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Bowling - Et - Al-2001-Global - Change - Biology PDF
Bowling - Et - Al-2001-Global - Change - Biology PDF
Bowling - Et - Al-2001-Global - Change - Biology PDF
Abstract
Because biological and physical processes alter the stable isotopic composition of
atmospheric CO2, variations in isotopic content can be used to investigate those pro-
cesses. Isotopic ¯ux measurements of 13CO2 above terrestrial ecosystems can poten-
tially be used to separate net ecosystem CO2 exchange (NEE) into its component
¯uxes, net photosynthetic assimilation (FA) and ecosystem respiration (FR). In this
paper theory is developed to partition measured NEE into FA and FR, using measure-
ments of ¯uxes of CO2 and 13CO2, and isotopic composition of respired CO2 and forest
air. The theory is then applied to ¯uxes measured (or estimated, for 13CO2) in a tem-
perate deciduous forest in eastern Tennessee (Walker Branch Watershed). It appears
that there is indeed enough additional information in 13CO2 ¯uxes to partition NEE
into its photosynthetic and respiratory components. Diurnal patterns in FA and FR
were obtained, which are consistent in magnitude and shape with patterns obtained
from NEE measurements and an exponential regression between night-time NEE and
temperature (a standard technique which provides alternate estimates of FR and FA).
The light response curve for photosynthesis (FA vs. PAR) was weakly nonlinear,
indicating potential for saturation at high light intensities. Assimilation-weighted dis-
crimination against 13CO2 for this forest during July 1999 was 16.8±17.1½, depending
on canopy conductance. The greatest uncertainties in this approach lie in the evalua-
tion of canopy conductance and its effect on whole-canopy photosynthetic discrimin-
ation, and thus the indirect methods used to estimate isotopic ¯uxes. Direct eddy
covariance measurements of 13CO2 ¯ux are needed to assess the validity of the
assumptions used and provide defensible isotope-based estimates of the component
¯uxes of net ecosystem exchange.
Keywords: canopy conductance, carbon dioxide, eddy covariance, forest micrometeorology, net
ecosystem exchange, stable isotopes
Received 24 January 2000; revised version received 29 June and accepted 27 August 2000
Introduction
Stable isotopes of carbon dioxide contain unique inform- CO2 (Farquhar et al. 1989). There is apparently no
ation about the biological and physical processes that fractionation associated with mitochondrial respiration,
exchange CO2 between terrestrial ecosystems and the and so the isotope ratio of respired CO2 should re¯ect
atmosphere. Photosynthesis discriminates against the that of photoassimilated carbon, which is subsequently
heavier 13C isotope in CO2, preferentially ®xing 12CO2 used for respiration (Lin & Ehleringer 1997; but see
into plant biomass, with a decrease in isotope ratio of leaf Duranceau et al. 1999). There can, however, be small
tissue of C3 plants of nearly 20½ relative to atmospheric variations in the carbon isotope ratios of various
chemical components of leaves, litter and soil organic
matter (Ehleringer et al. 2000; References therein); thus,
Correspondence and present address: D. Bowling, Department
of Biology, University of Utah, 257 S 1400 E, Salt Lake City, UT the isotopic composition of respired CO2 can vary from
84112, USA, tel +1/(801) 581-8917 of®ce +1/(801) 581-4665, that expected on the basis of photosynthetic discrimin-
e-mail bowling@biology.utah.edu ation alone. Nevertheless, photosynthesis during day-
light hours leaves the air in and near terrestrial In this study, equations are developed to separate NEE
ecosystems enriched in 13CO2, and respiration tends to into its photosynthetic and respiratory components using
dilute the air of the heavy isotope. This is apparent as a estimates of the net exchange of 13CO2. Canopy-scale
pronounced diurnal cycle in d13C at the ecosystem scale ¯uxes of 13CO2 are then described in a deciduous forest
(Flanagan et al. 1996) and as a seasonal cycle at the global in eastern Tennessee, and some related assumptions
scale (Trolier et al. 1996). from an earlier study addressed. The goal was not an
In principle, these natural labels will allow us to extensive characterization of the factors in¯uencing d13C
independently estimate the ¯uxes of net photosynthesis of forest air, but rather to determine whether or not stable
(FA) and ecosystem respiration (FR). The sum of these isotopic ¯uxes of 13CO2 could be used to successfully
opposing processes, net ecosystem CO2 exchange partition NEE in a natural forest. Finally the measured
(NEE = FR + FA, where upward CO2 ¯uxes are considered isotopic ¯uxes are combined with relevant isotopic and
positive), is now routinely measured at more than a meteorological information, and NEE partitioning is
hundred sites around the world. However, a mechanistic discussed in detail.
understanding of how photosynthesis and respiration
respond to various environmental changes is dif®cult to Theory
achieve when only net ¯uxes are measured. Three
measurement-based approaches are currently used to Conservation of mass for CO2 and 13CO2 is used to
estimate FR and FA at the canopy level. These include develop equations that can be used to partition net
scaling up soil, leaf, and stem chamber measurements ecosystem exchange. This approach is identical in
(Ryan et al. 1996; Law et al. 1999), locating eddy covari- principle to, but different in ®nal formulation from,
ance instruments below the canopy to directly measure those of Yakir & Wang (1996) and Lloyd et al. (1996).
soil respiration (Baldocchi et al. 1997, 2000), and estimat- Standard de®nitions for isotopic composition (d13C),
ing total ecosystem respiration ¯ux based on regressions isotope ratio (R), and photosynthetic isotope discrimin-
of nocturnal NEE vs. temperature (Goulden et al. 1996; ation (D) from the biological (Farquhar et al. 1989) rather
many studies since). Each of these methods at present than geochemical (Ciais et al. 1995; Hoefs 1997) literature
involves considerable uncertainty, and similar results are used.
Net ecosystem exchange (NEE) is given by conserv-
from the different approaches have so far been dif®cult
ation of mass for total CO2 (Wofsy et al. 1993)
to obtain (Lavigne et al. 1997). Stable isotopes provide a
unique and independent way to examine photosynthetic dC
NEE w0 C0 FR FA
1
and respiratory ¯uxes. dt
Yakir & Wang (1996) used micrometeorological ¯ux z
m
dC d
measurements and stable isotopes to separate NEE into C
zdz
2
dt dt
photosynthetic and respiratory components in several 0
crops, with simple canopy structure and minimal where w0 C0 is total CO2 ¯ux (measured by eddy
environmental heterogeneity. The objective of the pre- covariance), the overbar denotes Reynolds averaging,
sent paper was to investigate the utility of such an the primes denote ¯uctuations from this average, FR is
approach in a complex natural system that includes the total respiratory ¯ux of CO2 (from heterotrophs,
variation in those parameters likely to in¯uence photo- roots, and stems), FA the net photosynthetic assimilation
synthetic discrimination and the isotopic nature of of CO2 (gross photosynthetic uptake ± leaf respiration),
respired CO2. For example, variation between species, and rdC/dt the time rate of change of CO2 mole fraction
between age classes, and with height in a canopy is now (C) between ground level (0) and the measurement
well-established in light, photosynthetic rate, stomatal height (zm). (A list of symbols used is provided in
and hydraulic conductance, leaf nitrogen, and foliar Table 1.) The convention that upward scalar ¯uxes are
respiration (e.g. Brooks et al. 1991; Ellsworth & Reich positive is followed; hence, FA is a negative number
1993; Baldocchi & Collineau 1994; Yoder et al. 1994; during the day. rdC/dt is referred to as the storage ¯ux
Hubbard et al. 1999). Soil moisture varies spatially and of CO2 and is important when atmospheric stability
can in¯uence soil respiration rates signi®cantly alters vertical mixing and allows the mean C in the
(Davidson et al. 1998), either directly or through differ- canopy space to change. This term is obtained by
ences in nutrient availability and microbial community measuring C at various heights in and above the canopy
structure. These factors are likely to in¯uence photo- and using (2). Following Ruimy et al. (1995) and Lloyd
synthetic and respiratory isotope effects within a forest et al. (1996), nocturnal foliar respiration is included in FR,
and may substantially complicate isotope partitioning in but daytime foliar respiration is included in FA (net
a natural system. assimilation).
Conservation of mass for 13C can be applied to expand ments and standard eddy covariance (Bowling et al.
both equations. Multiplying through by isotope ratio, the 1999a). The storage iso¯ux can be obtained using ¯ask
following mass balance equations for 13CO2 are obtained measurements to characterize vertical pro®les of isotopic
composition and CO2. It is noted that Bowling et al.
d
Ra C Ra
w0
Ra C0 Rr FR FA
3 (1999a) interpreted iso¯ux (in d units) incorrectly as the
dt 1D
net ecosystem exchange of 13CO2 (which they denoted
13
z
m NEE), and similarly misinterpreted the eddy and
d
Ra C d storage iso¯ux terms. The use of R (eqns 3 and 4) instead
Ra C
zdz
4
dt dt of d notation would avoid the subtle distinction between
0
iso¯ux and net exchange of 13CO2. However, for
where 1 + D denotes the fractionation factor associated consistency with other CO2 mass balance studies we
with net photosynthesis, and Ra and Rr refer to the report 13CO2 exchange as an iso¯ux in this paper.
isotope ratios of CO2 in canopy air and respired CO2, d13CrFR (term III) represents the net ¯ux of 13CO2
respectively. In (3), the left-hand terms represent the net added to the atmosphere by the total respiration ¯ux FR
ecosystem exchange of 13CO2, which involve a net eddy having isotopic composition d13Cr. We assume that a
¯ux w0
Ra C0 and a storage ¯ux (eqn 4) of 13CO2. The single isotopic composition can be found that is
use of absolute isotope ratio (R = 13C/12C) introduces the representative of all components of ecosystem respir-
approximation [13CO2] » (13C/12C)*[total CO2] (where [] ation (Keeling 1958). The term (d13Ca± D)FA represents
denotes mole fraction), which involves an error of about the 13CO2 removed by photosynthesis, which is the total
1.11% for [13CO2] and is roughly constant with observed photosynthetic uptake FA times the isotope ratio of that
atmospheric variation in d13C and [CO2]. Alternatively, assimilated carbon. The isotope ratio of photosynthetic-
the isotope ratio (and PDB standard) can be rede®ned ally produced carbon is given by the source air (d13Ca)
relative to total carbon as R = 13C/(12C + 13C), in which modi®ed by the discrimination (D) associated with
case the above relationships are exact (neglecting 14C, photosynthesis. Discrimination is de®ned here as a
Tans et al. 1993). It is assumed herein that canopy air positive number, e.g. for an atmosphere with composi-
forms the CO2 substrate for photosynthesis, ignoring leaf tion ± 8½ and a photosynthetic discrimination of + 18½,
boundary layer conductance. The assumption is also FA(d13Ca ± D) = FA(± 8½ ± 18½).
made that there is no fractionation associated with Lloyd et al. (1996) used a mass balance approach to
develop similar equations. Their eqn 10 has been
autotrophic or heterotrophic respiration for 13CO2.
particularly helpful in determining the relative import-
Dividing by the PDB isotope ratio standard, subtract-
ance of photosynthesis, respiration, and turbulent trans-
ing (1), and converting to conventional d notation,
port of air into the canopy in controlling the isotopic
ignoring terms in D2 or smaller (Lloyd et al. 1996), the
composition of forest CO2 (Lloyd et al. 1996; Flanagan et al.
following is obtained
1997). This is a useful concept which has shown how
d
13 Ca C important both biological and physical (boundary-layer
w0
13 Ca C0 13 Cr FR FA
13 Ca ÿ D
dt depth, turbulent mixing) effects are in controlling isotopic
I II III IV (5) composition of CO2 in the surface layer. However, Lloyd's
approach requires several assumptions which are not
Although mass is still conserved by (1) and (5), when always satis®ed in a forest canopy, such as a well-mixed
using d notation terms I and II no longer equal the net canopy air space, which in a large closed canopy is usually
ecosystem exchange of 13CO2. Instead, their sum is the satis®ed only in late afternoon (e.g. Buchmann et al. 1996),
iso¯ux of 13CO2, which can be pictured as the product of and the dominance of certain one-way ¯ux terms over the
NEE (of total CO2) and the isotopic composition net eddy and storage ¯uxes. Lloyd et al. (1996) examine
(expressed in d units) of that net exchange. This quantity these assumptions in detail.
will be consistently referred to as iso¯ux, where There are also conceptual parameters in Lloyd's
iso¯ux = eddy iso¯ux (term I) + storage iso¯ux (term II). approach which are dif®cult to directly measure: Foi,
Writing this explicitly, the mean one-way ¯ux of CO2 into the canopy, which
may be complicated by coherent turbulence structure
(Raupach et al. 1996) and sampling interval consider-
iso¯ux = d13Cr (FR) + (d13Ca ± D)FA. (6)
ations (Lenschow et al. 1994), and in particular do, the
The eddy iso¯ux can be estimated using the ¯ux- mean isotopic composition of air moving into the
gradient method over appropriate sites (Yakir & Wang canopy. These parameters are included in the turbulent
1996), with hyperbolic relaxed eddy accumulation transport term in Lloyd's eqn 10, which is calculated as a
(Bowling et al. 1999b), or a combination of ¯ask measure- residual from other measured and modelled data (Lloyd
et al. 1996). Furthermore, the goal of separating of directly included in measured parameters. If the total
photosynthetic and respiratory ¯uxes cannot be achieved integrated canopy photosynthetic discrimination (D) is
using Lloyd's equation alone. known, two equations can be solved to obtain two
Equations (1) and (6) form the basis of the present unknowns, FA and FR, can be derived. Below, the
method to distill FA and FR from net ¯ux and net iso¯ux procedure for obtaining each of the terms in these
measurements. The in¯uence of turbulent transport is equations is detailed.
the presence of 17O were applied, and CO2 was separated convention used.) The four equations (1), (6), (8) and (9)
from N2O before analysis via gas chromatography. Mole contain ®ve unknowns (FA, FR, D, Ci, and gc). Provided
fraction of CO2 was determined by integrating the m/z that gc is known, these equations can be combined to
44 peak and comparing to injections from known provide a quadratic equation which provides only one
standards, with a precision of 6 5.5 mmol mol±1. This realistic solution for FA (derived in the Appendix). FR can
relatively large error for C results from variation in the then be found using (1).
300 mL injection volume of a sample into the mass gc was calculated from measured parameters by
spectrometer. Corrections were made for water vapour inverting the Penman±Monteith (PM) equation (e.g.
in the 500 ms ¯asks using 10-Hz water vapour density Grace et al. 1995)
data corrected to mean water vapour density at 36.0 m
(HMP 35D humitter, Vaisala, Woburn, MA), and 1:6 sra
Rn ÿ LE ÿ G ÿ H cp VPD
ÿ ra
10
matched exactly in time to the ¯ask sampling times. gc
LE
Differences in C between ¯asks resulting from errors in
absolute water vapour density are at least an order of where s is the slope of the saturation vapour pressure vs.
magnitude smaller than the precision of the C measure- temperature curve for water, Rn is net radiation, LE, G,
ment. and H are latent, soil, and sensible heat ¯uxes, r is air
density, cp is the speci®c heat of air, VPD is saturation
vapour pressure de®cit, g is the psychrometric constant,
Partitioning approach and the 1.6 factor arises in the conversion from
Equations (1) and (6) are used to partition NEE into its conductance of H2O to CO2. The aerodynamic resistance
components. In these equations respiration (FR) and term ra was computed as the sum of a resistance to
photosynthetic assimilation (FA) ¯uxes are assumed to be momentum (rm, which is a function of atmospheric
unknowns, and the exchange terms (NEE and iso¯ux) stability) and an extra term (rt) for turbulent transport of
are obtained as described above. d13Cr, the isotope ratio scalars using the approach of Magnani et al. (1998).
of respired CO2, was obtained using the Keeling-plot D was also estimated using a second approach. Evans
approach (d13Cr equals the intercept of a plot of d13Ca vs. et al. (1986) derived equations to calculate discrimination
the inverse of C on samples collected at night; Keeling by a leaf enclosed in a cuvette based on the mole fraction
1958). The isotope ratio of atmospheric CO2 (d13Ca) was and isotopic composition of CO2 in the inlet and outlet
either directly measured or calculated from C measured air streams. Lloyd et al. (1996) suggested that this concept
at 22.0 m and the ¯ask regression. could be extended to the `on-line' discrimination of an
D is calculated using an equation developed at the leaf entire canopy
scale (Farquhar et al. 1982)
ÿco
o ÿ i
DE
L15
Ci
co ÿ ci
D a
bR ÿ a
8
Ca
where co and ci (do and di) represent the CO2 mole
where a is the fractionation resulting from diffusion of fractions (isotope ratios) in air outside and inside the
CO2 in air (4.4½) into the leaf, bR is the net fractionation canopy air space, respectively. (Lowercase ci and co are
of the enzyme-catalysed ®xation (roughly 27.5½) of CO2, used here to distinguish from Ci developed earlier.)
and Ci and Ca are the CO2 mole fractions in the Combining Lloyd's equation with the Evans approach to
intercellular air space and ambient air, respectively. calculate photosynthetic discrimination from DE gives
Note that in this equation Ci is integrated over the whole
canopy, and the measured C at 22.0 m (near canopy top) co
1000
i ÿ o
is used for Ca. Although Lloyd et al. (1996) provide a co ÿ ci
D
EA15
useful formulation for integrating D over many canopy co
1000 i ÿ
i ÿ o
layers to provide a ¯ux-weighted average discrimination, co ÿ ci
canopy-scale measurements in a big-leaf analogue model
are used in preference here to estimate D via Ci obtained Notation in (EA15) is consistent with Lloyd et al. (1996)
from the gas exchange relation and differs from Evans et al. (1986). Herein co and ci are
estimated by averaging the 10-Hz CO2 time series when
ÿFA gc
Ca ÿ Ci ;
9 w¢ < 0 (co) and w¢ > 0 (ci), and derive do and di from co and
ci and the ¯ask regression (Table 2), and refer to this as
where gc is the integrated canopy stomatal conductance `on-line' discrimination by analogy with leaf measure-
to CO2. (The negative sign on FA is required by the sign ments. Note that estimation of do and di depends on the
Table 2 Geometric mean regressions of d13C vs. CO2 and the linear relation holds at all time scales important to
1/CO2 for ¯ask samples collected at varying temporal scales. turbulent transport of mass (roughly 100 ms to 30 min).
Bowling et al. (1999a) used the hyperbolic relaxed eddy
Flask type m b r2 n
accumulation (HREA) technique to collect updraft and
d13C = mC + b downdraft air for isotopic analysis, and showed that
All ¯asks ± 0.033 6 0.002 2.92 6 0.80 0.956 61 while the d13C-vs.-C relation is linear for both ¯ask
Night ± 0.026 6 0.003 ± 0.32 6 1.35 0.948 15 (whole-air) and HREA (updraft or downdraft samples),
Day1 ± 0.039 6 0.005 5.23 6 1.91 0.849 46 the slopes and intercepts for each type of sample were
30 min ± 0.036 6 0.003 4.06 6 1.16 0.991 8
not the same. This raises the question of whether the
30 s ± 0.033 6 0.003 2.85 6 1.22 0.959 31
application of (7) to 10-Hz ¯ux data is appropriate.
500 ms ± 0.033 6 0.004 3.02 6 1.57 0.943 22
The relationship between carbon isotopic composition
d13C = m(1/C) + b and CO2 mole fraction at Walker Branch in July 1999 is
All ¯asks 5962 6 314 ± 25.30 6 0.79 0.962 61 shown in Fig. 1(a). Samples were collected on timescales
Night2 5756 6 953 ± 24.87 6 2.16 0.918 15 that varied by more than three orders of magnitude, and
Day 5772 6 714 ± 24.80 6 1.87 0.845 46 the relation does not show the signi®cant change in slope
30 min 5696 6 306 ± 24.68 6 0.79 0.996 8
apparent in the HREA samples of Bowling et al. (1999a).
30 s 6091 6 410 ± 25.68 6 1.02 0.970 31
500 ms 5550 6 619 ± 24.14 6 1.59 0.943 22 Regressions for these samples are shown in Table 2. This
constitutes strong evidence that the d13C-vs.-C linearity
1
This regression was used to compute 13CO2 ¯uxes (eqn 7). holds at short timescales, and thus application of (7) for
2
The intercept of this regression was used as d13Cr. 13
CO2 appears legitimate. The variation in slope between
analyses conducted by HREA vs. ¯ask sampling that was
observed in our previous study (Bowling et al. 1999a)
must be a consequence of factors other than timescale
linear relation d = mC + b, and at present do and di are
incompatibility.
impossible to measure directly.
The d13C-vs.-C regressions for the daytime and night-
All measured and derived parameters were calculated
time samples differ signi®cantly. This is important
every 30 min over a 19-day period (13 July to 31 July
because the nocturnal mixing line represents the in¯u-
1999). There can be signi®cant run-to-run variability in
ence of respiration alone, while the daytime relation
measured ¯uxes associated with footprint changes,
shows the combined effects of photosynthetic discrimin-
nonstationarity of atmospheric turbulence, complex
ation and respiration. This was noted by Bowling et al.
topography, inadequate sampling interval, and other
(1999a) and is apparent in ®gs 7 and 8 of Flanagan et al.
factors (Moncrieff et al. 1996; Blanken et al. 1998).
(1996), which included only nocturnal data. However,
Application of this partitioning approach to individual
because the isotope ratio of forest CO2 is strongly
half-hour periods proved problematic and sometimes
resulted in unrealistic magnitudes for FR and FA, and in¯uenced by atmospheric stability, the daytime
errors in eddy covariance measurements are dif®cult to (nightime) in¯uence may persist into the early evening
assess for individual sampling intervals anyway. Results (morning). Flanagan's plots do include measured C in
are presented as ensemble-averages of each half-hour the range of 360±390 mmol mol±1, which likely include the
period over the 19-day time period, but note that the photosynthetic in¯uence.
partitioning approach was always applied to the half- d13C is plotted vs. 1/C in Fig. 1(b), and separated into
hour data. day and night periods, based on an arbitrary day/night
division of ±11½ (see also Fig. 3c). The intercept of a
regression of the nocturnal data is commonly interpreted
Results and discussion as the isotope ratio of respired CO2, integrated over the
whole ecosystem (Keeling 1958). A fundamental limit-
Relationship between d13C and C ation of the Keeling-plot approach is evident in the
It is ®rmly established in the literature that d13C and the ®gure; the intercept is extrapolated far beyond the region
inverse of C tend to be linearly related (Keeling 1958; that includes measurements, and small errors in deter-
numerous studies since). However, plots of d13C-vs.-C mination of the slope lead to ampli®ed errors in the
are also linear at the ecosystem and regional scales intercept (Buchmann et al. 1988). Dashed lines represent
(Friedli et al. 1987; Flanagan et al. 1996; Nakazawa et al. the 95% con®dence intervals on the nocturnal regression
1997a,b; Bowling et al. 1999a). Bowling et al. (1999a) slope, and lead to a range in estimated d13Cr of ±22.7 to
exploited this relationship to estimate 13CO2 ¯uxes. A ±27.0½. In the present partitioning exercise the regres-
critical and untested assumption of their approach is that sion intercept of ±24.9½ is used.
Fig. 1 (a) d13C of forest CO2 vs. CO2 mole fraction for ¯ask
samples collected at a variety of timescales. The 500-ms data Fig. 2 (a) Mean photosynthetically active radiation (b) mean air
have been corrected for the presence of water vapour in the temperature, and (c) mean vapour pressure de®cit. Data points
¯asks as described in the text; other samples were dried dur- in this ®gure (and in Figs 3±9) are means, and error bars are 1
ing collection. Samples were collected at heights of 37 m (30- SD of each quantity every half-hour during 13±31 July 1999.
min and 500-ms) and 26 m (30 s) above the ground; forest Dark panels in this and subsequent ®gures denote nocturnal
canopy height was 26±28 m (b) A Keeling plot of the same periods.
data, separated into day (open circles) and night (®lled circles)
periods. The solid line is a geometric mean regression of the
night-time data, and the dashed lines are the 95% con®dence variability in the ¯uxes, but consistent diurnal patterns
intervals on the slope. Equations for the regressions are shown
were observed. Similar variability has been observed in
in Table 2.
most eddy covariance studies (e.g. Moncrieff et al. 1996;
Yang et al. 1999) but error bars are often reported as
Environmental parameters, NEE, and d13Ca standard error rather than standard deviation. NEE
peaked on average at about ±23 mmol m±2 s±1, typical for
Nineteen-day ensemble averages of environmental para- this forest when water is not limiting (Baldocchi 1997).
meters are shown in Fig. 2. PAR peaked on average The release of stored respiratory CO2 in the morning
about 1150 mmol m±2 s±1, and mean air temperature hours was apparent as strong negative storage ¯ux
during the study ranged from 22 to 30 °C. High (Fig. 3a). Patterns for iso¯ux are similar (Fig. 3b), with a
evaporative demand was apparent most afternoons as mid-day peak of 620 mmol m±2 s±1½. The iso¯ux is not
mean VPD approached 1.5 kPa. Averages of NEE, simply a linear function of NEE as might be expected
iso¯ux, and d13Ca are shown in Fig. 3. These are the from (7) (discussed below). The strong opposing in¯u-
relevant measured parameters in the partitioning equa- ences of respiration and photosynthesis on forest air are
tions (1) and (6). There was signi®cant day-to-day apparent (Fig. 3c). CO2 was consistently depleted in the
b
Fig. 5 (a) Mean aerodynamic resistance to momentum (rm,
circles) and scalar (rt, triangles) transport, (b) mean friction
velocity (u*), (c) mean Obukhov length (L), and (d) mean ratio
of latent heat ¯ux to vapour pressure de®cit (LE/VPD).
estimate is based on changes in C (and d13C) rather than respiration ¯uxes are erroneously negative at midmorn-
changes in water vapour ¯ux. The difference in the PM ing. As discussed, the dip in gc during this period (10.30±
and on-line gc may indicate temporal changes in water use 12.00 hours) likely does not re¯ect actual physiological
ef®ciency (FA/LE) at the canopy scale. Alternatively, the changes in conductance of the forest. Photosynthesis is
difference may indicate that water vapour concentrations underestimated during this period and hence respiration
and ¯uxes are more affected by mixing of air from above becomes negative to compensate (eqn 1). When the
the forming boundary layer than are CO2 concentrations scatter in canopy conductance is removed by smoothing,
and isotope ratios. resulting FA and FR ¯uxes appear more realistic (Fig. 7b).
Photosynthetic ¯ux peaks at solar noon as would be
expected from leaf-level light response curves (note that
Isotope partitioning
NEE in the present data does not peak at solar noon), but
The partitioning results are summarized in Fig. 7. the respiration ¯ux remains negative during the morning
Measured NEE is shown in each panel for comparison. transition.
Regressions of nocturnal NEE vs. soil or air temperature As mentioned, the formulation of aerodynamic resist-
(derived during windy periods) are often used in eddy ance strongly controls the dynamics of the rise in gc
covariance studies to estimate total ecosystem respiration (Fig. 4). If the present estimates for ra were smaller, gc
¯ux, and net assimilation is calculated as a residual would rise earlier in the day and FA would be
[FA = NEE ± FR(T), Goulden et al. 1996]. The present proportionally larger (eqn 10). Using the mid-day
isotope-derived estimates of FR and FA are compared to minimum value for ra (Fig. 4) at all times of the day
those based on the regression reported for Walker Branch indeed increases the magnitude of the ¯uxes but results
by Greco & Baldocchi (1996) as an independent estimate remain noisy (Fig. 7c). Smoothing gc results in much
of respiration ¯ux (Fig. 7). It should be stressed that the smoother FR and FA ¯uxes (Fig. 7d) as expected.
temperature-based regressions are noisy and consider- Nocturnal NEE and FR in Fig. 7(d) are very similar, and
able variation is apparent in measured NEE at night that the daytime FR is higher than would be predicted from
cannot be explained by temperature variation (Goulden regression based on temperature. Photosynthetic ¯ux
et al. 1996). Thus these temperature-based ¯uxes are not peaks prior to solar noon.
necessarily the `correct' respiration ¯uxes, but are a The `on-line' estimate of gc is based on CO2 instead of
useful measure for comparison. H2O measurements. Partitioning results using this gc are
Shown in Fig. 7(a) are the ¯uxes obtained by using the shown in Fig. 7(e). Respiration ¯uxes appear to be
PM-derived conductance in Fig. 4. Considerable scatter underestimated during most of the day, implying the
is propagated to the ¯uxes from the gc scatter, and relatively small conductance forces FA to be too small.
The dynamics of the rise in conductance are similar in the controlling leaf stomatal conductance: light availability,
`on-line' and standard PM cases (Fig. 6), and the `on-line' Ca (and d13Ca), leaf temperature, saturation de®cit, and
estimate is lower in the afternoon. photosynthetic capacity, Ci/Ca (and thus D) of individual
The actual canopy conductance is likely to be inter- leaves (Garten & Taylor 1992; Ellsworth & Reich 1993;
mediate between the standard PM case and the case Roden & Pearcy 1993; Brooks et al. 1997; see also
involving minimum aerodynamic resistance, and hence References in Jarvis & McNaughton 1986). The degree
the correct assimilation and respiration ¯uxes are likely to which these variations in physiology integrate to the
intermediate between Fig. 7(b),(d). canopy level is not well understood. Further, use of the
By treating the canopy as a single layer to determine PM equation to determine a bulk canopy conductance to
canopy conductance and D, well-established complexity CO2 and its isotopes is complicated by the different roles
in vegetation canopies is explicitly ignored. Many studies of the soil in evaporative and CO2 ¯uxes (Raupach &
have shown that vertical gradients exist in those factors Finnigan 1988). Soil evaporation at Walker Branch in the
Fig. 7 Photosynthesis (FA, circles) and respiration (FR, squares) ¯uxes calculated from measured NEE (solid lines), iso¯ux, d13Cr, and
d13Ca, using (1) and (6). Each panel is associated with a canopy conductance in Figs 4 or 6, and a relevant discrimination (D) in
Fig. 9, through (8) and (9). Dotted lines represent respiration ¯ux estimated from an exponential relationship between nocturnal NEE
and air temperature (Greco & Baldocchi 1996), and the dashed-dotted lines are the derived photosynthetic ¯uxes calculated as
FA = NEE ± FR(T). Solar noon during this period was approximately 14.10 hours.
Weighted by
ratios of air and of leaf biomass (Farquhar et al. 1989). anyway). In the partitioning used herein night-time
However, instantaneous discrimination values can differ discrimination values are included to avoid arti®cially
substantially from the integrated estimate (Brooks et al. equating NEE and FR, and the solutions of (1), (6), (8) and
1997), and there is considerable variation in carbon (9) generally force FA to zero at night (Fig. 7).
isotope ratio of leaf biomass in this deciduous forest These discrimination estimates are lower than expec-
(Garten & Taylor 1992). ted. C3 plants generally have Ci/Ca near 0.6±0.9,
D in (6) represents the canopy-integrated photosyn- corresponding to a photosynthetic discrimination of 18±
thetic discrimination against 13CO2, and is analogous to 24½ (Farquhar et al. 1989). At present there are few
discrimination by a leaf. This is the same discrimination experimental data with which to compare these results.
described by Lloyd & Farquhar (1994) and Fung et al. The authors know of only one study in which photo-
(1997), applied in the present case on a smaller scale. D synthetic discrimination was directly measured under
has been approximated as DLF » d13Ca ± d13Cr by Lloyd & ambient conditions in the ®eld (at the leaf level,
Farquhar (1994), Flanagan et al. (1996), and Bakwin et al. Harwood et al. 1998). Their results showed a general
(1998). The mathematical difference is stressed between D trend of higher discrimination in the morning and lower
and other ecosystem discrimination values in the in the afternoon, with considerably larger overall diurnal
literature (De of Buchmann et al. (1998), which describe change (from ± 30 to ±15½ over the day). Lloyd et al.
the difference in isotopic composition of ecosystem (1996) used a model to estimate ecosystem FR, then used
respiration and the free troposphere, and DE of Lloyd an approach similar to the present one to derive D. Their
et al. (1996), which represents the combined in¯uences of results were quite similar in magnitude and diurnal
photosynthetic and (both) autotrophic and heterotrophic pattern for a tropical forest (± 20 to ±18½) but fairly noisy
respiratory ¯uxes on canopy (air). The formulations of (± 20 to ±16½) for a coniferous forest in Siberia. Trends in
large-scale inversion models (Ciais et al. 1995; Francey Ci/Ca for the present study (higher in the morning, lower
et al. 1995; Bousquet et al. 1999) use D, not De or DE. There in the afternoon) are consistent with those obtained in
are currently no direct measurements of D at the canopy leaf-level studies of mid-day stomatal closure (e.g.
scale. Tenhunen et al. 1984; KoÁppers & Schulze 1985).
Discriminations associated with each conductance are The isotope ratio of respired CO2 (d13Cr) represents a
shown in Fig. 9. Notable are the strong diurnal patterns, production-weighted average of all organic carbon being
with higher discrimination in the early morning and metabolized in the ecosystem, and the heterotrophic
lower discrimination in the afternoon. Patterns are similar component should integrate carbon ®xed over a period
for D derived from both water vapour (PM) and carbon of days to decades. The DLF de®ned by Lloyd & Farquhar
dioxide (`on-line') measurements. These diurnal changes (1994) is thus a multiyear integrator of D. However, the
in discrimination are required to produce realistic diurnal autotrophic contribution to the isotope ratio of ecosystem
patterns in FA and FR. Discrimination values at night were respiration should respond to changes in moisture
scattered and omitted from Fig. 9 (because there is no availability (as discrimination changes) and is likely to
photosynthetic ¯ux at night these values are irrelevant in¯uence DLF on a seasonal or interannual timescale. The
present estimates (Fig. 9) are based on half-hourly to the same degree that addition of one mole of
measurements, and are more indicative of short-term respiratory CO2 would decrease it. Formally, isotopic
photosynthetic activity. Isotopic in¯uences on the atmo- equilibrium can be de®ned by d13Cr = d13Ca ± D, over an
sphere are most signi®cant during periods of strong ¯ux. appropriate time interval. If this equality holds, then (6)
Thus the relevant discriminations are those when FA is is linearly dependent on (1) and iso¯ux = d13Cr (NEE).
maximal in Fig. 7 (12.00±15.00 hours). Flux-weighted Further, the ratio of the ¯uxes (iso¯ux/NEE) at equili-
average discriminations for each case are shown in brium would be simply the Keeling intercept, d13Cr. How
Table 3, and are similar for all cases, including DLF. The does this ratio compare in the present case? To answer
¯ux-weighted discriminations obtained by the present this question an expression for the ratio iso¯ux/NEE in
measurements (16.8±17.1½, or 18.1½ for the long-term terms of mean quantities needs to be derived.
value) are at the low end of the typical C3 range, Formally, the total vertical ¯ux of 13CO2 is described
corresponding to Ci/Ca near 0.54±0.59 (Table 3 and by
Fig. 9). Error bars in Table 3 result from propagating the
error of NEE, gc, FA, etc. The large variability in these 13
CO2 flux w13 CO2
11
parameters translates to large variability in ¯ux-
weighted discrimination (using standard errors instead
of standard deviations would decrease the error estim- which can be estimated (as an iso¯ux) using the standard
ates in Table 3 by a factor of roughly Ö19). isotopic approximation
Bakwin et al. (1998) used data from the NOAA global
sampling network to estimate discrimination at regional w
13 Ca C:
12
scales. After fossil fuel contributions were removed, with
d13Ca = ± 7.9½ and d13Cr = ±24.4½ (tall towers in Expanding each term using Reynolds averaging, and
Wisconsin and North Carolina with large regions of C3 using d instead of d13Ca for clarity,
deciduous forest) or ±24.7½ (their mean value at north
temperate latitudes), they obtained estimates for DLF of wC
w w0
0
C C0 :
13
16.5±16.8½, which are in direct agreement with the
present results. Because the tall tower measurements Multiplying the terms, recognizing that the mean of a
sample large regional air masses, it is likely that Bakwin's primed quantity is zero, and assuming w gives
results include some in¯uence of C4 crop photosynthesis,
which is abundant in the midwestern USA, and should
w0 C0
Cw0 0 w0 0 C0 :
14
lower the average regional discrimination relative to the
Walker Branch results presented here. The assumption is made that d = mC + b, and thus
Lloyd & Farquhar (1994) and Fung et al. (1997) mC b and 0 mC0 . Substituting these terms into
modelled global discrimination at large scales with fairly the ¯ux equation gives
different results for C3 vegetation averaged around
latitudinal bands (17.8½ and 20½, respectively). The eddy isoflux
2mC bw0 C0 mw0 C0 C0 :
15
former study explicitly included mesophyll resistance in
their model while the latter did not, and this difference Thus the eddy iso¯ux of 13CO2 is a function of the total
was thought to explain the contrast in their results (Fung eddy ¯ux of CO2, the mean CO2 mole fraction during the
et al. 1997). However, the present contribution also measurement period (C), and a triple moment term. The
ignores mesophyll resistance and the results are more ®rst term on the right-hand side of the equation is
consistent with those of Lloyd & Farquhar (1994). It typically two orders of magnitude larger than the triple
should be stressed that direct comparison between the moment term (data not shown), so the eddy iso¯ux can
present localized measurements and these studies is be well-approximated by the mean quantities
dif®cult because of the large differences in spatial scale.
eddy isoflux
2mC bw0 C0 :
16
Isotopic equilibrium and the dependence of iso¯ux on The ratio of eddy iso¯ux/total CO2 ¯ux in this case is
NEE
proportional to 2mC b. This ratio is not constant but
The simultaneous solution of (1) and (6) requires their varies over a diurnal cycle with the mean ambient CO2
independence. At isotopic equilibrium, the isotopic mole fraction C, which implies that the isotopic composi-
effects of photosynthesis and respiration in an ecosystem tion of net CO2 ¯ux is not constant over a diel period. A
would be equal and opposite. Removal of one mole of plot of iso¯ux/NEE (which adds the further complica-
CO2 by photosynthesis would enrich canopy air in 13CO2 tion of storage ¯uxes) from Fig. 3(a),(b) follows this
relationship very closely (not shown), varying about a system respiration (excluding the rhizosphere) is un-
mean near the Keeling plot intercept. likely to change signi®cantly based on short-term
Ideally, isotopic ¯uxes can be measured directly with changes in photosynthetic discrimination, because the
the eddy covariance technique, but at present this is substrate for respiration does not change.
impossible for isotopes of CO2. Thus, indirect approaches Gaudinski et al. (2000) used radiocarbon measurements
need to be used to estimate the iso¯ux (such as eqn 7). As to estimate that 59% of soil respiration at Harvard Forest
noted above, the linear relation and the use of (7) appears was derived from carbon that resided in the plant/soil
robust. However, the distinction between this relation system for less than one year, and that the average age of
and the Keeling (1958) equation carbon respired by heterotrophs was 8 years. If the
heterotrophic component stays more or less constant,
13 Ca slope=C 13 Cr
17 but the autotrophic component changes over a season or
between years, then equilibrium is unlikely. Thus, a
is subtle but potentially very important. It is unclear change in whole-canopy discrimination in response to
which equation is a better predictor of d13C based on C moisture availability will alter the isotopic equilibrium of
within the typical range of atmospheric CO2 (see an ecosystem on a timescale of weeks to months. Direct
regressions in Table 2 and Bowling et al. 1999a). measurements of 13CO2 ¯ux, rather than the indirect
Instead, in a fashion similar to (7), the Keeling equation methods of Yakir & Wang (1996), Bowling et al. (1999a),
could be used to estimate d13Ca, and then calculate 13CO2 and this study, are necessary to assess the validity of
eddy iso¯ux. Keeling's approach was intended originally
these assumptions.
to be used only at night, and assumes mixing of back-
ground CO2 at sunset with respired CO2 having a single
isotopic composition throughout the night. Using (17) to Conclusions
predict d13Ca during the daytime assumes that all isotopic
In this study relevant theory has been developed and
variation comes from a single source, and forces isotopic
applied to measurements in a temperate deciduous forest
equilibrium. In fact, substituting (17) into (14) in the
in order to assess the utility of stable isotopes in
derivation above yields the predicted eddy iso¯ux/total
ecosystem-scale studies of carbon dioxide and water
CO2 ¯ux = d13Cr. In the absence of direct measurements of
13 vapour exchange. Stable isotopes of CO2 can be used in
CO2 ¯ux, the partitioning approach outlined in this
combination with standard micrometeorological ¯ux
study is dependent on the assumptions made about the
measurements to partition net ecosystem CO2 exchange
relationship between isotopic composition and CO2 mole
into photosynthetic and respiratory ¯uxes. Despite
fraction. If, in fact, (17) is correct, then (6) is a multiple of
potential complications, the approach used was success-
(1). In this case perfect isotopic equilibrium exists, there is
ful for 13CO2 in a complex natural system. Expected
no unique information in 13C, and 13C/12C measurements
diurnal patterns and magnitudes of FA and FR were
cannot be used to partition net ecosystem exchange.
obtained which were consistent with those from other
However, most terrestrial ecosystems are unlikely to
approaches, and consistent with our understanding of
be in isotopic equilibrium with the present atmosphere.
The long-term disequilibrium between soil organic these ¯uxes at the leaf level. Whole-canopy photosyn-
matter and atmospheric CO2 is now well established thetic discrimination was lower than expected but was
(Schimel et al. 1994; Bird et al. 1996; Trumbore 2000). The consistent with other estimates in the literature. This
Keeling relationship appears strong for 13C at night, and approach is quite sensitive to assessment of canopy
it is perhaps more appropriate to use it instead of conductance through its in¯uence on D, and to assump-
d13C-vs.-C during nocturnal periods (as here) to calculate tions made about the relationship between isotopic
13
CO2 eddy iso¯ux. During the day, the isotopic effects of composition and CO2 mole fraction.
photosynthesis may be different than those of respir-
ation. Although Flanagan et al. (1996) found little vari- Acknowledgements
ation within a season in d13Cr in boreal forests, recent We thank K. Wilson and D. Baldocchi for collecting and sharing
work in coniferous forests of Oregon and Washington, their ¯ux and meteorological data, D. Schindler and B. Logan for
USA, shows large (2±6½) within-site seasonal variation hard work and much enthusiasm in the ®eld, and D. Yakir, J.
White, J. Berry, J. Lloyd, P. Blanken and L. Scott for thoughtful
in d13Cr, which correlates well with plant water status discussions. C. Cook and G. Hund provided invaluable
(Bowling, Fessenden and Ehleringer, unpubl. data). assistance with the isotopic measurements. This research was
Whole-canopy photosynthetic discrimination appears to funded equally by TECO NSF grant IBN9814507 and the
respond to moisture limitations in a manner consistent National Institute for Global Environmental Change through
with leaf level observations. It is speculated that the the U. S. Department of Energy (Cooperative Agreement DE-
FC03±90ER61010). Any opinions, ®ndings, and conclusions or
isotope ratio of the heterotrophic component of eco-
recommendations expressed in this publication are those of the Stable Isotopes, Integration of Biological, Ecological, and Geochemical
authors and do not necessarily re¯ect the views of NSF or DOE. Processes (ed. Grif®ths H), pp. 203±221. BIOS Scienti®c, Oxford.
Buchmann N, Kao W-Y, Ehleringer JR (1996) Carbon dioxide
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Appendix: solution of partitioning equations. which upon rearrangement yields the quadratic equation
The formal combination of (1), (6), (8) and (9) can yield an bR ÿ a 2
ÿ FA
13 Ca ÿ bR ÿ 13 CR FA
equation for FA. First, solving (9) for Ci/Ca, and gc Ca
substituting this into (8) yields
13 CR NEE ÿ isoflux 0:
A4
D bR
bR ÿ aFA =
gc Ca :
A1
The solution to this equation is
Next, this D is substituted into (6), and collecting like
terms ÿ
13 Ca ÿ bR ÿ 13 CR
FA
2
a ÿ bR =
gc Ca
bR ÿ a 2 q
isoflux 13 CR
FR
13 Ca ÿ bR FA ÿ FA : 2
13 Ca ÿbR ÿ13 CR ÿ4
bR ÿa
13 CR NEEÿisoflux
gc Ca g c Ca
A5
A2 2
a ÿ bR =
gc Ca
Multiplying (1) by d13CR and subtracting from (A2) gives and only one of the two roots yields a realistic value for
FA.
isoflux ÿ 13 CR NEE
13 Ca ÿ bR ÿ 13 CR FA ÿ
bR ÿ a 2
FA
A3
gc Ca