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

Tree Physiology 17, 637--645
© 1997 Heron Publishing----Victoria, Canada

Influence of environmental and plant factors on canopy photosynthesis
and transpiration of apple trees
RITA GIULIANI,1 F. NEROZZI,2 E. MAGNANINI1 and L. CORELLI-GRAPPADELLI1
1

Dipartimento di Colture Arboree, University of Bologna, via Filippo Re 6, 40126 Bologna, Italy

2

Istituto di Ecofisiologia delle Piante Arboree da Frutto, National Research Council, Bologna, Italy

Received July 5, 1996

Summary We estimated carbon and water flows, canopy
conductance and the assimilation/transpiration ratio of fruiting
and non-fruiting apple trees grown in the field, from daily gas
exchange measurements taken during the summer with a
whole-canopy enclosure device. The relationships between

photosynthetic and transpirational responses and environmental conditions were also investigated, as well as the role of
canopy conductance in controlling carbon dioxide and water
vapor exchange.
Light-saturated net photosynthetic rates, which were higher
for the fruiting canopy than for the non-fruiting canopy,
showed a general decrease in the afternoon, particularly for the
non-fruiting canopy, compared with rates in the morning.
When light was not limiting, the afternoon decrease in net
photosynthesis appeared to be regulated more by non-stomatal
factors than by changes in canopy conductance. Canopy conductance, which was higher for the fruiting canopy than for the
non-fruiting canopy, may actively regulate photosynthetic activity and may also be modulated by feedback control in
response to assimilation capacity. We conclude that adjustments in canopy conductance, which were partially dependent
on the vegetative--reproductive status of the tree, control the
equilibrium between photosynthesis and transpiration. We also
demonstrated that whole-canopy chambers can be used to
estimate photosynthetic and transpirational responses thereby
overcoming the difficulty of scaling these physiological responses from the leaf to the whole-canopy level.
Keywords: assimilation/transpiration ratio, canopy conductance, whole-canopy enclosure system.

Introduction

Photosynthesis is primarily driven by solar radiation, whereas
transpiration also depends on the temperature and humidity of
air. Transpiration is induced by evaporative demand resulting
from net radiation absorbed by leaves and the drying power of
the atmosphere, which in turn is related to wind speed and
relative humidity (Monteith and Unsworth 1990).
Stomata, through which CO2 and water vapor diffuse into
and out of the leaf, are involved in the regulation of both
photosynthesis and transpiration (Jarvis and Morison 1981).

The control of stomatal aperture involves state variables (e.g.,
leaf water potential and intercellular carbon dioxide concentration), interactions between processes (transpiration and photosynthetic rates), and is related to environmental conditions, in
particular to the water vapor concentration difference between
the leaf surface and the bulk air (Jones 1992).
Although the processes of photosynthesis and transpiration
have been thoroughly investigated in individual leaves, the
contributions of the environmental and physiological factors
driving and controlling gas exchange at the whole-canopy
level are not well defined. It is difficult to extrapolate the
physiological behavior of the whole canopy from single-leaf

responses, because a collection of leaves may not accurately
represent the complexity of the canopy. Moreover, the control
of single-leaf and whole-canopy responses involves several
variables and it is reasonable to assume that the same variable
has somewhat different effects at the canopy scale than at the
leaf level. Also, experimental data for whole-tree performance
are required to validate the results obtained by mechanistic
approaches (Thornley and Johnson 1990).
For woody perennials, and in particular fruit trees, enclosure
systems able to estimate gas exchange between the whole-canopy, considered as a ‘‘big leaf,’’ and the atmosphere have
recently been developed (Palmer and Rom 1986, Snelgar et al.
1988, Adaros et al. 1989, Wibbe and Lenz 1989, Garcia et al.
1990, Buwalda et al. 1992a). The simultaneous monitoring of
environmental parameters (incoming photosynthetically active radiation, CO2 concentration, air temperature and humidity) allows estimation of physiological responses (net
photosynthesis, dark respiration and transpiration) and calculation of whole-canopy conductance (Lhomme 1991, Avissar
1993, McNaughton 1994) directly from measurements performed on the entire canopy.
The present work was undertaken to investigate canopylevel relationships between diurnal trends of environmental
variables and photosynthetic and transpirational activities, and
the control exerted by plant factors on these responses. Specifically, daily observations were collected with whole-canopy
chambers on one heavily cropping and one non-fruiting tree

grown in the field. The crop load treatments were chosen to test
how source--sink relationships affect the regulation of wholecanopy gas exchange. Canopy conductance for both trees was

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GIULIANI ET AL.

calculated, and its role in controlling gas exchange between the
whole-canopy, considered as a ‘‘big leaf,’’ and the atmosphere
was evaluated.
Materials and methods
Plant material
Measurements were carried out on two five-year-old apple
trees, in an orchard located in the Po Valley (Northern Italy)
near Bologna (44°30′ N; 10°36′ E). The trees, cv. Smoothee
grafted on Pajam 2 rootstock, were trained as slender spindles
and spaced 2.5 m in rows 4 m apart. At bloom, two trees were
chosen of similar trunk diameter, branch development and
number of flower clusters. In one tree, all flower clusters were
removed by hand. Both trees received the same standard cultural (irrigation, fertilization, pest control, etc.) management

program throughout the season.
Tree leaf areas were determined after full canopy development, immediately before the gas exchange measurements.
The leaves on each tree were counted and one in 50 leaves was
collected and assigned to a spur or extension shoot leaf sample,
as reported by Palmer (1987). The area of each sampled leaf
was measured with an LI-3000 (Li-Cor, Inc., Lincoln, NE) leaf
area meter. The average spur and extension shoot leaf area thus
obtained was then multiplied by the corresponding total leaf
number. Canopy leaf areas of about 10 and 20 m2 were estimated, for the crop load tree (about 20 fruits m −2 final leaf
area) and the non-fruiting tree, respectively. Canopy volumes
were about 4.2 and 6.2 m3 for the fruiting and the non-fruiting
canopy, respectively.
Leaf dry weight per unit area was determined from a sample
of 30 bourse shoot leaves per tree, which were collected, at full
canopy development, at the end of August. Leaf area was
estimated with the Li-Cor LI-3000 leaf area meter and leaves
were then dried at 70 °C to constant weight.
Field whole-canopy system and measurements
An open system, similar to that described by Corelli-Grappadelli and Magnanini (1993), was used to measure canopy
gas exchange in the field. The system consisted of a polyethylene chamber enclosing the entire canopy, a centrifugal airfan, and a butterfly valve to control flow. Because of the rapid

and large fluctuations in ambient CO2 concentration occurring
in the orchard, a second chamber, acting as a buffer for air
mixing, was placed before the assimilation chamber to even
out the fluctuations. The various components were connected
by lengths of 100-mm diameter plastic pipe.
Air flow rate through each chamber was adjusted, based on
canopy leaf area, to obtain CO2 differentials within the linearity range of the infrared gas analyzer (IRGA) and, at the same
time, to minimize air temperature increases inside the chamber. A small thermal differential (chamber air temperatures
were 5 and 10% higher than ambient air on fruiting and
non-fruiting trees, respectively) between outlet and inlet dry
bulb temperatures was recorded. Flow rates were estimated by
measuring the time required to fill, through the outlet air
stream, a cylindrical polyethylene bag having a volume of

0.767 m3. The average flow rate for the fruiting canopy was
20 dm3 s −1, whereas that for the non-fruiting canopy was
33 dm3 s −1. The time constant of the enclosure system was
calculated as the ratio between chamber volume and air flow
rate. Because the volume was about 13.5 m3 in both cases, the
time constants were about 12 and 7 min for the fruiting and the

non-fruiting canopy, respectively.
Canopy gas exchange measurements, which were performed on one tree at a time, started in mid-August and
continued until mid-September in 1--3 day cycles of uninterrupted measurements. Incoming photosynthetically active radiation (Q) was monitored with a calibrated quantum sensor
Li-Cor LI-190SB, placed horizontally above the canopies,
outside the chamber. The Q values were corrected for light
attenuation caused by the polyethylene canopy enclosure. Although the polyethylene film (0.1 mm thick) was spectrally
neutral, it caused a 20% reduction in light intensity over the
300--900 nm range.
At the chamber’s inlet and outlet, dry and wet bulb temperatures were measured by calibrated solid state detectors, and
CO2 concentrations of the inlet and outlet air streams were
continuously monitored by a portable IRGA (ADC-LCA2,
Analytical Development Co., Hoddesdon, U.K.). All measurements were recorded and stored every 3 min by a CR10 data
logger (Campbell Scientific Ltd., Loughborough, U.K.).
Leaf gas exchange was also measured, after removal of the
enclosure chamber. Over 100 mid-bourse shoot leaves were
chosen on external spurs, and light-saturated net photosynthetic activity was determined. Data were collected in the
morning and afternoon of sunny days with the portable IRGA
equipped with a Parkinson broadleaf chamber.
Data analysis
Net photosynthetic rate (A, g CO2 m −2 s −1) and transpiration

rate (E, g H2O m −2 s −1) were estimated by the mass balance
method (see Appendix A):
φ
A = ([CO 2]in − [CO2]out (t + δt)) −
S
V
([CO2]out (t + δt) − [CO 2]out (t))
Sδt
φ
V
E = (χout(t + δt) − χin) +
(χout (t + δt) − χout (t)),
S
Sδt

where φ is air flow rate (m3 s −1), S is canopy leaf area (m2), t is
time (s), V is chamber volume (m3), χ is air absolute humidity
(g m −3), and subscripts ‘‘in’’ and ‘‘out’’ refer to inlet and outlet
chamber values, respectively. The units of A and E were converted and expressed as µmol m −2 s −1 and mmol m −2 s −1,
respectively.

Mean canopy temperature was set equal to the outlet dry
bulb temperature. Preliminary evidence showed that the difference between the mean canopy temperature of a well-irrigated
fruit tree and air temperature did not exceed 2--3 °C (Rossi
et al. 1996).

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CANOPY PHOTOSYNTHESIS AND TRANSPIRATION

Canopy conductance (gc, mm s −1) was calculated as (see
Appendix B):
g c = 0.462

ET
,
D

where T is dry bulb temperature (K) and D is canopy air vapor
pressure (Pa).
On the assumption that differences in stomatal conductance

entail an energetic trade-off between the potential increments
in photosynthesis and the increased costs associated with the
corresponding increments in transpiration (Cowan 1990), an
assimilation/transpiration ratio (ATR, µg CO2/mg H2O) was
calculated for each canopy.
For each canopy, data used for the present analysis were
obtained for 3 days between day-of-the-year (DOY) 245 and
DOY 255.
Results
Daily trends for environmental parameters (Q, T, D), taken on
a day representative of the measurement period, and the concurrent physiological responses (A, E, gc) of the fruiting tree
are reported in Figure 1. Maximum Q measured outside the
canopy enclosure (about 1750 µmol m −2 s −1) was reached

Figure 1. Diurnal courses of the environmental parameters and corresponding physiological responses for the fruiting canopy during DOY
247: (a) T (dashed line) and Q (continuous line); (b) D (dashed line)
and E (continuous line); (c) gc (dashed line) and A (continuous line).

639

around noon, whereas maximum T (nearly 35 °C) was observed in the afternoon (Figure 1a). There was a diurnal trend
of decreasing ambient CO2 concentration (C a) from 350 ppm
in the morning to 325 ppm in the afternoon (data not shown).
Canopy air vapor pressure deficit and E, which were closely
correlated, exhibited maxima of about 1.25 kPa and 2.25 mmol
H2O m −2 s −1, respectively, in the afternoon (Figure 1b). Net
photosynthetic rate increased until midday and reached a
maximum value of about 9.5 µmol CO2 m −2 s −1 coincident
with the highest value of gc (nearly 5.5 mm s −1). Both A and gc
showed a decreasing trend in the afternoon which was more
marked for A (Figure 1c).
There was a nonlinear relationship between E and D for both
trees. The fruiting tree values showed a higher slope, and the
maximum E was about twice (about 2.5 mmol H2O m −2 s −1)
that of the non-fruiting tree (Figure 2).
The relationship between gc and D differed between the
fruiting and non-fruiting trees at different temperatures. For
the fruiting tree, the relationship between gc and D was negative and exponential at temperatures of 20, 25, 30 and 35 °C
(Figure 3a), whereas for the non-fruiting tree the relationship
was negative and exponential only at 35 °C, with no relationship at the lower temperatures (Figure 3b). There was a positive, linear relationship between gc and T in both canopies
(Figure 4), at vapor pressure deficits of 0.5 and 1.0 kPa.
In both canopies, there was a hyperbolic relationship between gc and Q. Stomata responded rapidly to Q values lower
than 100 µmol m −2 s −1, whereas at greater Q values, gc increased slightly. Moreover, gc of the fruiting tree was about
twice that of the non-fruiting tree (Figure 5).
Boundary line relationships (Webb 1972) between A and Q
are shown for both canopies in Figure 6. Because the source-sink relationship within the tree may affect A, morning and
afternoon data have been treated separately. Under similar
light conditions, the boundary line for the fruiting tree showed

Figure 2. Effect of D on E of the fruiting (s) and the non-fruiting (d)
canopy. The SE max was 0.16 and 0.10 for the fruiting and non-fruiting
tree, respectively. Data points are means of 10 values.

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GIULIANI ET AL.

a steeper initial slope and higher light-saturation values than
for the non-fruiting tree. Both canopies showed higher A in the
morning than in the afternoon. In the fruiting tree, A at saturating Q decreased slightly from about 9.5 µmol CO2 m −2 s −1 in
the morning to 9.0 µmol CO2 m −2 s −1 in the afternoon (Figure 6a), whereas this difference, which may reflect a real
decrease in potential A, was more pronounced in the non-fruiting tree where A was about 25% lower in the afternoon than in
the morning (8 versus 6 µmol CO2 m −2 s −1 under saturating
light conditions) (Figure 6b).
The relationship between gc and canopy A at irradiances
above 500 µmol m −2 s −1 is shown in Figure 7, and data for the
general leaf-level relationship between gs and A at irradiances
above 500 µmol m −2 s −1 are shown in Figure 8. A Q threshold
of 500 µmol m −2 s −1 was chosen on the basis of the weak
dependence of A on gc at higher light intensities (cf. Figures 5
and 6). This threshold irradiance was also supported by the
finding that, at values lower than 500 µmol m −2 s −1, there was
no correlation between A and gc (data not shown). In the
fruiting canopy, both morning and afternoon values of A

Figure 4. (a) Effect of T on gc of the fruiting canopy at D = 0.5 kPa (s)
and D = 1.0 kPa (d) (SEmax = 0.52). (b) Effect of T on gc of the
non-fruiting canopy at D = 0.5 kPa (s) and D = 1.0 kPa (d) (SEmax =
0.49). All data points are means of 10 values.

Figure 3. (a) Effect of D on gc of the fruiting canopy at different
temperatures: T = 20 °C (r), T = 25 °C (e), T = 30 °C (d) and T =
35 °C (s) (SE max = 0.64). (b) Effect of D on gc of the non-fruiting
canopy at different temperatures: T = 25 °C (e), T = 30 °C (d) and
T = 35 °C (s) (SE max = 0.50). All data points are means of 10 values.

Figure 5. Effect of Q on gc of the fruiting (s) and the non-fruiting (d)
canopy. The SEmax was 0.55 and 0.25 for the fruiting and non-fruiting
canopy, respectively. Data points are means of 10 values.

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CANOPY PHOTOSYNTHESIS AND TRANSPIRATION

641

showed an asymptotic trend with increasing gc (Figure 7a). In
contrast, in the non-fruiting canopy, only the morning values
of A showed an asymptotic pattern with increasing gc, whereas
the afternoon A values were relatively low and nearly constant
(Figure 7b). Moreover, for the non-fruiting tree, gc ranged from
2 to 4 mm s −1 in the afternoon, whereas the morning range and
the range observed for the fruiting tree during daytime was
from 2 to 6 mm s −1.
At the leaf scale, no differences between morning and afternoon values of A with respect to leaf stomatal conductance (gs)
were observed (data not shown). Pooled morning and afternoon values of A with respect to gs showed an increasing trend
and gs and A values were greater than the corresponding data
for both canopies (Figure 8).
For both canopies, ATR plotted against A differed between
the morning and afternoon (Figure 9). In the morning, a bellshaped trend was found, with higher values for the fruiting tree
than for the non-fruiting tree. Maximum ATR for both trees
occurred at A values of around 150 µg CO2 m −2 s −1 (i.e.,
3.4 µmol CO2 m −2 s −1) (Figure 9a). In the afternoon, an asymp-

Figure 7. (a) Effect of canopy conductance on A of the fruiting canopy
in the morning (d) and in the afternoon (s). The SEmax was 1.38 and
0.65 in the morning and afternoon, respectively. (b) Effect of canopy
conductance on A of the non-fruiting canopy in the morning (d) and
in the afternoon (s). The SE max was 0.91 and 0.60 in the morning and
afternoon, respectively. Data points are means of 10 values.

Figure 6. (a) Effect of Q on A of the fruiting canopy in the morning
(d) and afternoon (s). (b) Effect of Q on A of the non-fruiting canopy
in the morning (d) and afternoon (s). The continuous line is the
boundary line for morning values and the dashed line is the boundary
line for afternoon values.

Figure 8. Effect of stomatal conductance on A, estimated from leaf
data collected from both canopies in the morning and in the afternoon.
Data points are means of 10 values.

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GIULIANI ET AL.

Figure 9. (a) Assimilation/transpiration ratio (ATR) plotted against A
for the fruiting (s) and the non-fruiting (d) canopy in the morning.
The SEmax was 3.2 and 2.0 for the fruiting and non-fruiting tree,
respectively. (b) Assimilation/transpiration ratio against A for the fruiting (s) and the non-fruiting (d) canopy in the afternoon. The SEmax
was 3.8 and 1.0 for the fruiting and non-fruiting tree, respectively.

totic relationship was shown at lower ATR values, but it was
similar for both trees. Moreover, over a range of A values from
100 to 400 µg CO2 m −2 s −1 (i.e., 2.3 to 9.0 µmol CO2 m −2 s −1),
ATR remained constant, indicating a nearly linear relationship
between A and E (Figure 9b).

Discussion
The functional approach, usually applied to photosynthesis
and transpiration data estimated by leaf gas exchange measurements, was scaled to the whole canopy, considered as a ‘‘big
leaf,’’ and applied to data obtained from a whole-canopy enclosure system. We restricted our study to two trees, one fruiting
and one non-fruiting, based on the assumption that their widely
different vegetative--reproductive conditions would affect the
interaction between canopy and environment and induce different physiological equilibria.
The diurnal trends in Q, T, D, A, E and gc reported in
Figure 1 are similar to those reported by Eckstein and Robinson (1995) for banana leaves. In accordance with their analysis, increasing E in the morning was attributed to increasing D.
As stomata began to close around noon, A decreased slightly,

whereas E, driven by D, continued to increase although less
than in the morning. The decrease in E that occurred later in
the afternoon was induced by decreasing D and partial stomatal closure. Thus, stomatal feedback may be responsible for
the nonlinear trend between E and D in Figure 2. This nonlinear trend is also in agreement with the leaf data reported by
Jones (1992) who showed, over a wide range of D values, a
decrease in E beyond a D of 1 kPa. Generally, trees control
transpiration by adjustment of stomatal conductance, as shown
by the negative relationship between gc and D observed at
various air temperatures in the fruiting canopy (Figure 3a).
However, in the non-fruiting canopy, a similar negative exponential relationship was found only at 35 °C, but not at lower
temperatures (Figure 3b). A possible explanation for this lack
of correlation between gc and D at low temperatures is that
stomatal control of canopy transpiration is strong only when
the total boundary layer conductance/stomatal conductance
ratio is high (Meinzer and Grantz 1991, Monteith 1995). Despite the air flow passing through the assimilation chamber, the
denser canopy of the non-fruiting tree may have caused conditions of low boundary layer conductance and thus a greater
degree of decoupling from the environment (Jarvis and
McNaughton 1986). The different behaviors of the fruiting and
non-fruiting canopies indicate that geometric and structural
plant characteristics and source--sink relationships might be
involved in a feedback control of canopy conductance. That is,
canopy conductance was negatively related to canopy leaf area
and positively affected by the presence of crop load. The
negative relationship between canopy conductance and leaf
area supports observations by Meinzer and Grantz (1991) that,
during plant development, increasing stomatal closure with
increasing leaf area limits the increase in transpiration per
plant, and represents a homeostatic mechanism for maintaining nearly constant leaf water status over a wide range of plant
sizes and environmental conditions.
Studies of fruiting and non-fruiting peach (DeJong 1986),
plum (Gucci et al. 1991) and apple (Jones and Cumming 1984,
Lenz 1986) trees all indicate that the presence of fruits tends to
have a positive influence on stomatal conductance. Because
photosynthesis leads to removal of intercellular carbon dioxide, it has been postulated that assimilation partially controls
stomatal conductance by affecting changes in carbon dioxide
concentration, to maintain a constant value (Morison 1987).
However, the role of CO2 in stomatal movements is controversial. Consequently, it is not clear if stomatal conductance is
affected by fruiting as a result of the depletion of CO2 in the
substomatal cavity, or as a result of the generally enhanced
photosynthetic activity induced by the presence of fruits (Monselise and Lenz 1980, Fujii and Kennedy 1985), or if a hormonal mechanism is involved (Lenz 1986).
The weak dependence of gc on Q observed above 10% of full
sunlight (Figure 5), and which closely resembles the typical
single-leaf response reported in the literature (Lakso 1994),
confirms the conclusion of Knapp and Smith (1990) that stomata of apple trees do not exhibit sun-tracking behavior. Our
data support Turner’s suggestion (Turner 1991) that light func-

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CANOPY PHOTOSYNTHESIS AND TRANSPIRATION

tions as an ‘‘activating factor’’ for stomatal opening; however,
light alone is not able to modulate canopy conductance.
The asymptotic relationships between gc and A (Figure 7)
and, at the leaf scale, between gs and A (Figure 8) suggest a
threshold, when light is not a limiting factor, above which A is
controlled by non-stomatal factors. Farquhar and Sharkey
(1982) concluded that carbon assimilation rate could increase
only marginally with conductance above the values at which
regeneration of ribulose bisphosphate carboxylase-oxygenase
(RuBP) enzyme becomes limiting.
Our results indicate that non-stomatal factors account for the
afternoon decrease in A observed in the non-fruiting canopy.
The effects of T and D on canopy conductance and respiratory
activity (dark respiration and photorespiration) are of less
importance. Mesophyll limitations on carbon fixation, which
are related to nonstructural carbohydrates accumulating in
leaves (Gucci et al. 1991), limiting phloem loading (Körner
et al. 1995) and assimilate distribution (Flore and Lakso 1989),
as a result of the low vegetative-sink demand at this time of the
growing season, are considered to be responsible for the afternoon decline in A in the non-fruiting canopy. The higher leaf
mass per unit leaf area observed in the non-fruiting tree than in
the fruiting tree (13.4 versus 11.8 mg cm −2) also supports this
explanation (cf. Palmer et al. 1997). In contrast, the strong fruit
demand for assimilates in the cropping tree minimized leaf
saturating conditions, thereby preventing the afternoon depression of A in the fruiting canopy. Moreover, the lower foliage
area density, the consequent lower self-shading and the large
carbon allocation to fruits, all contributed to the higher morning A observed in the fruiting canopy than in the non-fruiting
canopy.
Because stomata track the adaptative changes in the photosynthetic apparatus, as a result of their coupling with mesophyll activity (Wong et al. 1979, Schulze and Hall 1982,
Morison 1987), the lower afternoon gc values in the non-fruiting canopy were partially a consequence of the decrease in A.
Thus, canopy conductance can also be modulated by feedback
control in response to assimilation capacity.
For both canopies, the low light compensation point observed in the afternoon could be related to the positive effect
of T on A (data not shown). Because of the thermal inertia of
air, similar Q values tended to occur at higher temperatures in
the afternoon than in the morning. Despite their differing
photosynthetic and transpiration responses, the fruiting and
non-fruiting canopies showed similar diurnal ATR patterns,
confirming the assumption that, under well-watered conditions, the vegetative--reproductive status of the tree controls the
equilibrium between the processes of photosynthesis and transpiration by adjusting canopy conductance.

Conclusions
A primary role is ascribed to canopy conductance in controlling whole-tree gas exchange. However, plant factors such as
canopy structure, canopy leaf area and foliage area density also
affect conductance, and consequently all contribute to modulating gas exchange of the whole canopy. Moreover, non-sto-

643

matal factors, which were closely related to source--sink relationships and were affected by the presence of fruits, are also
able to regulate CO2 exchange and induce adjustments in
canopy conductance.
Analysis of the data collected by the whole canopy enclosure system indicates that this method offers an opportunity to
overcome the complexity of scaling single-leaf data to the
whole-canopy level. The technique also yields measured values that can be compared with the results of theoretical scaling
from leaf to canopy.
Acknowledgments
Research supported by the National Research Council of Italy, Special
Project RAISA, Sub-project No. 2, Paper No. 2855. We thank Prof.
E. Baldini and Drs. F. Rossi and S. Poni for critical reading of the
manuscript and advice.

References
Adaros, G., H.J. Weigel and H.J. Jäger. 1989. Environment in open-top
chambers and its effects on growth and yield of plants. I. Measurement of microclimatic parameters. Gartenbauwissenschaft 54:165-171.
Avissar, R. 1993. Observation of leaf stomatal conductance at the
canopy scale: an atmospheric modeling perspective. BoundaryLayer Meteorol. 64:127--148.
Buwalda, J.G., T.G.A. Green, J.S. Meekings and D.J. Coneybear.
1992a. Measurements of canopy gas exchange of kiwifruit vines
using a suite of whole-canopy cuvettes. Environ. Exp. Bot. 32:425-438.
Corelli-Grappadelli, L. and E. Magnanini. 1993. A whole-tree system
for gas-exchange studies. Hortscience 28:41--45.
Cowan, I.R. 1990. Economics of carbon fixation in higher plant. In On
the Economy of Plant Form and Function. Ed. T.J. Givnish. Cambridge University Press, Cambridge, U.K., pp 133--170.
DeJong, T.M. 1986. Effects of reproductive and vegetative sink activity on leaf conductance and water potential in Prunus persica L.
Batsch. Sci. Hortic. 29:131--137.
Eckstein, K. and J.C. Robinson. 1995. Physiological responses of
banana (Musa AAA; Cavendish sub-group) in the tropics. II. Influence of climatic conditions on seasonal and diurnal variations in gas
exchange of banana leaves. J. Hortic. Sci. 70:157--167.
Farquhar, G.D. and T.D. Sharkey. 1982. Stomatal conductance and
photosynthesis. Annu. Rev. Plant Physiol. 33:317--345.
Flore, J.A. and A.N. Lakso. 1989. Environmental and physiological
regulation of photosynthesis in fruit crops. Hortic. Rev. 11:111-157.
Fujii, J.A. and R.A. Kennedy. 1985. Seasonal changes in the photosynthetic rate on apple trees: a comparison between fruiting and nonfruiting trees. Plant Physiol. 78:519--524.
Garcia, R.L., J.M. Normann and D.K. McDermitt. 1990. Measurements of canopy gas exchange using an open chamber system.
Remote Sens. Rev. 5:141--162.
Gucci, R., C. Xiloyannis and J.A. Flore. 1991. Gas exchange parameters, water relations and carbohydrate partitioning in leaves of
field-grown Prunus domestica following fruit removal. Physiol.
Plant. 83:497--505.
Jarvis, P.G. and K.G. McNaughton. 1986. Stomatal control of transpiration. In Advances in Ecological Research. Academic Press, New
York, pp 1--49.

TREE PHYSIOLOGY ON-LINE at http://www.heronpublishing.com

644

GIULIANI ET AL.

Jarvis, P.G. and J.I.L. Morison. 1981. The control of transpiration and
photosynthesis by the stomata. In Stomatal Physiology. Eds. P.G.
Jarvis and T.A. Mansfield. Cambridge University Press, Cambridge, U.K., pp 247--279.
Jones, H.G. 1992. Plants and microclimate, 2nd Edn. Cambridge
University Press, Cambridge, U.K., 428 p.
Jones, H.G. and I.G. Cumming. 1984. Variation of leaf conductance
and leaf water potential in apple orchards. J. Hortic. Sci. 59:329-336.
Knapp, A.K. and W.K. Smith. 1990. Stomatal and photosynthetic
responses to variable sunlight. Physiol. Plant. 78:160--165.
Körner C., S. Pelaez-Riedl and A.J.E. Van Bel. 1995. CO 2 responsiveness of plants: a possible link to phloem loading. Plant Cell Environ.
18:595--600.
Lakso, A.N. 1994. Apple. In Handbook of Environmental Physiology
of Fruit Crops. Volume I: Temperate Crops. Eds. B. Schaffer and
P.C. Andersen. CRC Press, Inc., Boca Raton, FL, pp 3--42.
Lenz, F. 1986. Fruits effects on transpiration and dry matter production
in apples. In The Regulation of Photosynthesis in Fruit Trees. Eds.
A.N. Lakso and F. Lenz. Symp. Proc. Publ. N.Y. State Agr. Exp.
Sta., Geneva, NY, pp 101--105.
Lhomme, J.-P. 1991. The concept of canopy resistance: historical
survey and comparison of different approaches. Agric. For. Meteorol. 54:227--240.
McNaughton, K.G. 1994. Effective stomatal and boundary-layer resistances of heterogeneous surfaces. Plant Cell Environ. 17:1061-1068.
Meinzer, F.C. and D.A. Grantz. 1991. Coordination of stomatal, hydraulic and canopy boundary layer properties: do stomata balance
conductances by measuring transpiration? Physiol. Plant. 83:324-329.
Monselise, S.P. and F. Lenz. 1980. Effect of fruit load on photosynthesis rates of budded apple trees. Gartenbauwissenschaft 45:220--224.
Monteith, J.L. 1995. A reinterpretation of stomatal responses to humidity: theoretical paper. Plant Cell Environ. 18:357--364.
Monteith, J.L. and M.H. Unsworth. 1990. Principles of environmental
physics, 2nd Edn. Edward Arnold, London, 291 p.
Morison, J.I.L. 1987. Intercellular CO 2 concentration and stomatal
response to CO2. In Stomatal Function. Eds. E. Zeiger, G.D. Farquhar and I.R. Cowan. Stanford University Press, Stanford, CA,
pp 229--251.
Palmer, J.W. 1987. The measurements of leaf area in apple trees.
J. Hortic. Sci. 62:5--10.
Palmer, J.W. and C.R. Rom. 1986. Preliminary results using a wholecanopy gas exchange system on field grown apple trees. In Regulation of Photosynthesis in Fruit Crops. Ed. T.M. DeJong. Symp.
Proc. Publ. U.C. Davis, Davis, CA, pp 90--91.
Palmer, J.W., R. Giuliani and H.M. Adams. 1997. The effect of crop
load on fruiting and leaf photosynthesis of Braeburn/M26 apple
trees. Tree Physiol. In press.
Rossi, F., F. Nerozzi, O. Facini and T. Georgiadis. 1996. Orchard-atmosphere physical exchanges: modelling the thermal canopy regime for the determination of sensible and latent heat fluxes. Acta
Hortic. 416:169--176.
Schulze, E.-D. and A.E. Hall. 1982. Stomatal responses, water loss
and CO2 assimilation rates of plants in constrasting environments.
In Physiological Plant Ecology II. Encyclopedia of Plant Physiology, New Series, Vol. 12B. Eds. O.L. Lange, P.S. Nobel, C.B.
Osmond and H. Ziegler. Springer-Verlag, New York, pp 181--230.
Snelgar, W.P., G.S. Bayley and P.J. Manson. 1988. Temperature studies on kiwifruit vines using relocatable greenhouses. N.Z. J. Exp.
Agric. 16:239--339.

Thornley, J.H.M. and J.R. Johnson. 1990. Plant and crop modelling. A
mathematical approach to plant and crop physiology. Oxford Science Publications, Oxford, U.K., 669 p.
Turner, N.C. 1991. Measurement and influence of environmental and
plant factors on stomatal conductance in field. Agric. For. Meteorol.
54:137--154.
Webb, R.A. 1972. Use of the boundary line in the analysis of biological data. J. Hortic. Sci. 47:309--319.
Wibbe, M. and F. Lenz. 1989. Wieviel CO2 nimmt ein Apfelbaum an
heißen Tagen im Sommer auf? Erwerbsobstbau 31:88--90.
Wong, S.C., I.R. Cowan and G.D. Farquhar. 1979. Stomatal conductance correlates with photosynthetic capacity. Nature 282:424--426.

Appendix A
Under the experimental conditions of the study, air mixing
inside the chamber allows the assumption that the CO2 concentration ([CO2]) and absolute humidity (χ) inside and coming
out of the chamber are equal. Hence, the temporal variability
of [CO2] and χ inside the chamber can be described by the
differential equations:
V

V

d[CO 2]

dt

= φ([CO 2]in − [CO 2]) − AS

dχ
= φ(χin − χ) + ES ,
dt

where V is the volume of the whole-canopy chamber, φ is the
air flow rate (m3 s −1), S is the canopy surface area, A is net
photosynthetic rate (g CO2 m −2 s −1) and E is transpiration rate
(g H2O m −2 s −1).
Because measurements are taken every three minutes and
this is a shorter period than the time constant of the system, A,
E, [CO2] and χ coming into the chamber are considered to
remain stationary in the lagtime between two measurements.
Thus, the solutions of the previous equations are:
φ
A = ([CO2]in − [CO 2](t + δt)) +
S
φ [CO2](t) − [CO2](t + δt)
S
φ
exp( δt) − 1
V
φ
φ χ(t + δt) − χ(t)
E = (χ(t + δt) − χin ) +
.
S
S
φ
exp( δt) − 1
V

Because the ratio between φ and V is small, the solutions could
be approximated to:
φ
V
([CO 2]out (t + δt)
A = ([CO2]in − [CO 2]out (t + δt) −
S
Sδt
− [CO2]out (t))

TREE PHYSIOLOGY VOLUME 17, 1997

CANOPY PHOTOSYNTHESIS AND TRANSPIRATION

φ
V
E = (χout (t + δt) − χin ) +
(χout (t + δt) − χout(t)).
S
Sδt

Carbon dioxide concentration is expressed in g per cubic meter
and is obtained by converting the direct measurements, expressed in parts per million (ppm):
[CO 2] = 10 3

MCO 2PT0
V0P0T

cpP

γ=

λ

Mw
M air

645

,

where λ is the latent heat for water evaporation, cp is the
specific heat of air and Mair is the molar mass of air.
Appendix B

xppm ,

From the energy balance equation:
where M CO 2 is the molar mass of CO2, V0 is the molar volume
at T0 and P0. The value of T0 is equal to 273 °K and P0 is equal
to 1.013×105 Pa. T is the measured dry bulb temperature and P
is the atmospheric pressure set equal to P0.
Absolute air humidity (χ) is related to partial water vapor
pressure e:
χ=

λE =

ρcp
Dgc,
γ

where ρ is dry air density, D is the canopy air vapor pressure
deficit, calculated as:
D = e s ( T) − e ,

M we
,
RT

where Mw is the molar mass of water, R the gas constant and T
the dry bulb temperature. Following a thermodynamic approach, e is calculated from dry (T) and wet bulb temperatures
(Tw) (Monteith and Unsworth 1990, Jones 1992):
e = es(T w ) − γ(T − Tw ),

where es is the saturation vapor partial pressure, calculated as:
 T(18.564 − T/254.4 ) 
es(T) = 6.13753 exp 
,
(T + 255.57 )


Tw is the wet bulb temperature and γ is the psychrometric
constant:

it is possible to compute the canopy conductance, gc. It is
important to observe that the gc is the conductance to the
diffusion of water vapor inside the chamber, that is the inverse
of the sum of stomatal, boundary layer and aerodynamic resistances of the canopy enclosed in the chamber. Hence:
 λγ  E
gc = 
D.
 ρcp 

From the perfect gas law and relations previously reported:
gc =

R ET
ET
= 0.4619
,
Mw D
D

which is the relationship used in this paper.

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