species are indicated
by the differences in the shapes of the curves in Figure 1. Each
curve was generated based on means of the parameter values
for the species. For P. tremuloides, A increased rapidly with
increasing Q up to 500 µmol m –2 s –1, then continued to increase without reaching full saturation even when Q exceeded
1500 µmol m –2 s –1. The Amax for P. tremuloides was close to
16 µmol m –2 s –1. In contrast, the dominant tree species
P. mariana and L. laricina reached Amax (1.8 and 2.6 µmol m –2
s –1, respectively) at a Q of about 1000 µmol m –2 s –1. For the
understory shrubs, Amax ranged from 9 to 11 µmol m –2 s –1,
with a lower rate for L. groenlandicum of 5.9 µmol m –2 s –1,
reaching saturation at Q > 500 µmol m –2 s –1. For the two herbaceous plants, Amax of Anemone quinquefoia L. was similar to
that for the understory shrubs and Amax for Cornus canadensis L. was similar to that for L. groenlandicum. The moss
P. schreberi had an Amax of 2.0 µmol m –2 s –1, and reached saturation at low values of Q (< 100 µmol m –2 s –1).
Values of photosynthetic light-use efficiency, ε, were in the
range of 70 to 85 mmol CO2 mol –1 for most of the study species (Figure 2). However, exceptionally low ε values were
found for P. mariana (15 mmol CO2 mol –1) and L. laricina
(16 mmol CO2 mol –1). In contrast, ε for P. schreberi was high
at 102 mmol CO2 mol –1.
When data for all species were combined, there was a trend
of increasing Amax with increasing foliar nitrogen concentration expressed on a leaf area basis (Figure 3). However, the
data for L. laricina, P. mariana and P. schreberi fell well below the line. The high Amax for P. tremuloides is attributable to
high foliar nitrogen concentration, whereas the low Amax values for P. schreberi and, to a lesser extent, for L. groenlandicum and C. canadensis, were associated with low foliar
nitrogen concentrations. However, in P. mariana, Amax was
low even though foliar nitrogen concentration was reasonably
high. There was no clear relationship between ε and foliar nitrogen concentration.
Discussion
Photosynthetic rates of P. mariana shoots at our site (Figure 1)
are similar to the low rates that have been measured previously
in more intensive studies. Brooks et al. (1997), Flanagan et al. (1997) and Middleton et al. (1997) determined a
mean photosynthetic rate at saturating irradiance in midsum-
TREE PHYSIOLOGY VOLUME 21, 2001
PHOTOSYNTHESIS IN A BOREAL FOREST ECOSYSTEM
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Figure 1. Relationship between photosynthesis and incident irradiance for leaves of
the 11 study species. The
curves are generated from the
non-rectangular hyperbola
given in Equation 1 based on
the mean parameters for each
species.
mer of 3 µmol m –2 s –1. Sullivan et al. (1997) reported a seasonal mean A of 2.7 µmol m –2 s –1. However, maximum rates
of photosynthesis of P. mariana shoots measured with an oxygen electrode under conditions of saturating irradiance and
CO2 concentration were 19 µmol m –2 s –1 (Middleton et al.
1997, Sullivan et al. 1997). Similarly, for L. laricina, the low
rates of photosynthesis are close to the value of 2.2 µmol m –2
s –1 reported by MacDonald and Lieffers (1990) and
Dang et al. (1991). Measurements of diffusive conductance
for both P. mariana and L. laricina (MacDonald and
Lieffers 1990, Dang et al. 1991) suggest that photosynthesis is
restricted principally by low mesophyll conductance rather
than stomatal limitation. However, strong correlations between stomatal conductance and photosynthesis (Sullivan et al. 1997), and the marked sensitivity of conductance to
increasing air saturation deficit, particularly in late summer
(Dang et al. 1997a), suggest that the low photosynthetic rates
of P. mariana under field conditions are attributable to low
stomatal conductance (Flanagan et al. 1997).
Figure 2. Values of maximum photosynthetic rate at saturating irradiance (Amax) and photosynthetic light-use efficiency (ε). The data are
means of six measurements for each species and the bars indicate one
standard error. The shading patterns from left to right classify the
plants into dominant trees, understory shrubs, herbaceous plants and
moss (see Table 1).
Figure 3. Relationship between maximum rate of photosynthesis at
saturating irradiance (Amax) and foliar nitrogen concentration per unit
leaf area (N) for the species measured. The line shown is a linear regression through the data, excluding points for Picea mariana, Larix
laricina and Pleurozium schreberi, giving the relationship Amax =
0.047N + 6.871, r 2 = 0.68.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
928
WHITEHEAD AND GOWER
Photosynthetic rates were much higher for P. tremuloides
than for P. mariana and L. laricina (Figures 1 and 2). This is
consistent with the midsummer peak value of A for
P. tremuloides of 12.6 µmol m –2 s –1 (Middleton et al. 1997) to
15 µmol m –2 s –1 (Brooks et al. 1997, Flanagan et al. 1997).
The difference in photosynthetic rates between P. tremuloides
and P. mariana is attributed to higher values of stomatal conductance for P. tremuloides than for P. mariana, despite
greater sensitivity of conductance to air saturation deficit for
P. tremuloides compared with P. mariana (Dang et al. 1997a).
Photosynthetic rates for the moss P. schreberi were low
(Figure 1) and saturation was reached at a Q < 100 µmol m –2
s –1. These photosynthetic rates are not directly comparable
with the measurements that were made by Goulden and
Crill (1997) on a ground area basis with large chambers. Furthermore, our measurements of net photosynthesis were restricted to the green component. However, in both studies,
photosynthesis was maximal at similar values of Q.
The dominant tree species at the study site was P. mariana,
accounting for 87% of the basal area. Larix laricina comprised
a much smaller component, accounting for a further 5% of
basal area (Gower et al. 1997). Populus tremuloides trees occurred only as isolated individuals. Thus, despite high photosynthetic rates for P. tremuloides, low A and high rates of respiration by P. mariana and L. laricina resulted in low rates of
net carbon uptake by the forest canopy (Pattey et al. 1997).
Nevertheless, net carbon uptake was sufficient for this ecosystem to be a significant carbon sink, at least during the summer
growing season (Jarvis et al. 1997).
During periods following rain, up to 50% of carbon uptake
by the whole ecosystem is attributable to moss (Goulden and
Crill 1997). This highlights the significance of the large surface area of moss and its high photosynthetic light-use efficiency (Figure 2), enabling net carbon uptake at irradiances at
the forest floor as low as 20 to 40 µmol m –2 s –1 even in clear
sky conditions (Goulden et al. 1997). Although the understory
shrubs and herbaceous plants had moderate photosynthetic
rates (Figures 1 and 2), it is unlikely that their contribution to
ecosystem carbon uptake was high because of their low leaf
area index. The species with the largest leaf area was L. groenlandicum, but its Amax was the lowest among the woody shrubs
and herbaceous plants. However, similar to some prairie
grasses (Heckathorn and DeLucia 1991), the propensity of
L. groenlandicum to roll its leaves during dry periods may facilitate its prolonged contribution to ecosystem carbon uptake
during summer dry periods.
Photosynthetic light-use efficiency of most of the study species was similar, with a mean of 76 mmol CO2 mol –1 (Figure 3); however, we found higher values for P. schreberi and
lower values for L. laricina and P. mariana. The low value of
15 mmol CO2 mol –1 for P. mariana and L. laricina is in agreement with the mean value of 37 mmol CO2 mol –1 reported for
the same species at saturating CO2 concentration (Sullivan
et al. 1997). However, we note that our comparative estimates
of photosynthetic light-use efficiency for the different species
do not take into account the effects of complex shoot geometry
on radiation interception. To compare data for the complex
shoot structures of P. mariana, L. laricina and P. schreberi
with each other and with broad-leaved species, measurements
of the ratio of projected shoot area to total surface area (Stenberg 1996) are required to calculate the degree of self-shading
and the actual surface area illuminated. These measurements
were not made for the species at our site, so the estimates of
photosynthetic light-use efficiency should be considered tentative.
The vertical distribution of photosynthetic capacity within
stands (Dang et al. 1997b) and differences in rates of photosynthesis among tree species in boreal forests (Brooks et al.
1997) are related to differences in foliar nitrogen concentration. Furthermore, a linear relationship can be drawn through
our data for broad-leaved species in the canopy and understory
(Figure 3); however, the data for P. mariana, L. laricina and
P. schreberi fall well below this line. We suggest, therefore,
that the relationship between photosynthesis and foliar nitrogen concentration for the dominant conifers and the moss differs from that for the broad-leaved species in the canopy and
understory. Thus, the “universal” slope for the relationship between Amax and nitrogen concentration for a wide range of species from different biomes reported by Reich et al. (1999) does
not hold for species in different canopy layers within a single
ecosystem. We conclude that scaling photosynthesis from
leaves to the canopy for this boreal ecosystem requires more
information than leaf area, nitrogen concentration and the employment of a radiative transfer model (Leuning et al. 1995,
Dang et al. 1997b).
Acknowledgments
This work was supported by the Foundation for Research, Science
and Technology, New Zealand and funding from NSF and NASA to
Stith Gower. David Whitehead sincerely thanks Stith Gower and the
TE6 team for inviting him to the site.
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