Tree Physiology 22, 219–229
© 2002 Heron Publishing—Victoria, Canada
Photosynthesis and respiration of black spruce at three organizational
scales: shoot, branch and canopy
M. B. RAYMENT,1,2 D. LOUSTAU3 and P. G. JARVIS1
1
IERM, University of Edinburgh, Edinburgh EH9 3JU, U.K.
2
Author to whom correspondence should be addressed ([email protected])
3
INRA-Forets, BP 45, 33611 Gazinet, France
Received March 16, 2001; accepted August 18, 2001; published online February 1, 2001
Summary To gain insight into the function of photosynthesis and respiration as processes operating within a global ecosystem, we measured gas exchange of mature black spruce
(Picea mariana (Mill.) B.S.P.) trees at three organizational
scales: individual shoots, whole branches and a forest canopy.
A biochemical model was fitted to these data, and physiological parameters were extracted. Pronounced seasonal variation
in the estimated model parameters was found at all three organizational scales, highlighting the need to make physiological
measurements throughout the year. For example, it took over
100 days for physiological activity to increase from zero during the springtime thaw to its yearly maximum. Good agreement was found between parameter values estimated for the
different organizational scales, suggesting that, in the case of
aerodynamically rough, largely mono-specific forest canopies,
physiological parameters can be estimated from eddy covariance flux measurements. The small differences between
photosynthetic parameters estimated at the different scales
suggest that the overall spatial organization of photosynthetic
capacity is nearly optimized for carbon uptake at each scale.
Keywords: BOREAS, Picea mariana, scaling.
Introduction
In recent years, considerable effort has been put into largescale field experiments aimed at improving our understanding
of the interactions between the land surface and the lower atmosphere (e.g., FIFE (Sellers et al. 1992), BOREAS (Sellers
et al. 1997)). A major objective has been to develop and
parameterize simulation models of the processes controlling
the exchange of gases and energy between the biosphere and
the atmosphere. The parameterized models, together with remote sensing, can then be used to facilitate the integration of
these processes over areas larger than the initial study site
(e.g., a land surface parameterization for the entire boreal forest from two sites in central Canada). The parameterized models also enable computer simulations of the likely biological
effects of possible future climates.
The extraction of physiologically meaningful parameters
from measured flux data is an essential part of this modeling
procedure because such parameters can help us understand
how mass and energy fluxes can be scaled up in space and
time. Analysis of physiological parameters may also help us
understand the biology of the ecosystem. For example, physiological parameters could be used to determine whether variation in growth rates of branches at different heights in the
canopy is a straightforward consequence of different incident
photon flux densities (PFD), or whether branches become
physiologically acclimated to their differing light environments. Similarly, physiological parameters could be used to
determine if part of the seasonality observed in ecosystem behavior is a function of biological changes in the biosphere and
not simply a reflection of seasonality in the climate. Physiological parameters also provide a basis for quantitative comparisons of ecosystem function among different ecosystems.
The time constants of most biological control processes
vary from minutes to years, and their assessment is essential
for predicting the behavior of vegetation canopies. If model
parameterizations based on short-term measurements of physiological behavior are inappropriate for the whole season, the
biological function must be monitored throughout the year and
perhaps over a number of years. A convenient way of acquiring
long-term data for foliage in a forest ecosystem is with automated branch bags that measure gas exchange of whole
branches by infrared gas analysis (Dufrêne et al. 1993, Saugier
et al. 1997). From data collected over a long period, it is possible to derive model parameters from the natural variation in
the driving environmental variables.
A complete description of photosynthesis, however, is only
possible when the physiology is studied outside the range of
normal environmental variation. This is particularly true in the
case of the response of photosynthesis to increased concentrations of CO2. Conventional methods used to characterize
ecophysiolocal functions (e.g., stomatal action or photosynthetic capacity) are typically carried out at the tissue or organ
scales, and the results scaled up to the whole canopy. In practice, however, the procedures used for scaling between organizational scales are seldom validated. This is primarily because
measurements of whole-canopy exchanges made, for example, with the eddy covariance technique, measure the summation of all the ecosystem exchange processes, of which canopy
220
RAYMENT, LOUSTAU AND JARVIS
exchange is but one. Therefore, before whole canopy data can
be used to validate scaling methods, the other biotic processes
(notably heterotrophic respiration in the soil) need to be accounted for.
It may be possible to scale up measurements made at the
leaf or shoot scale to some intermediate scale (e.g., the
branch), enabling validation of the procedures against direct
measurements at a range of scales. Success in scaling from
leaf to branch then gives the confidence to apply these procedures to scaling from leaves to the entire canopy.
This paper describes a study of photosynthesis and respiration of the most extensive Canadian boreal forest tree species,
black spruce (Picea mariana (Mill.) B.S.P.), based on gas exchange measurements made at three organizational scales:
shoot, branch and canopy. Variation in physiological parameters over the course of a year and between organizational
scales was investigated. Transpiration and conductance measurements were made at the same time and are described in a
companion paper (Rayment et al. 2000).
Materials and methods
The study was made at the BOREAS southern study area
(SSA) old black spruce (OBS) site in northern Saskatchewan,
Canada, during 1996. A full description of the site is given by
Jarvis et al. (1997).
Gas exchange
Shoot measurements In July and October 1996, measurements were made on shoots in the upper, mid- or lower crown
of four black spruce trees. Each measured shoot had a total
needle area of about 70 cm2 and comprised four to seven needle age classes (typically, needles were retained for up to
10 years). One intercellular CO2 concentration (ci) and one
photosynthetic photon flux density (400 to 700 nm) (Q) response curve of net CO2 assimilation rate, transpiration and
stomatal conductance was made for each of 14 shoots in July
and six shoots in October using an open gas exchange system
with climate control (Compact Minicuvette System, Walz,
Effeltrich, Germany). Shoots were placed horizontally in the
cuvette and received bilateral illumination from two fiber-optic
illuminators (Walz) comprising 200 parallel optical fibers applied to the glass lid of the cuvette at a distance of 3 cm from the
needle surface. The ci response curves were determined by
varying ambient CO2 mole fraction (ca) from 1500 to 0 µmol
mol –1 in saturating Q (1500 µmol m –2 s –1 at the needle surface).
The Q response curves were determined by varying Q from
1100 to 0 µmol m –2 s –1, with ambient CO2 concentration (ca )
set to 1500 µmol mol –1. Air temperature was set at 17.5 °C, and
dew point temperature was set at 8 °C. Because illumination
was bilateral, gas exchange was calculated on an illuminated
needle area basis, i.e., 2.54 times projected area.
In July, temperature responses of gas exchange were determined for five shoots both in the dark and at an irradiance of
1200 µmol m –2 s –1. These measurements were repeated on six
different shoots in October. After several hours acclimation to
20 °C, each shoot was placed in the cuvette at 30 °C. Data were
recorded when gas exchange reached a steady state. The temperature response measurements were repeated as the cuvette
temperature was decreased from 30 to 5 °C, in 5 °C steps. At
each temperature, an equilibration time of about 40 min was
required. Based on the assumption that daytime shoot respiration rates are similar to nighttime shoot respiration rates, the
temperature response of shoot respiration was determined
with the protocol described, but with the cuvette enclosed in
aluminum foil.
After completion of the gas exchange measurements, the
shoots were excised. The needles of each shoot were dried at
65 °C and weighed according to their age class. Total needle
surface area was estimated based on values of specific needle
area measured on 30 samples each of five needles. The total
surface areas of the 30 samples were calculated from their
length and width assuming a rhomboidal cross section with a
shape factor (i.e., the ratio of total to projected area) of 2.54. A
different specific needle area was applied to each needle age
class, but no significant differences in specific needle area
were found with respect to needle location in the crown. Total
N and P contents of the needles were determined after digestion in hot sulfuric acid by the Kjeldahl method and molybdate
ascorbate method, respectively, using an automated analyzer
(Autoanalyser II, Technicon, Dublin, Ireland). In October,
subsamples of fresh needles of each shoot were frozen in the
field and transported to the laboratory for chlorophyll analysis.
Branch measurements We used ventilated closed-system
branch bags according to the methodology developed at the
Université Paris Sud-Orsay (Dufrêne et al. 1993). The branch
bags have been described by Rayment and Jarvis (1999a) and
Rayment et al. (2000), and are discussed only briefly here. Two
branch bags were installed on each of two trees, one bag was
positioned in the upper canopy (8 m height) and one in the
lower canopy (5.3 m height). Modal tree height was about
10.2 m. Water vapor and CO2 exchange were measured on each
branch every 20 min, together with air and leaf temperature, incident Q and relative humidity. At the end of the year, the
branches were excised and needle area, needle and wood dry
mass and chlorophyll and nutrient contents were measured for
current-year and all previous years’ needles (see Rayment and
Jarvis 1999a).
Canopy measurements An eddy covariance flux measuring
station was installed with the anemometer and gas analyzer intake positioned at 27 m height. The system comprised a closed
path infrared gas analyzer (LI-6262, Li-Cor, Lincoln, NE),
an ultrasonic anemometer (Solent A1012R, Gill Instruments,
Lymington, England) and Edinburgh EdiSol software. The full
technical specification is described in detail by Moncrieff et al.
(1997). An automatic weather station mounted close to the
eddy flux system recorded a full suite of meteorological data. A
complete description of the equipment installation is given by
Jarvis et al. (1997).
Tree canopy CO2 exchange data were extracted from the net
ecosystem flux data by correcting for the simultaneous fluxes
of CO2 from soil respiration and moss photosynthesis. The
measurement and spatial integration methods used to deter-
TREE PHYSIOLOGY VOLUME 22, 2002
PHYSIOLOGY AT THREE ORGANIZATIONAL SCALES
mine soil respiration are described by Rayment and Jarvis
(1997) and Rayment and Jarvis (1999b), respectively. Moss
photosynthetic rates were predicted from data provided by
L.B. Flanagan (Carlton University, Ottawa, ON, Canada). The
fluxes measured at the canopy scale differed from measurements made at the shoot and branch scales in that the data represented a 30-min mean rather than measurements over
shorter periods.
Model parameterization: photosynthesis
Shoot measurements Net CO2 assimilation rate (A; µmol CO2
m –2 s –1), transpiration (E; mmol H2O m –2 s –1), stomatal conductance for water vapor (gw; mmol H2O m –2 s –1) and for CO2
(gc; mmol CO2 m –2 s –1) and substomatal, intercellular CO2
mole fraction (ci ) were calculated according to von Caemmerer
and Farquhar (1981). A full description of the calculation of the
boundary layer and stomatal conductances, and the models derived to describe them are given in Rayment et al. (2000). Maximal velocity of carboxylation (Vmax), observed maximal
electron transport rate (Jmax; µmol e– m –2 s –1), daytime “dark”
respiration (R d; µmol CO2 m –2 s –1) and apparent quantum efficiency of electron transport (α; µmol e– µmol –1 quanta) were
determined from the response curves obtained with each shoot
(assuming that CO2 mole fractions in chloroplasts (c c) and
substomatal intercellular spaces (c i ) were equal), based on the
photosynthesis model proposed by Farquhar et al. (1980) and
modified by subsequent authors (Harley et al. 1992, Lewis et
al. 1994, Walcroft et al. 1997).
All model parameters were extracted from the data by least
squares analysis using the SAS NLIN or REG procedures.
Branch measurements Branch bag data were used only when
the regression line through the concentration versus time data
points (from which the flux was calculated) fitted the data with
an r 2 value > 0.95. Photosynthetic models were fitted only to
data collected in the daytime, defined as the period when incident Q was > 3 µmol m –2 s –1.
The von Caemmerer and Farquhar (1981) model of photosynthesis describes carbon assimilation rate as the minimum
of two potential limitations: the carboxylation-limited rate
(Av) and the RuBP regeneration (electron transport)-limited
rate (Aj). Parameters Vmax, Jmax and θ (the convexity of the light
response curve of Jmax) are typically determined by analysis of
the response of photosynthetic CO2 uptake to experimental
changes in ci. Despite only a limited natural variation in ci
in our study (330 µmol mol –1 < ci < 400 µmol mol –1 for all
branches), it was possible to determine analytically the environmental criteria under which the photosynthetic rate could
be guaranteed to be limited by either carboxylation or RuBP
regeneration. Figure 1a shows an analysis of a part of the
Farquhar model. It is clear that, for the range of ci experienced,
photosynthesis proceeds at the carboxylation-limited rate (Av)
when needle temperature is below 25 °C and Q is above
500 µmol m –2 s –1. Similarly, Figure 1b illustrates that photosynthesis proceeds at the RuBP regeneration-limited rate (Aj)
when ci is between 330 and 400 µmol mol –1, Q is less than
170 µmol m –2 s –1 and needle temperature is above 15 °C.
221
These criteria were obtained by iteratively setting criteria under which photosynthesis was limited by carboxylation in order to determine Vmax, then prescribing this parameter and θ
(0.677) and fitting the full Farquhar model to all daytime data
to determine Jmax. Parameters R d and α were estimated from
the A–Q response function at Q < 50 µmol m –2 s –1.
These conditions provided enough data points for accurate
determination of Vmax by nonlinear regression. The more severely restricting conditions imposed to ensure limitation by
RuBP regeneration (high temperature plus low light) resulted
in fewer data being available to estimate the parameters describing this limitation. In addition, when environmental conditions were such that photosynthesis was limited by Aj (i.e.,
high temperature plus low light), the actual electron transport
rate was much less than Jmax (see Figure 1a), so Jmax could be
estimated only by extrapolation. Consequently, the confidence
intervals for Jmax and θ were broad. Moreover, parameters Jmax
and θ are highly correlated when obtained by fitting the model
to measurements made in normal environmental conditions.
Therefore, θ was fixed at the value found at the shoot scale
(0.677) and Jmax was determined by first estimating Vmax
(based on the low temperature plus high light criteria), then
prescribing this parameter in a procedure to fit the full Farquhar model to all the daytime data. The temperature response
parameters for Vmax, Jmax and R d were set equal to the values
determined at the shoot level. To investigate changes in these
parameters over time, the data were grouped into consecutive
20-day periods.
Canopy measurements Effects of changes in CO2 concentration of the air column below the eddy covariance sensor (the
so-called storage flux) were added to the eddy covariance data
to yield the biotic flux, i.e., biotic flux = eddy flux + storage
flux. From this biotic flux, the forest floor CO2 flux (Rayment
and Jarvis 1999b) was subtracted, resulting in a measure of gas
exchange of the aboveground parts of the canopy. Parameters
for the Farquhar model of photosynthesis were extracted from
the canopy data by the same iterative process as for the branch
data. Likewise, the canopy data were also grouped into consecutive 20-day periods. The temperature response parameters for
Vmax, Jmax and R d were set equal to the values determined at the
shoot level, and R d and α were estimated from the A–Q response function at Q < 50 µmol m –2 s –1.
Model parameterization: respiration
An Arrhenius “activation energy” temperature response (e.g.,
Lloyd and Taylor 1994) was fitted to the shoot, branch and
canopy data collected when Q = 0 µmol m –2 s –1. The model
was of the form:
29315
. 
 E0  
R T = R20 exp 
 1 −
,
 29315


T 
. R
(1)
where RT is CO2 efflux rate (µmol CO2 m –2 s –1) at needle temperature T (K), R20 is efflux rate at 20 °C, R is the gas constant
(8.314 J mol –1 K –1) and E0 is the activation energy (56,734 J
mol –1 K –1) determined from shoot measurements.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
222
RAYMENT, LOUSTAU AND JARVIS
Figure 1. Carboxylation rate (Av; µmol
CO2 m –2 s –1) and potential electron
transport rate (Aj; µmol e– m –2 s –1)
versus (a) incident photosynthetic photon flux density (Q; µmol m –2 s –1) and
(b) needle temperature calculated from
the Farquhar model (Tl; °C). Parameters Vmax and Jmax were determined
iteratively from data; values of other
parameters are given in the text.
Although for needle-leaf plants RT and T are usually well
coupled, needle temperature was used as the driving variable
for the shoot and branch flux measurements, but air temperature was used for the canopy measurements. For both the
branch- and canopy-scale measurements, the data were
grouped into consecutive 20-day periods, and the respiration
models were fitted to the data when incident Q = 0. The canopy data were further screened to exclude periods when turbulence was considered too low for the eddy covariance
technique to produce reliable data, thus the models were fitted
to data collected when the friction velocity (U*) was above
0.35 m s –1 (Jarvis et al. 1997). Because the majority of nighttime respiration derives from soil efflux (M.B. Rayment,
poster presentation at the XXth EGS Conference, Hamburg,
Germany, 1995), and the estimate for the spatially integrated
rate of soil efflux was itself derived from a model in which the
main driving variable was temperature (Rayment and Jarvis
1999b), net ecosystem flux data were not corrected for soil
CO2 efflux to avoid the circularity of fitting a model to
model-derived data.
Results
Shoot photosynthesis
Table 1 shows the values of Vmax, Jmax, θ, R d and α in shoots in
July and October. There was no relationship between Vmax and
the position of the shoot in the canopy; however, there was a
significant difference (P < 0.05) in Jmax between the upper and
lower canopy. Between July and October, Vmax tended to decrease in shoots in the middle of the canopy, whereas Jmax, θ
and α measured in the same shoots decreased significantly
(P < 0.05) over the same period. Estimated mean values of
Vmax, Jmax, R d and α for shoots are superimposed on the estimates of these parameters for branches and the canopy in Figure 2.
TREE PHYSIOLOGY VOLUME 22, 2002
PHYSIOLOGY AT THREE ORGANIZATIONAL SCALES
223
Table 1. Mean values (± 95% confidence intervals) of the parameters Vmax, Jmax, θ, R d and α of the Farquhar model of photosynthesis (Equations 2–8). Values were estimated from A–ci and A–Q response functions made on 14 shoots in the upper, mid- and lower canopy at the BOREAS
SSA OBS site in July and October 1996.
Period
Shoot position
(n)
Vmax
(µmol CO2 m –2 s –1)
Jmax
(µmol e– m –2 s –1)
θ
Rd
(µmol CO2 m –2 s –1)
α
(mol e– mol –1 quanta)
July
July
July
Oct
Upper (6)
Mid (5)
Lower (3)
Mid (6)
16.0 ± 5.5
15.8 ± 4.1
23.7 ± 9.5
13.5 ± 2.6
64.1 ± 15.6
47.1 ± 6.5
46.6 ± 10.9
26.9 ± 12.8
0.64 ± 0.10
0.73 ± 0.09
0.66 ± 0.13
0.43 ± 0.28
0.72 ± 0.27
0.53 ± 0.55
0.75 ± 0.92
0.45 ± 0.21
0.24 ± 0.07
0.21 ± 0.03
0.24 ± 0.08
0.06 ± 0.04
Branch nighttime respiration
Neither nitrogen (N) nor phosphorus (P) concentration of
the needles used for gas exchange measurements differed significantly between crown levels (Table 2). In contrast, there
was a significant effect (P < 0.05) of needle age class on needle
P concentration, with the highest concentration in the youngest needles. This effect was almost significant (P = 0.078) for
N concentration. Specific needle area did not differ between
crown levels but was significantly higher (P < 0.05) in the current-year needles, i.e., age class 1996, than in older needles.
The patterns of distribution of N and P were still significant
when N and P concentrations were expressed on a surface area
basis, i.e., when age differences were not accounted for by the
differences in specific needle area.
Figure 3 shows the seasonal time courses of parameters for
the temperature response of nighttime respiration for the
branches. The R20 was significantly higher (P < 0.05) around
Day 100 and Day 300 than in the middle of the year, although
the highest respiration rates were observed in the middle of the
year. Between the springtime thaw and Day 140, there was a
gradual decrease in temperature sensitivity. Between Day 140
and Day 300, E0 varied little. After Day 300, temperature sensitivity increased rapidly. There were no consistent significant
differences among the respiration parameters for the different
branches, although differences between individual 20-day periods were significant.
Branch photosynthesis
Canopy respiration
Figure 2 shows the values of Vmax, Jmax, R d and α derived for
the branches for successive 20-day periods. There was pronounced seasonality in both Vmax and Jmax for all branches.
Both parameters were close to zero at the start of the measurement period, peaked during the summer and declined later in
the year. Values of R d and α were both zero at the beginning
and end of the measurement period; R d reached a maximum in
midsummer and α reached a maximum around Day 220.
The seasonal time courses of the parameters for the net ecosystem response of respiration to temperature are given in Figure 3. After an initial decline, R20 increased until the middle of
the year, then decreased to nearly zero by the end of the measurement period. Nighttime respiration rates measured at the
start and end of the measurement period were similar. There
was considerable variation in E 0 throughout the year, although
the 95% confidence limits were large.
Canopy photosynthesis
Values of Vmax, Jmax and α derived for the canopy for successive 20-day periods are shown in Figure 2. Both Vmax and Jmax
were low at the start of the measurement period, reached maxima in late summer and declined later in the year. Parameter α
followed a similar seasonal time course to Vmax and Jmax, but
there was a marked reduction in α in the middle of the year
even though the 95% confidence intervals for estimated α
were large.
Shoot nighttime respiration
Parameter values for the respiration model (Equation 1) fitted
to the shoot data are given in Table 3. Shoot position in the canopy had no significant effect on any of the parameters. Although not statistically significant (because of the small
sample size), shoot respiration rate at 20 °C (R20) was reduced
by half between July and October. A small increase in temperature sensitivity was observed over the same period. Mean values for R20 and E0 measured on shoots are superimposed on the
estimates of these parameters for the branches and for the canopy in Figure 3.
Discussion
Temporal variation
Large variation in photosynthesis and respiration parameters
over time is an important characteristic of this boreal forest.
There was a marked ramping up of the parameters describing
biochemical activity (Vmax, Jmax and α) from the time that air
temperature first rose above zero at the start of the season (Day
98; see Figure 2). This steady rise in activity continued even
after air temperature had reached a seasonal maximum and
daily incident Q had started to decrease. Parameter Vmax continued to increase until a severe drop in air temperature occurred around Day 250, whereupon it started to decline.
Despite the large seasonal variation in Vmax and Jmax, the temperature responses of these parameters changed little between
summer and winter, i.e., activation energies were constant and
there was no evidence of photosynthetic acclimation to seasonal temperature change (D. Loustau et al., unpublished
data). For the branches and the canopy, a large part of the annual variation in Vmax was closely correlated with changes in
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
224
RAYMENT, LOUSTAU AND JARVIS
Figure 2. (a) Seasonal course of maximum rate of carboxylation (Vmax),
(b) light-saturated rate of electron
transport (Jmax), (c) seasonal course of
daytime “dark” respiration (Rd) and
(d) apparent quantum efficiency of
electron transport (α) of the Farquhar
model of photosynthesis for shoots
(䉮), branches (䊊, 䊉) and canopy (䉭,
䉱) at the BOREAS SSA OBS site
from April to December 1996. Each
value was calculated from measurements averaged over a 20-day period.
Two values are given: the rate corrected to 20 °C and the actual rate
measured. Note that canopy values
have been divided by the leaf area index, such that all parameters are expressed on an illuminated area basis.
Error bars represent 95% confidence
limits for the parameter estimates.
Vmax20. This suggests that the observed seasonality in Vmax reflects a seasonal change in photosynthetic activity at the biochemical level rather than at the environmental level, and any
direct effects of temperature on Vmax must have been mainly
limited to short-term (diurnal) temperature variations. Dang et
al. (1998) reported that differences between photosynthetic
TREE PHYSIOLOGY VOLUME 22, 2002
PHYSIOLOGY AT THREE ORGANIZATIONAL SCALES
225
Table 2. Specific needle area (± 95% confidence intervals) and needle nutrient concentrations averaged with respect to age class and vertical position in the canopy in 1996 at the BOREAS SSA OBS site. In July 1996, needles were sampled on shoots collected at three heights in the canopy
(upper, mid- and lower) from five trees with a total sample size of n = 61. In October 1996, 15 shoots were collected from the mid-canopy level
only (Oct), and total sample size was n = 59.
Shoot position
Needle age class
1992
1993
1994
1995
1996
All
7.6
11.0
7.8
6.8
7.1
7.5
–
6.8
N concentration (mg g –1)
Upper
Mid
(Oct)
Lower
5.2
5.8
–
–
6.3
6.3
6.4
6.6
7.3
6.8
7.4
6.8
7.2
6.1
7.5
7.0
P concentration (mg g –1)
Upper
Mid
(Oct)
Lower
0.47
0.51
0.49
–
0.63
0.50
0.59
0.56
0.66
0.54
0.60
0.59
0.64
0.51
0.62
0.59
Specific needle area (cm2 g –1)
Upper
Mid
Lower
39.6 ± 0.3
39.7 ± 0.8
41.2 ± 0.9
42.6 ± 1.7
42.4 ± 3.7
40.5 ± 1.8
38.7 ± 3.6
40.6 ± 1.9
42.0 ± 0.4
43.8 ± 2.9
43.7 ± 1.0
44.8 ± 3.8
parameters estimated for black spruce in each of three intensive field campaigns were small; however, their earliest measurement on black spruce was made on Day 157, at the end of
the ramping-up period (see Figure 2a).
Several environmental variables such as the timing of the
soil thaw and freeze, the seasonal pattern of soil temperature
and soil water availability, the occurrence of spring and autumn frosts, and late summer reduction in atmospheric humidity, co-varied with photosynthetic capacity (Pmax) at the OBS
site in 1996. All of these factors may contribute to the seasonality in Pmax in the boreal forest. However, generalizations cannot be drawn from data based on a single year of physiological
observations.
The high values of R20 around Day 100 coincided with bud
burst and subsequent rapid shoot extension. The high values of
R20 late in the year, around Day 300, followed the first nighttime frosts, and probably resulted from increased demands for
repair and biosynthesis. The seasonal change in the response
of respiration to temperature contrasts with the assumption
made by Ryan et al. (1997) that the sensitivity of black spruce
respiration to temperature is constant over the year for trees at
this site.
Table 3. Mean values (± 95% confidence intervals) of the estimated
parameters in an Arrhenius “activation energy” model of the response
of shoot respiration to temperature. The values were estimated from
gas exchange measurements made on 11 shoots at the BOREAS SSA
OBS site in July and October 1996.
Period
Shoot position (n) R20 (µmol m –2 s –1) E 0 (J mol –1 K –1)
July
Upper (1)
Mid (3)
Lower (1)
0.08 ± 0.10
0.24 ± 0.30
0.15 ± 0.05
68842 ± 23676
48847 ± 24147
47515 ± 6155
October
Mid (6)
0.11 ± 0.03
57568 ± 5186
0.92
1.32
1.01
1.03
42.2 ± 2.9
44.7 ± 2.9
48.6 ± 4.1
0.72
0.71
–
0.64
–
–
–
Shoot Pmax, estimated from shoot A–Q response curves
(4.7 ± 2.1 µmol m –2 s –1), was slightly higher than the values
measured by Middleton et al. (1997) for black spruce at the
same site in 1994 (3.10 ± 0.22 µmol m –2 s –1). This difference
presumably reflects differences between the bilateral illumination system used in the present study and the unilateral system used by Middleton et al. (1997). Bilateral illumination
reduces mutual shading within a shoot (Wang and Jarvis
1990). The values of Vmax and Jmax, which were derived from
shoot measurements, were broadly typical of published values
for other Picea species (Wullschleger 1993).
Needle N concentrations were low (Table 2), about half the
value typically found in plantation-grown black spruce at similar latitudes (Lamhamedi and Bernier 1994). Needle P concentrations were less than 1 mg g –1, which is considered a sign
of P deficiency (Lamhamedi and Bernier 1994) (Table 2), and
were found to correlate with differences in branch Pmax
(Rayment and Jarvis 1999a). This correlation indicates a possible P limitation to photosynthesis. Photosynthesis, however,
showed a pronounced sensitivity to ambient oxygen concentration (D. Loustau et al., unpublished observations). This suggests that, despite the low needle P concentration, photosynthesis was not limited by the triose phosphate utilization rate
and that most effects of nutrient deficiency on photosynthesis
were probably mediated through carboxylation activity and
the electron transport rate. This is consistent with studies of
the effects of N fertilization on northern latitude forests where
the application of additional N significantly increased photosynthetic capacity (Mitchell and Hinckley 1993, Teskey et al.
1994, Roberntz and Stockfors 1998).
Spatial variation
Although branches in the upper canopy received almost twice
as much light over the year as branches in the lower canopy
(estimated from incident Q multiplied by projected branch
area), total carbon uptake of branches in the upper canopy was
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
226
RAYMENT, LOUSTAU AND JARVIS
Figure 3. (a) Seasonal course of respiration rate corrected to 20 °C (R20) and
(b) activation energy (E0) based on the
Arrhenius “activation energy” model of
respiration temperature response for
shoots, branches and canopy at the
BOREAS SSA OBS site from April to
December 1996. Each value was calculated from measurements averaged
over 20-day periods. Note that shoot
and branch parameters are expressed
on a needle area basis and canopy parameters are expressed on a ground
area basis. Error bars represent 95%
confidence limits for the parameter estimates.
only 38% higher than in the lower canopy (Rayment and Jarvis
1999a). There were no significant differences in Vmax or Pmax
of shoots and branches with height. This finding is consistent
with the almost uniform vertical distribution of specific needle
area and N and P concentrations in the canopy (Table 2). However, it contrasts with the vertical stratification of photosynthetic capacity and N concentrations observed in many vegetation
canopies (Field and Mooney 1986, Pearcy and Sims 1994,
Hollinger 1996). This apparent lack of photosynthetic acclimation to Q may be the result of the aggregation of needles
into tall, narrow, dense tree crowns that do not form a closed
canopy. In the study trees, the strongest gradient of light occurs horizontally along the branches, from the needles at the
ends of the branches that are nearly always in sunlight, to those
in the interior of the crown that are always shaded. Currentyear needles growing at the ends of the branches had, on average, 13% higher N and P concentrations than older needles
(Table 2), suggesting that there is some degree of optimization
of N allocation, but in the horizontal rather than the vertical direction. The branch bag technique, because it integrates
photosynthetic rate over the whole of the branch, would tend
to obscure differences in photosynthesis resulting from N allocation patterns in the study trees.
Although separate measurements of photosynthetic parameters based on needle age were not made, it is reasonable to assume that current-year needles had higher Pmax than older
needles because a reduction in photosynthetic activity in needles older than 1 year has been observed in black spruce (Hom
Table 4. Comparison between model parameters (± 95% confidence intervals) estimated from measurements at three organizational scales at the
BOREAS SSA OBS site. Measurements were made between 15 and 20 °C in July 1996. The values of temperature sensitive parameters are given
at 20 °C. Parameters are expressed on an illuminated leaf area basis.
Model
Parameter
Photosynthesis
Vmax
18.5 ± 5.9
13.2 ± 0.7
Farquhar et al.
Jmax
Rd
α
52.6 ± 9.2
0.67 ± 0.51
0.23 ± 0.06
44.3 ± 0.8
0.61 ± 0.04
0.14 ± 0.005
R20
E0
0.16 ± 0.15
55,068 ± 17,993
Respiration
Shoot
Branch
0.54 ± 0.01
50,445 ± 2485
TREE PHYSIOLOGY VOLUME 22, 2002
Canopy
11.3 ± 1.1
41.1 ± 1.5
–
0.054 ± 0.077
2.33 ± 0.42
63,742 ± 21,412
PHYSIOLOGY AT THREE ORGANIZATIONAL SCALES
and Oechel 1983). Concomitant reductions in nutrient content
and Pmax have also been observed in other coniferous species
(e.g., Porté and Loustau 1998). Thus, the growth of new needles at the shoot tips, resulting in the formation of an outer shell
of new foliage, may be regarded as the main mechanism by
which this species allocates photosynthetic capacity to the
most illuminated part of the canopy. Nutrient reallocation
among mature needles probably plays only a minor role in acclimation.
Canopy photosynthesis
Several workers have attempted to treat whole canopies as
equivalent to a big leaf and estimate canopy parameters for a
simple light response model (Ruimy et al. 1995). When calculated on a leaf area basis, estimated canopy Pmax (3.02 ±
0.07 µmol m –2 s –1) was lower than that found for maritime
pine (Pinus pinaster (Ait.)) (16.4 µmol m –2 s –1; Y. Brunet et
al., poster presentation cited in Ruimy et al. 1995), Douglas-fir
(Pseudotsuga menziesii (Mirb.) Franco) (8.2 µmol m –2 s –1;
Price and Black 1990) and Sitka spruce (Picea sitchensis
(Bong.) Carrière) (5.5 µmol m –2 s –1; Jarvis 1994), but similar
to that found in black spruce at a more northerly latitude
(about 3.8 µmol m –2 s –1; Goulden et al. 1997). Estimated day
respiration was also lower in our study (0.18 ± 0.16 µmol m –2
s –1) than in maritime pine (0.35 µmol m –2 s –1), Douglas-fir
(0.71 µmol m –2 s –1) and Sitka spruce (1.27 µmol m –2 s –1), but
slightly higher than in the more northerly black spruce stand
(0.126 µmol m –2 s –1) (references as above). The value of α for
our stand (0.017 ± 0.014) was similar to the values of 0.018
and 0.02 found in maritime pine (Y. Brunet et al., poster presentation cited in Ruimy et al. 1995) and Douglas-fir (Price
and Black 1990), respectively, and lower than the values of
0.04 and 0.051 found in a more northerly black spruce stand
(Goulden et al. 1997) and in Sitka spruce (Jarvis 1994), respectively. Compared with other coniferous ecosystems,
therefore, this boreal ecosystem has rather low photosynthetic
activity.
Lloyd et al. (1995) estimated leaf-area-based values for
Vmax (15.5 µmol m –2 s –1), Jmax (29.5 µmol m –2 s –1) and R d
(0.16 µmol m –2 s –1) for a tropical rainforest canopy. These values are remarkably similar to the values we found for a boreal
forest canopy (Table 4). This similarity is particularly striking
in view of the theoretical difficulties in determining Vmax and
Jmax at higher organizational scales. Notably, the canopy consists of many foliage elements subject to a wide variety of environmental conditions, so that although some elements may
be operating under carboxylation limited conditions, photosynthesis in others may be limited by electron transport.
227
time respiration using this method were not possible.
In Table 4, mean model parameter values estimated for each
of the three organizational scales for the period Day 180 to
Day 200, between 15 and 20 °C, are compared. Estimated canopy parameters that were calculated on a ground area basis
have been divided by the estimated leaf area index (4.4; see
Chen et al. 1997) so that all parameters are expressed on a leaf
area basis. Although this is a crude method to scale between
leaf and canopy, because photosynthesis is a nonlinear function of absorbed radiation and absorbed radiation is a nonlinear function of leaf area, it nevertheless provides a means by
which the functional differences between organizational
scales can be compared.
Most of the estimated parameters were found to vary with
organizational scale. Estimated values of Vmax and Jmax decreased with increasing organizational scales, although the
differences were not statistically significant. Values reported
by Meir (1996) for Vmax (26–59 µmol m –2 s –1) and Jmax (40–
105 µmol m –2 s –1) measured on leaves of tropical rainforest
trees were typically three times higher than values of Vmax
(15.5 µmol m –2 s –1 expressed on leaf area basis) and Jmax
(29.5 µmol m –2 s –1 expressed on leaf area basis) for the whole
canopy at the same site (Lloyd et al. 1995). Jarvis (1994) observed an increase in Pmax with scale in a study of needle, shoot
and canopy photosynthesis in Sitka spruce, but this may have
been largely a consequence of the rates being expressed on total projected needle area, shoot silhouette area and ground area
bases, respectively. Similarly, Jarvis (1994) found that respiration increased with organizational scale from needles to shoots
to canopy. In contrast, we found that differences between estimates of R d for the different scales were not significantly different. The difficulties in estimating daytime respiration of the
canopy alone have been discussed above.
There was a significant reduction in α in branches compared
with shoots, and in the canopy compared with branches, presumably because of more mutual shading of needles in
branches than in shoots and more mutual shading in the canopy than in the branches—an effect that was not observed in
Sitka spruce (Jarvis 1994).
Nighttime respiration increased significantly (P < 0.05) between branches and shoots and between the canopy and
branches, reflecting the increased costs of supporting an increasing amount of biomass. The temperature sensitivity of
respiration was not significantly different at any scale, even
though, in the canopy, an increased proportion of autotrophic
respiration takes place in the woody stem, which is relatively
less well coupled to changes in air temperature.
Variation in parameters between organizational scales
Conclusion
Not all the physiological parameters describing the functioning of this boreal forest ecosystem could be extracted at each
organizational scale. For instance, canopy daytime respiration
rate (R d), calculated from the y-axis intercept of the Q response
curve of canopy uptake, was particularly sensitive to errors in
the corrections applied for the soil and understory CO2 exchanges, and consequently, reliable estimates of canopy day-
The order of magnitude agreement among parameter values at
the three organizational scales suggests that, at least for aerodynamically rough, largely mono-specific forest canopies,
physiological parameters may be estimated from eddy covariance flux measurements with reasonable accuracy. The
small differences between Vmax and Jmax at the different scales
also suggest that the overall spatial organization of photosyn-
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
228
RAYMENT, LOUSTAU AND JARVIS
thetic capacity is more or less optimized for carbon uptake at
each of the scales, and contrasts strongly with the threefold reduction in photosynthetic capacity found for tropical rainforests. We note that, despite the different spatial organizations of boreal and tropical forests, there is a remarkable
similarity between the estimates of Vmax and Jmax for the whole
canopy.
Acknowledgments
Thanks to Jonathon Massheder, University of Edinburgh, for correcting the eddy covariance data used in this study. Thanks also to Steve
Scott, Pete Levy, Yadvinder Malhi, Mike Perks, Ford Cropley and
John Moncrieff, University of Edinburgh, for keeping the measurement systems running during absences from the field. This work was
made possible through funding provided through the NERC TIGER
programme, and through the BOREAS project, part of the NASA
Mission to Planet Earth.
References
Chen, J.M., P.M. Rich, S.T. Gower, J.M. Norman and S. Plummer.
1997. Leaf area index of boreal forests: theory, techniques and
measurements. J. Geophys. Res. 102:29,429–29,443.
Dang, Q.-L., H.A. Margolis, M.R. Coyea, S.Y. Mikailo and G.J.
Collatz. 1997. Regulation of branch-level gas exchange of boreal
trees: roles of shoot water potential and vapor pressure difference.
Tree Physiol. 17:521–535.
Dufrêne, E., J.-Y. Pontailler and B. Saugier. 1993. A branch bag technique for simultaneous CO2 enrichment and assimilation measurements on beech (Fagus sylvatica L.). Plant Cell Environ. 16:
1131–1138.
Farquhar, G.D., S. von Caemmerer and J.A. Berry. 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90.
Farquhar, G.D. and S.C. Wong. 1984. An empirical model of stomatal
conductance. Aust. J. Plant Physiol. 11:191–210.
Field, C. and H.A. Mooney. 1986. The photosynthesis–nitrogen relationship in wild plants. In On the Economy of Plant Form and
Function. Ed. T.J. Givnish. Cambridge University Press, Cambridge, pp 25–55.
Goulden, M.L., B.C. Daube, S.M. Fan, D.J. Sutton, A. Bazzaz,
J.W. Munger and S.C. Wofsy. 1997. Physiological responses of a
black spruce forest to weather. J. Geophys. Res. 102: 28,987–
28,996.
Harley, P.C., R.B. Thomas, J.F. Reynolds and B.R. Strain. 1992.
Modelling photosynthesis of cotton grown in elevated CO2. Plant
Cell Environ. 15:217–282.
Harley, P.C., J.A. Weber and D.M. Gates. 1985. Interactive effects of
light, leaf temperature, CO2 and O2 on photosynthesis in soybean.
Planta 165:249–263.
Hollinger, D.Y. 1996. Optimality and nitrogen allocation in a tree canopy. Tree Physiol. 16:627–634.
Hom, J.L. and W.C. Oechel. 1983. The photosynthetic capacity, nutrient content and nutrient use efficiency of different needle ageclasses of black spruce Picea mariana found in interior Alaska.
Can. J. For. Res. 13:834–839.
Jarvis, P.G. 1994. Capture of carbon dioxide by a coniferous forest. In
Resource Capture by Forest Crops. Eds. J.L. Monteith, R.K. Scott
and M.H. Unsworth. Nottingham University Press, Nottingham, pp
351–374.
Jarvis, P.G., J.M. Massheder, S.E. Hale, J.B. Moncrieff, M. Rayment
and S.L. Scott. 1997. Seasonal variation of carbon dioxide, water
vapor and energy exchanges of a boreal black spruce forest. J.
Geophys. Res. 102:28,953–28,966.
Lamhamedi, M.S. and P.Y. Bernier. 1994. Ecophysiology and field
performance of black spruce Picea mariana: a review. Ann. Sci.
For. 51:529–551.
Leuning, R. 1995. A critical appraisal of a combined stomatal–photosynthesis model for C3 plants. Plant Cell Environ. 18:339–355.
Lewis, J.D., K.L. Griffin, R.B. Thomas and B.R. Strain. 1994. Phosphorus supply affects the photosynthetic capacity of loblolly pine
grown in elevated carbon dioxide. Tree Physiol. 14:1229–1244.
Lloyd, J. and J.A. Taylor. 1994. On the temperature dependence of
soil respiration. Funct. Ecol. 8:315–323.
Lloyd, J., J. Grace, A.C. Miranda, P.W. Meir, S.C. Wong, B.S.
Miranda, I.R. Wright, J.H.C. Gash and J. McIntyre. 1995. A simple
calibrated model of amazon rain-forest productivity based on leaf
biochemical-properties. Plant Cell Environ. 18:1129–1145.
Meir, P.W. 1996. The exchange of carbon dioxide in tropical forest.
Ph.D. Thesis, Univ. Edinburgh, 208 p.
Middleton, E.M., J.H. Sullivan, B.D. Bovard, A.J. Deluca, S.S. Chan
and T.A. Cannon. 1997. Seasonal variability in foliar characteristics and physiology for boreal forest species at the five Saskatchewan tower sites during the 1994 boreal ecosystem–atmosphere
study. J. Geophys. Res. 102:28,831–28,844.
Mitchell, A.K. and T.M. Hinckley. 1993. Effects of foliar nitrogen
concentration on photosynthesis and water use efficiency in Douglas-fir. Tree Physiol. 12:403–410.
Moncrieff, J.B., J.M. Massheder, H. deBruin, et al. 1997. A system to
measure surface fluxes of momentum, sensible heat, water vapour
and carbon dioxide. J. Hydrol. 189:589–611.
Pearcy, R.W. and D.A. Sims. 1994. Photosynthetic acclimation to
changing light environments: scaling from the leaf to the whole
plant. In Exploitation of Environmental Heterogeneity by Plants.
Eds. M.M. Caldwell and R.W. Pearcy. Academic Press, San Diego,
pp 145–174.
Porté, A. and D. Loustau. 1998. Variability of the photosynthetic
characteristics of mature needles within the crown of a 25-year old
Pinus pinaster. Tree Physiol. 18:223–232.
Price, D.T. and T.A. Black. 1990. Effect of short-term variation in
weather on diurnal canopy CO2 flux and evapotranspiration of a juvenile Douglas-fir stand. Agric. For. Meteorol. 50:139–158.
Rayment, M.B. and P.G. Jarvis. 1997. An improved open chamber
system for measuring soil CO2 effluxes in the field. J. Geophys.
Res. 102:28,779–28,784.
Rayment, M.B. and P.G. Jarvis. 1999a. Long term measurement of
photosynthesis, respiration and transpiration of black spruce. Can.
J. For. Res. 29:1528–1538.
Rayment, M.B. and P.G. Jarvis. 1999b. Temporal and spatial variation of soil respiration in a Canadian boreal forest. Soil Biol.
Biochem. 32:35–45.
Rayment, M.B., D. Loustau and P.G. Jarvis. 2000. Measuring and
modeling conductances of black spruce at three organizational
scales: shoot, branch and canopy. Tree Physiol. 20:713–723.
Roberntz, P. and J. Stockfors. 1998. Effects of elevated CO2 concentration and nutrition on net photosynthesis, stomatal conductance
and needle respiration of field-grown Norway spruce trees. Tree
Physiol. 18:233–241.
Ruimy, A., P.G. Jarvis, D.D. Baldocchi and B. Saugier. 1995. CO2
fluxes over plant canopies and solar radiation: a review. Adv. Ecol.
Res. 26:1–68.
TREE PHYSIOLOGY VOLUME 22, 2002
PHYSIOLOGY AT THREE ORGANIZATIONAL SCALES
Ryan, M.G., M.B. Lavigne, S.T. Gower, L.B. Flanagan, J.R. Brooks
and J.R. Ehleringer. 1997. Annual carbon cost of autotrophic respiration in boreal forest ecosystems in relation to species and climate.
Photosynthesis and carbon isotope discrimination in boreal forest
ecosystems: a comparison of functional characteristics in plants
from three mature forest types. J. Geophys. Res. 102: 28,861–
28,869.
Saugier, B., A. Granier, J.-Y. Pontailler, E. Dufrêne and D.D. Baldocchi. 1997. Transpiration of a boreal pine forest measured by
branch bag, sap flow and micrometeorological methods. Tree
Physiol. 17:511–519.
Sellers, P.J., F.G. Hall, G. Asrar, D.E. Strebel and R.E. Murphy. 1992.
An overview of the First International Satellite Land Surface Climatology Project (ISLSCP) Field Experiment (FIFE). J. Geophys.
Res. 97:18,345–18,371.
Sellers, P.J., F.G. Hall, R.D. Kelly, et al. 1997. BOREAS in 1997: experiment overview, scientific results, and future directions. J.
Geophys. Res. 102:28,731–28,769.
229
Teskey, R.O., H.L. Gholz and W.P. Cropper, Jr. 1994. Influence of climate and fertilization on net photosynthesis of mature slash pine.
Tree Physiol. 14:1215–1227.
von Caemmerer, S. and G.D. Farquhar. 1981. Some relationships between the biochemistry of photosynthesis and the gas exchange of
leaves. Planta 153:376–387.
Wang, Y.P. and P.G. Jarvis. 1990. Influence of crown structural properties on PAR absorption, photosynthesis, and transpiration in
Sitka spruce: application of a model (MAESTRO). Tree Physiol. 7:
297–316.
Walcroft, A.S., D. Whitehead, W.B. Silvester and F.M. Kelliher. 1997.
The response of photosynthetic model parameters to temperature
and nitrogen concentration in Pinus radiata D. Don. Plant Cell Environ. 20:1338–1348.
Wullschleger, S.D. 1993. Biochemical limitations to carbon assimilation in C3 plants: a retrospective analysis of the A/Ci curves from
109 species. J. Exp. Bot. 44:907–920.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com