Agricultural and Forest Meteorology 116 (2003) 19–36
Photosynthesis, respiration and conservative carbon
use efficiency of four field grown crops
R. Albrizio, P. Steduto∗
CIHEAM-IAMB-Bari, via Ceglie 9, 70010 Valenzano (BA), Italy
Received 3 April 2002; received in revised form 18 November 2002; accepted 16 December 2002
Abstract
The present work aims at testing the hypothesis that carbon use efficiency (CUE) of sunflower, grain sorghum, wheat and
chickpea crops, having different photosynthetic pathways (C3 , C4 ) and yield composition (carbohydrates, proteins, lipids),
will hold constant over the natural thermal regime occurring during the entire crop cycle in the open field. All crops were
well watered. Sunflower and sorghum had two treatments of nitrogen application, while wheat had only one suitable level of
nitrogen, and chickpea had no nitrogen at all. Canopy temperature, day-time net photosynthesis (P), and night-time respiration
(R) were monitored by closed-system canopy chambers, properly automated for continuous measurements. Night-time respiration response to temperature and noon-time photosynthesis were measured at leaf scale,
as well. Results showed a strictly
linear relationship (i.e. constant CUE) between cumulative P ( P ) and cumulative R ( R) over the entire cycle of sorghum
(slope = 2.28) and wheat (3.35), and up to anthesis of sunflower (2.08) and chickpea (2.83), irrespective of the thermal
regimes evolution and nitrogen
nutritional levels. The same linearity was maintained when relationships were observed in
terms of biomass versus R. In sunflower, significant deviation from linearity is observed after anthesis, with a difference
between the two nitrogen treatments. No conclusions could be drawn for post-anthesis chickpea due to the interruption of the
experiment caused by an intense thunderstorm. Leaf-scale respiration responses to temperature were insufficient to explain
the corresponding behaviour at canopy-level.
© 2003 Elsevier Science B.V. All rights reserved.
Keywords: Canopy gas-exchange; Carbon balance; CUE; P/R ratio
1. Introduction
Knowledge of crop carbon balance, as a response
of CO2 gain (photosynthesis, P) and CO2 loss (respiration, R) to environmental conditions, is fundamental
to the understanding and quantitative assessment of
plant growth, primary productivity of ecosystems and
the impact of climate change on vegetation.
∗ Corresponding author. Tel.: +39-080-4606224;
fax: +39-080-4606206.
E-mail address: [email protected] (P. Steduto).
Crop respiration has been much less studied, as
compared to photosynthesis, for various reasons
such as methodological difficulties in measurements
(Loomis and Connor, 1992; Amthor and Baldocchi,
2001) and conceptual limitations in modelling (Ryan,
1991; Choudhury, 2001). Hence, the accuracy of predictions of the carbon balance is largely dependent
on the uncertainties associated with the estimation
of respiration (Waring et al., 1998; Högberg et al.,
2001). Most of these uncertainties, in turn, are related
to the extrapolation of inferences drawn from lower
hierarchical scale experiments (e.g. short-term and/
0168-1923/03/$ – see front matter © 2003 Elsevier Science B.V. All rights reserved.
doi:10.1016/S0168-1923(02)00252-6
20
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
or leaf/plant level) to boundary conditions of
higher hierarchical scale (e.g. long-term and/or
crop/community level).
A dominant approach to carbon balance modelling,
in fact, frames the respiratory responses within the
low-hierarchy “growth-maintenance” paradigm (e.g.
Ryan, 1991), where plant respiration is partitioned
into the functional components of construction, maintenance and ion uptake (Farrar, 1985; Lambers, 1985;
Amthor, 1986), with a resulting R response to environmental conditions considerably different from the
corresponding P response.
For instance, short-term observations generally
show that, over normal ranges of plant temperatures, respiration is highly sensitive to temperature
while photosynthesis is relatively insensitive (Amthor,
1989). This observation tacitly implies that respiration
(R) and photosynthesis (P) are somehow independent fluxes, minimising the importance of the energy
and substrates provided by P for R of the existing
plant structures (Lawlor, 1995; Dewar et al., 1999)
and, consequently, overlooking the underlying links
between R and P. Similarly, short-term studies have
demonstrated the strong correlation existing between
maintenance respiration and tissue nitrogen content
(e.g. Ryan, 1991).
In contrast, long-term whole-plant experiments have
shown a strictly bounded relationship between R and
P over a wide range of temperatures (Gifford, 1994,
1995; Tjoelker et al., 1999) and that the primary impact of nitrogen fertilisation is via leaf area growth
rather than leaf nitrogen content (e.g. Garcia et al.,
1988). This suggests that, at the community level, the
strict link between R and P would hold over a reasonable range of temperature and nitrogen availability to
the community.
A strict proportionality between R and P was
also found by Byrd et al. (1992) in both ‘C3 ’ and
‘C4 ’ species, grown under controlled environments
over a relatively long period and a wide range of
nitrogen levels, indicating that an increase in photosynthesis, induced by higher nitrogen leaf content,
causes a proportional increase in the whole-plant
respiration, irrespective of the CO2 assimilation
pathway.
Moreover, a close relationship between P and R,
often expressed in terms of ratio between net primary production (NPP) and gross primary production
(GPP), has been also reported by Waring et al. (1998)
in a forest ecosystem, and by Gifford (1995), Tjoelker
et al. (1999) and Cheng et al. (2000) under variable
CO2 concentrations during long-term whole-plant experiments.
The conservative behaviour of carbon use efficiency
(CUE), observed by Gifford (1995) induced the same
author to propose the constancy of CUE (otherwise
indicated as constant NPP/GPP ratio) as an appropriate simplification, for higher hierarchical scales, to
approach modelling of respiration (Dewar, 1996) and
productivity predictions (McCree, 1988; Cheng et al.,
2000). The advantage would be in the reduced difficulty of deriving NPP directly from GPP rather than
from carbohydrate allocation (Waring et al., 1998),
likely with much smaller errors involved (Landsberg
and Waring, 1997).
Therefore, a constant NPP/GPP ratio is viewed as a
robust approach to carbon balance modelling (Dewar
et al., 1999; Cheng et al., 2000).
The literature review highlights that there is still
plenty of room for further investigations on such a
topic, due to the following experimental constraints:
reduced number of experiments and observations focusing on CUE determination under variable environmental conditions and mostly confined to temperature
and CO2 (Gifford, 1995; Tjoelker et al., 1999; Cheng
et al., 2000); limited understanding of the mechanisms
stabilising the ratio between photosynthesis and respiration (Gifford, 1995); uncertainty on whether CUE
constancy is species-dependent and invariant under
different nutritional status (Luo et al., 1996; Cheng
et al., 2000); most of the experiments being carried out
in artificially controlled environments; the micrometeorological field experiments (e.g. Baldocchi, 1994;
Suyker and Verma, 2001; Saigusa et al., 2002) are
affected by methodological limitations (Amthor and
Baldocchi, 2001).
Furthermore, the investigation on the conservative
behaviour of CUE assumes special importance when
the carbon cost required for different biomass compositions varies largely among species. For instance,
in the studies of Cheng et al. (2000) on sunflower,
and of Gifford (1995) on wheat, the crop cycle was
investigated only up to the vegetative stage leaving
it questionable whether CUE remains constant also
after forming the reproductive organs. Indeed, the
only long-term experiment reporting R and P over
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
the whole cycle of field-grown sunflower (Whitfield
et al., 1989) showed that cumulative dark respiration
increased proportionally to net assimilation only up to
anthesis, while it increased more than proportionally
thereafter, causing a curvilinear relationship between
R and P.
An additional and important aspect is the response
of crop CUE while environmental variables such as
thermal regimes and nutrient levels, and growth expressions such as plant ontogeny and translocation of
assimilates and nitrogen, change concurrently under
natural out-door conditions. In this regard, little information exists on the whole seasonal expression of crop
respiration of different species grown in open field and
under different nutrient supplies (Biscoe et al., 1975;
Rochette et al., 1996).
The objective of this work, then, was to contribute
to the consolidation of the paradigm that assumes
constant NPP/GPP ratio by testing the hypothesis
that CUE will remain conservative over the natural
thermal regime occurring during the entire cycle of
four field crops (sunflower, grain sorghum, wheat and
chickpea) having different habitus, climatic and nutrient requirements, photosynthetic pathway (C3 and
C4 ), and yield composition (carbohydrates, proteins,
lipids). The CUE of sunflower and sorghum was also
inspected under two nitrogen-nutrient levels. Leaf
respiration response to temperature (short-term) was
also investigated to observe possible relationships
with canopy-level responses.
2. Materials and methods
All trials took place at the experimental field of
the Mediterranean Agronomic Institute (IAMB) located in Valenzano (Bari), Southern Italy (41◦ 03 N,
16◦ 52 E, 72 m a.s.l.) in two subsequent years (1998
and 1999). The soil of the experimental field, around
0.5–0.6 m deep, is a sand clay-loam and defined as
Typic Haploxeralfs Lithic Ruptic-Xerorthenic Xerochrepts according to the USDA soil taxonomy. The
climate is typically Mediterranean, characterised by
average annual rainfall of about 400–500 mm distributed mainly during autumn and winter, with average maximum temperature reaching 30–35 ◦ C during
summer time.
21
2.1. Field trials
Sunflower (Helianthus annuus L.) hybrid “Turbosol” and grain sorghum (Sorghum bicolor L. Moench.)
hybrid “Ramada” were both sown on 1 April 1998
in rows 0.60 and 0.40 m apart, respectively. The corresponding final plant density was of 5.6 plant m−2
for sunflower, and 16.7 plant m−2 for sorghum, and
complete emergence occurred 18 days (19 April) and
20 days (21 April) after planting (DAP), respectively.
Both crops were differentiated in nitrogen supply:
treatment N1 was well fertilised with urea, treatment
N0 was the unfertilised control. N1 treatment received
five nitrogen applications through the irrigation water
(fertigation), with a total amount of 110 kg ha−1 for
sunflower and 130 kg ha−1 for sorghum.
Durum wheat (Triticum durum L.) cv. “Appulo”
and chickpea (Cicer arietinum L.) cv. “Sultano” were
sown on 18 December 1998 and on 2 March 1999,
respectively, in rows 0.18 and 0.35 m apart. The corresponding final plant density was of 255 plant m−2
for wheat and 28 plant m−2 for chickpea, and complete emergence occurred on 12 January (25 DAP)
and 19 March (17 DAP), respectively. Due to the expected great difficulties in controlling nitrogen in relation to water regimes of a winter crop, wheat had
no nitrogen treatment differentiation, but only one
nitrogen-fertilisation schedule corresponding to five
urea applications, with a total amount of 110 kg ha−1 .
No nitrogen fertilisation was applied to chickpea because of its nitrogen fixation ability.
Each of the four crops was grown in a 2000 m2
plot, fertilised with phosphorus, well irrigated, and
maintained in healthy conditions.
2.2. Canopy CO2 gas-exchange measurements
Canopy CO2 gas-exchanges were measured by
canopy chambers, operating as closed-system, properly automated for day and night monitoring of CO2
flux, without any climate control.
The automated system enables the chamber to keep
the top wall closed and airtight during measurements
and to hold it open in between consecutive measurements, so that the chamber can continuously stand
over a canopy minimising the disturbance of the crop
environment. The basic chamber unit, made of polycarbonate walls, had a ground surface area of 0.84 m2
22
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
(1.4 m × 0.6 m) and a height of 0.5 m, with a total volume of 0.42 m3 . More chamber units were mounted on
top of each other to accommodate plant growth. The
top wall is zip-fastened on one side so that a simple
string can pull up the other side. The alternate motion of pulling and releasing the string (to open and
close the top wall) is run by a simple rotating engine, relay-driven by a micrologger (CR10X, Campbell Sci., Logan, UT, USA) through an intermediary
circuit.
While taking measurements, the atmosphere inside
the chamber is stirred by four high-speed brush-less
fans (Micronell, Vista California, CA, USA) mounted
at the lower side of the chamber (two for each corner of the wall fastening the top cover) and directed
diagonally upward, providing 0.65 m3 min−1 air displacement. The infrared gas analyser (IRGA) used for
the CO2 concentration measurements was the Li-6262
(Li-Cor Inc., Lincoln, NE, USA), operating in absolute
mode. Two fine-wire chromel–constantan thermocouples (0.075 mm, Type E, Campbell Sci., Logan, UT,
USA) were mounted inside the chamber for air temperature measurements (Tin ).
The chambers, one for each crop and treatment,
were operated automatically using a 12 V 60 Ah car
battery as power supply. A detailed description of the
chamber system used in this experimental work and
its performance are given in Steduto et al. (2002).
Chamber data acquisition from all sensors starts
after 5 s from closure, at 0.5 s interval, and for 15 s.
The measurement is repeated every 15 min for 2–3
days, with the chamber continuously standing at the
same location. The CO2 flux, expressed as carbon
exchange rate (CER), was calculated by deriving the
slopes relating the variation of concentrations to time
through the quadratic regression method (Wagner
et al., 1997), utilising the well-established equations
for closed-systems (e.g. Ball, 1987) and canopy
chambers (Steduto et al., 2002).
The point-in-time CER values (every 15 min) were
integrated over time to obtain daily CER averaged
over the 2–3-day period. Such a period represents a
measurement set. After each set, all plants enclosed in
the chamber were sampled for leaf area (by leaf area
meter, LI-3000, Li-Cor Inc., Lincoln, NE, USA) and
biomass (by dry weighing) determinations. The chamber was moved to a different location for subsequent
measurement sets at about 7–10-day intervals. CER,
accounting for the number of plants enclosed in the
chamber, was differentiated in terms of net photosynthesis (P) and dark respiration (R), with P flux calculated during day-time hours (from sunrise to sunset)
and R flux calculated during night-time hours (from
sunset to sunrise).
Concerning P measurements, it should be recognised that under sunny days chambers tend to increase
the amount of diffuse radiation within the canopy
(Denmead et al., 1993). On the other hand, there is a reduction of direct-radiation transmittance by the chamber walls (Steduto et al., 2002). The net result can be
an increased P during sunny days and no modification
of P during cloudy days (Denmead et al., 1993).
Since CER also includes the CO2 efflux from the
soil (CS ), always positive during day and night, the
actual fluxes of P and R should be calculated as
CER + CS and CER − CS , respectively, keeping in
mind that the presence of the chamber might alter CS
(Lund et al., 1999). From preliminary experiments,
though, it was observed that shortly after irrigation,
CS was very low, slightly increasing over the following couple of days, and generally close to the
operational resolution of the measurement method
(≈1–2 ␮mol m−2 s−1 ). This observation was also reported by Steduto (1993) for a maize-cropped field.
Since the measurement sets were taken after irrigation,
when the gas diffusivity of the soil was minimal, it
was decided to neglect the soil CO2 contribution to the
CER measurements and to accept the uncertainty possibly introduced by this variable. To derive cumulative
CO2 fluxes, for the days between measurement sets, P
was derived using a correlation with intercepted solar
radiation, and R was derived using a correlation with
biomass.
Notwithstanding some of the limitations of the
canopy chambers, diurnal measurements of CER
show to be comparable with corresponding measurements taken with micrometeorological methods (e.g.
Held et al., 1990; Dugas et al., 1991; Steduto et al.,
2002), while nocturnal measurements of CER appear
to be even more reliable than those taken by eddy
covariance method, due to stable atmosphere or intermittent eddies occurring during night-time (Amthor
and Baldocchi, 2001; Saigusa et al., 2002).
CO2 -exchange monitoring started on: 21 May (50
DAP, and plants with three pairs of leaves) for sunflower; 12 June (71 DAP, with 0.45 m high crop) for
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
grain sorghum; 29 March (101 DAP, 10 days before
the flag leaf emission) for wheat; 28 April (57 DAP,
with 20–25 cm high plants) for chickpea. They finished on: 19 August (140 DAP, at senescence phase)
for sunflower; 9 September (160 DAP, at physiological maturity) for sorghum; 31 May (164 DAP, at milk
maturity of grains) for wheat; 16 June (106 DAP, at
starting of pod setting) for chickpea. Unfortunately,
the chickpea crop cycle was interrupted by a violent
thunderstorm with hail at the pod-filling stage. Upon
completion of the experiment, 10 measurement sets
were obtained for sunflower, eight for sorghum, and
six for wheat and chickpea.
Due to the high experimental sophistication and
costs of the gas-exchange system and equipments, no
treatment replicates were included in the experimental design, and the measurements within each treatment can be considered only as “pseudo-replicates”
(Hurlbert, 1984). Since pseudo-replicates are not statistically independent, they yield an inappropriate error term to test the null hypothesis. In other terms,
observed significant differences between treatments
are not legitimate on a pure inferential-statistics basis.
Notwithstanding the reduced statistical power, an appraisal of the treatments effect is based also on the biological and mechanistic knowledge of the processes
involved in the system under investigation, and on the
very high accuracy of the CO2 exchange-rates determination, as detected through a wide set of preliminary tests carried out on the canopy chamber before
starting the experiments (Steduto et al., 2002). Moreover, the main objective of this study was to quantify
the carbon balance through CO2 exchange rates, while
comparison between treatments was only secondary.
These justifications were recognised also by Luo et al.
(2000), for gas-exchange experiments. The least significant differences between treatments and regression
slopes were evaluated by the Student’s t-test.
On the same days canopy chambers were operated, leaf photosynthetic rates (Al ) were measured by
LI-6400 (Li-Cor Inc., Lincoln, NE, USA), in order to
compare photosynthetic responses at leaf and canopy
scales.
2.3. Leaf respiration responses to temperature
Leaf respiration response (Rl ) to leaf temperature
(Tl ) was taken by using LI-6400.
23
Tl was measured by direct contact of the abaxial
surface of the leaf with the fine-wire thermocouple
mounted in the LI-6400 leaf chamber.
Rl response curves were determined during
night-time, generally from 23:00 to 1:00 h. The measurement started at actual leaf temperature value and
continued, in a step-wise fashion, with temperature
increases of 3 ◦ C up to the maximum value allowed
by the instrumentation (generally 12–14 ◦ C above
ambient). Thereafter, the measurements continued
downward with temperature decrease of 3 ◦ C until
crossing the initial temperature and down to the minimum value allowed by the instrumentation (generally
8–9 ◦ C below ambient). At each step, gas-exchange
variables were recorded after achieving steady-state
conditions (about 5 min) and about 1 h was needed
to obtain one curve. Measurements at about 10-day
intervals were taken from 29 May up to 30 July
(58–121 DAP) for sunflower, from 19 June up to 27
August (78–147 DAP) for sorghum, from 27 April up
to 31 May (130–164 DAP) for wheat, and from 25
May up to 10 June (85–100 DAP) for chickpea.
3. Results
3.1. Seasonal canopy carbon exchange rates
Daily integrals of P and R for sunflower, sorghum,
wheat and chickpea during the whole crop cycle are
shown in Fig. 1(a–d).
Whole-stand net primary production (P) initially
increased steeply for all the crops, reaching the
maximum net CO2 assimilation rate of: 79.8 and
97.0 g m−2 per day, for N0 and N1 treatments of
sunflower, respectively; 64.5 and 92.3 g m−2 per day,
for N0 and N1 treatments of sorghum, respectively;
38.5 g m−2 per day for wheat and 86.6 g m−2 per day
for chickpea. Peak values of P occurred at full anthesis for the two treatments of both sunflower (22 June,
82 DAP) and sorghum (12 July, 102 DAP), and at
the end of anthesis for wheat (7 May, 140 DAP) and
chickpea (4 June, 95 DAP). P tended progressively
to decline while the senescence progressed, reaching
the minimum values at the end of the measurement
time for all the crops. Chickpea was not monitored
until the end of its cycle, because a hail thunderstorm
completely destroyed the crop.
24
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
Fig. 1. Daily values of day-time photosynthesis (P) and night-time respiration (R) during the crop cycle of (a) sunflower, (b) sorghum, (c)
wheat and (d) chickpea. In (a) and (b), open and closed symbols represent nitrogen treatments N0 and N1 , respectively.
Daily P in N1 treatment was consistently higher than
in N0 for both sunflower and sorghum crops, although
N effect was much stronger in sorghum. In sunflower,
in fact, P of N1 was higher than P of N0 only around
anthesis (from 82 to 89 DAP), while no differences
were observed for the rest of the season. In sorghum,
instead, P of N1 was higher than P of N0 from the
beginning of fertilisation up to the end of the season.
Daily dark respiration (R) increased during the
early vegetative phases, reaching the maximum values
of: 50.0 and 54.0 g m−2 per day for N0 and N1 treatments of sunflower, respectively; 28.3 and 42.1 g m−2
per day for N0 and N1 treatments of sorghum, respectively; 12.3 g m−2 per day for wheat and 31.1 g m−2
per day for chickpea. Peak values of R occurred coincidentally with the filling stage of sunflower, wheat
and chickpea reproductive organs, and with the flowering stage of sorghum. Rates of R tended to decline
toward the end of the crop cycle for all the crops,
as a consequence of ceased growth respiration and
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
decreased maintenance respiration rate, associated
with an extensive senescence.
The effect of N fertilisation on R showed to be analogous to the effect on P. In the case of sunflower, R
of treatment N1 was higher than R of N0 only around
the seed-filling stage (from 89 to 98 DAP), while a
slightly higher R of N0 was observed for the rest of
the season. In sorghum, instead, R of N1 was higher
than R of N0 from the week after the first fertilisation
up to the end of the season.
25
respectively. The reductions of both the regressions were associated with an evident breakdown
of
stage. The increase in
linearity at the anthesis
R, as compared to
P and biomass, was relevant even if a new linearity was re-established after
anthesis.
In contrast to what observed for sunflower, N0 and
N1 treatments of sorghum fitted the same regression as
CUE (Fig. 2b) and growth efficiency (Fig. 3b) during
the whole crop cycle. This finding indicates that N
level affected carbon gain (as either P or biomass)
and carbon loss (R) in a similar way, and that the two
N treatments had similar efficiencies throughout the
whole season.
Comparing the CUE of the different crops (Table 1),
pre-anthesis sunflower had the lowest value (2.08)
followed by sorghum (2.28), chickpea (2.83) and
wheat (3.35). The same order was reflected also in
growth efficiency, except chickpea that showed lower
growth efficiency than sorghum, most likely due to
a greater allocation of biomass into
system.
its root
The tighter regressions between
P
and
R, as
compared to biomass versus
R (see r2 values),
indicate the very high accuracy of P and R determinations using the canopy chambers and IRGA
systems.
Table 2 reports the total net photosynthesis (Pt ) and
total dark respiration (Rt ) values obtained at the end
of each crop season, along with the seasonal Pt /Rt ratio. Sorghum of treatment N1 had the highest Pt value
(4.94 kgCO2 m−2 , 16% higher than N0 ), closely followed by sunflower of treatment N1 (4.24 kgCO2 m−2 ,
3.2. Cumulative carbon exchange rates,
carbon use and growth efficiencies
Except for sunflower, both cumulative P ( P )
and
biomass were linearly correlated with cumulative
R ( R) for all four crops during the entire season
(Figs. 2 and 3). Slopes and determination
coefficient
(r2 ) values of the regressions
between
P and
R
and between biomass and R, determined on ground
surface-area basis for all crops and treatments, are reported in Table 1. The slopes of such regressions are
measures of the CUE and of growth efficiency, respectively.
N0 and N1 treatments of sunflower fitted the same
regression either in terms of carbon use (Fig. 2a)
or growth efficiencies (Fig. 3a), in pre-anthesis,
while the value of the carbon use (and growth) efficiency strongly declined in post-anthesis. Between
pre- and post-anthesis, CUE decreased by 47 and
36% for N0 and N1 , respectively, while growth efficiency decreased by 82 and 90% for N0 and N1 ,
Table 1
Slopes and determination coefficient (r2 ) of the regressions between cumulative day-time photosynthesis ( P ) and night-time respiration
( R), and between biomass and
R, of the investigated crops and nitrogen treatments
Crop
Treatments
Regression
P vs.
R
Regression biomass vs.
R
Slope
r2
Slope
r2
Sunflower pre-anthesis
N0
N1
2.08
0.991
1.05
0.957
Sunflower post-anthesis
N0
N1
1.10
1.34
0.998
0.989
0.19
0.11
0.744
0.476
Sorghum
N0
N1
2.28
0.996
1.24
0.984
Wheat
Chickpea
–
–
3.35
2.83
0.987
0.991
1.78
1.14
0.984
0.988
Regressions of sunflower are distinguished between pre- and post-anthesis stages.
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R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
Fig. 2. Regressions between cumulative day-time photosynthesis ( P ) and night-time respiration ( R) over the crop cycle of (a) sunflower,
(b) sorghum, (c) wheat and (d) chickpea. In (a) and (b), open and closed symbols represent nitrogen treatments N0 and N1 , respectively.
9% higher than N0 ), chickpea1 (2.34 kgCO2 m−2 ) and
wheat (1.97 kgCO2 m−2 ). In terms of Rt , instead, sunflower of treatment N0 ranked first (2.52 kgCO2 m−2 ,
5% higher than N1 ), followed at a certain distance
by sorghum of treatment N1 (2.16 kgCO2 m−2 , 17%
higher than N0 ), chickpea1 (0.83 kgCO2 m−2 ) and
1
Chickpea season ended at the pod-filling stage.
wheat (0.59 kgCO2 m−2 ). It is interesting to observe
that while sorghum Rt of N1 was higher than N0 , the
situation was reversed, though slightly, in the case of
sunflower with Rt of N0 about 5% higher than N1 .
Most likely, this was due to increased biochemical
activity during post-anthesis of sunflower, induced by
accelerated senescence
in the
N0 treatment.
Although
P versus
R is just an alternative
way of expressing the relationship of cumulative net
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
27
Fig. 3. Regressions between biomass and cumulative night-time respiration ( R) over the crop cycle of (a) sunflower, (b) sorghum, (c)
wheat and (d) chickpea. In (a) and (b), open and closed symbols represent nitrogen treatments N0 and N1 , respectively.
primary productivity ( NPP)
against the cumulative
gross primary productivity ( GPP), with NPP = P
and GPP = P + R, we prefer to retain the plot
P versus
R because of its higher resolving
power.
Taking
sunflower
as an example, when plotting
NPP versus GPP (Fig. 4), both slope differences
between pre- and post-anthesis and between N0 and
N1 treatments, become less evident than when plot-
ting
P versus
R (Fig. 2), although r2 remain
the same (0.99). In the case of Fig. 4, the slope differences between pre- and post-anthesis are 0.16 for N0
and 0.11 for N1 , while in the case of Fig. 2 they are
0.98 and 0.74, respectively. The graphical resolution
becomes even worse when plotting NPP versus GPP
on daily basis (Fig. 5). In this case, the slope change
between pre- and post-anthesis, and the difference
28
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Table 2
Total seasonal day-time photosynthesis (Pt ), total seasonal night-time respiration (Rt ), and corresponding Pt /Rt ratio, of the investigated
crops and nitrogen treatments
Crop
Treatments
Pt (kgCO2 m−2 )
Rt (kgCO2 m−2 )
Pt /Rt ratio
Sunflower
N0
N1
3.90
4.24
2.52
2.39
1.55
1.77
Sorghum
N0
N1
4.16
4.94
1.81
2.16
2.30
2.29
Wheat
Chickpeaa
–
–
1.97
2.34
0.58
0.83
3.40
2.82
a
Chickpea season ended at the pod-filling stage.
between N treatments, completely disappear, with an
overall single slope value of 0.66 and r 2 = 0.93. This
example draws the attention on the risks in interpreting various types of graphical data processing.
3.3. R response to temperature at canopy and
leaf scales
The canopy-scale variation of
P / R ratio
with the variation of daily average air temperature
measured inside the canopy chamber (Tin ), through
the seasonal cycle of the four crops, is shown in
Fig.
6.Three different cases are evident: (i) a constant
P / R ratio (slope not significantly different from
zero) in sunflower at pre-anthesis and in both N treatments, in sorghum over the whole season and in both
N treatments,
and in chickpea over the whole season.
The
P / R ratio had an average (avg) value of
2.58 and a standard deviation (S.D.) of ±0.30, over
◦
the measured Tin range
between 16.0 and 34.2 C;
(ii) a constant P / R ratio (slope not significantly
different from zero) in sunflower
at post-anthesis and
in both N treatments. The
P / R ratio was lower
(avg = 1.77, S.D. = ±0.16) than the pre-anthesis
Fig. 4. Regressions between cumulative net primary productivity ( NPP) and cumulative gross primary productivity ( GPP) over the
crop cycle of sunflower, distinguished between pre- and post-anthesis stages. Open and closed symbols represent nitrogen treatments N0
and N1 , respectively.
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
29
Fig. 5. Regressions between daily net primary productivity (NPP) and daily gross primary productivity (GPP) over the crop cycle of
sunflower. Open and closed symbols represent nitrogen treatments N0 and N1 , respectively.
Fig. 6. Canopy-scale variation of cumulative day-time photosynthesis to cumulative night-time respiration (
of daily average air temperature inside the canopy chamber (Tin ), for all the crops and treatments.
◦
value, over themeasured
Tin range 23.6–28.9 C; (iii)
a decreasing
P / R ratio, from 4.92 to 3.41, in
wheat over the Tin range 11.0–21.0 ◦ C.
When observing the response, at leaf scale, of dark
respiration (Rl ) to increased leaf temperature (Tl ) for
P / R) ratio with variation
all crops (Fig. 7), the curves are almost exponential,
at least until the leaves remained rich in nitrogen (N
content >3%). In fact, toward the end of the growing season, when leaves were losing their N content
(N < 2%), Rl rates varied only slightly and remained
30
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
Fig. 7. Leaf respiration (Rl ) response to leaf temperature (Tl ) of (a) sunflower, (b) sorghum, (c) wheat and (d) chickpea. Responses refer
to different dates and leaf nitrogen content (N).
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
about constant. Sunflower (C3 plant) and sorghum (C4
plant) had similar Rl response over the same temperature range (25–28 ◦ C) and nitrogen content (Fig. 7a
and b). Wheat (Fig. 7c) did not show any response to
Tl ranging between 16.0 and 27.2 ◦ C, most likely due
to the low leaf N content, while over a similar range of
temperatures chickpea (Fig. 7d) doubled its respiration
flux from about 50–100 ␮g m−2 s−1 . The Rl versus Tl
responses reported in Fig. 7 are examples of many
different measurements made throughout the crop cycles, all showing similar trends to those reported here.
Unfortunately, no Rl versus Tl responses curves were
available before flowering of wheat and chickpea.
4. Discussion
The four species examined in the present work covered a relatively wide range of field-crops commonly
grown in agriculture systems, including the two major
photosynthetic pathways (C3 and C4 ), different yield
composition (carbohydrates, proteins, lipids) and variable climatic requirements in terms of radiation and
thermal regimes. The two N levels compared, although
only for two crops, further extended the investigation
giving a better understanding of the CUE behaviour.
4.1. Photosynthetic assimilation
Canopy photosynthetic assimilation is evaluated as
a result of the compounding effect of total leaf area
and photosynthetic rate per unit surface of leaf area,
representing, respectively, the “sink size” and the “sink
intensity” for CO2 . In all crops, seasonal net assimilation trends (Fig. 1) closely followed leaf area development, with peak values of leaf area index (LAI)
of 2.7 and 3.5 for N0 and N1 treatments of sunflower,
respectively; 5.5 and 7.0 for N0 and N1 treatments of
sorghum, respectively; 6.2 for chickpea and 3.0 for
wheat.
Both N treatments of sunflower had higher daily
P peak values than the corresponding N treatments
of sorghum (Fig. 1), while the situation was reversed
when the total seasonal values (Pt ), along the whole
crop cycle, were considered (Table 2). The higher Pt
of sorghum, as compared to sunflower, resulted from
greater leaf area duration of sorghum. The superiority of sunflower on sorghum, in terms of daily P peak
31
values, was also evident through photosynthetic measurements made at leaf scale. Leaf photosynthetic rate
(Al ), at the P peaks, was 39 and 30 ␮mol m−2 s−1 for
sunflower and sorghum, respectively. No significant Al
differences between the two N treatments were found
in both crops; it may be explained on the ground that
Al was measured only in the leaves of the upper canopy
layer fully exposed to sunlight.
Although there is large evidence of the greater photosynthetic capacity of C4 , as compared to C3 species
(e.g. Sage and Pearcy, 1987), it is not surprising to
find higher photosynthetic values for sunflower than
for sorghum, at both canopy and leaf scales, due to
higher activity of Rubisco enzyme, associated with its
more efficient electron transport (Ranty and Cavaliè,
1982) and higher stomatal conductance (Körner et al.,
1979), all conferring to sunflower the exceptional photosynthetic ability under optimal water status (Connor
and Sadras, 1992; Connor and Hall, 1997).
The N treatment had only a mild effect on canopy
gas-exchange of sunflower, as compared to sorghum.
Around anthesis, N0 reduced the leaf area of sunflower
in terms of both expansion (about 30%) and duration
(about 28%), while maintaining nitrogen concentration and photosynthetic activity per unit leaf area almost constant. These findings are consistent with the
widely accepted view that leaf expansion for sunflower
represents the most important adaptive mechanism to
environmental stress, including nitrogen (Hocking and
Steer, 1983; Connor and Sadras, 1992), and that the
primary impact of nitrogen fertilisation is via leaf area
growth rather than via leaf nitrogen content (Garcia
et al., 1988).
Among the four crops, chickpea ranked third in
terms of daily peak values of P (Fig. 1), immediately
following N1 treatments of sunflower and sorghum.
Because of the ability of its rooting system to fix nitrogen, chickpea can be considered as a fertilised crop. Its
good photosynthetic capacity was confirmed through
the Al value, which followed sorghum at very short
distance, reaching about 27 ␮mol m−2 s−1 around anthesis. Unfortunately, we cannot fully compare the Pt
of chickpea with the other crops because its crop cycle was not completed (Table 2). Wheat ranked at the
last position in terms of both daily peaks and Pt values, as a consequence of its relatively low LAI and
low leaf photosynthetic rate, the latter never exceeding 20 ␮mol m−2 s−1 .
32
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
It is interesting to notice that satisfactory consistency between peaks of daily P and Al was observed
for all crops, even if the N effect was not observed in
terms of Al measured at the upper canopy layer. This
seems to indicate that the sink intensity at leaf scale
is a valid indicator of the assimilation rate at canopy
scale, although observations done at lower hierarchical levels (leaf scale) do not allow to easily extrapolate
information to higher levels of organisation (canopy
scale).
4.2. Dark respiration
Total dark respiration determinations along the entire growing season have been of significant importance as little information exists in the literature on
the seasonal R pattern of crops grown in open field
(Amthor, 1989; Loomis and Connor, 1992).
Sunflower had the highest dark respiration either
in terms of daily peak (R) or total seasonal (Rt ) values, followed by sorghum, chickpea and wheat (Fig. 1,
Table 2). The effect of N fertilisation on respiration
was analogous to the effect on photosynthesis. The Rt
value of sunflower in N0 was slightly higher than in
N1 (Table 2) as a consequence of lower CUE during
post-anthesis (Fig. 2, Table 1). Even if such superiority of N0 was not statistically significant, it can be
the result of accelerated senescence due to the strong
translocation of N from the leaves to the reproductive organs. This indicates that the nitrogen effect at
canopy scale does not always follow the same pattern
expected at leaf scale, and that higher N content does
not necessarily mean higher respiration, as already reported in some studies carried out either in controlled
environments (e.g. Pavlik, 1983) or in the field (e.g.
Mitchell et al., 1991).
The amount of carbon lost through dark respiration
in comparison to that fixed through net photosynthesis, along the whole season, was about 60% for sunflower, while it was approximately 45, 35 and 30% for
sorghum, chickpea and wheat, respectively, without
showing significant differences between the N treatments (Table 2). The largest Rt value of sunflower is
consistent with the higher energy demand for producing oily seeds than chickpea in producing proteins
and sorghum and wheat in producing carbohydrates.
These findings indicate to what extent the carbon
cost for respiration is much more dependent on the
composition of biomass (Penning de Vries, 1975) than
on other factors, such as N content and photosynthetic
pathway (Byrd et al., 1992). Consequently, if chickpea had finished its growing cycle, we would have
likely found a higher post-anthesis respiratory cost for
chickpea than for sorghum.
4.3. Constancy of carbon use and
growth efficiencies
Similarly to radiation and water use efficiency
studies reported in the literature (e.g. Sinclair and
Muchow, 1999), we prefer to use the “cumulative
approach” of the variables to regress for determining both carbon use and growth efficiencies. In fact,
it has been largely shown (e.g. Monteith, 1994;
Steduto and Hsiao, 1994) that the mechanism behind the correlation between cause/effect variables,
or strongly linked processes, dominantly overwhelms
the statistical weakness of the regression operated on
cumulative values (Demetriades-Shah et al., 1992),
with the additional advantage of conferring robustness to the linearity of these relationships. Depending
on the variables and time-scales considered in the
analysis, the resolving ability of some relationships
may disappear, as shown in Figs. 4 and 5 where the
graphical interpretation of the results is substantially
different from the one corresponding to the results of
Fig. 2. For these reasons, we prefer to stay with the
“cumulative approach” in discussing our results.
A first outstanding outcome
of this
study is the linearity observed between P and
R (Fig. 2) and
between biomass and
R (Fig. 3), demonstrating
that both carbon-use and growth efficiencies were invariant throughout the whole crop cycle of sorghum
and wheat, and up to anthesis for chickpea and sunflower. These findings imply that, whatever the environmental conditions occurring during the crop cycle
(e.g. radiation and temperature regimes), the growth
processes (e.g. growth and maintenance respiration,
translocation of assimilates, ontogeny evolution and
crop ageing, etc.), and the nitrogen supply (in the case
of sorghum, and in sunflower up to anthesis), there
was a concerted action among all these occurrences, so
that the overall resulting CUE (and growth efficiency)
at canopy scale remains unaffected.
A second remarkable outcome is the rupture of the
linearity in CUE (and growth efficiency) for sunflower
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
at anthesis. This finding demonstrates that respiratory
costs due to biomass composition strongly dominate
carbon balance. In chickpea, due to the interruption
of the cycle during the early pod-filling stage, we
cannot demonstrate whether CUE would change in
post-anthesis (protein production), similarly to what
observed in sunflower (lipid production).
According to Gifford (1995), there are no obvious
reasons to predict that CUE would be invariant along
a crop cycle, and possible mechanisms responsible
for this conservative behaviour need to be further explored. Some theoretical support to explain constancy
between photosynthesis and respiration has been provided by some experiments (Farrar and Williams,
1991), modelling studies (Dewar, 1996; Dewar et al.,
1999) and some theoretical discussions (O’Neill et al.,
1986; Cheng et al., 2000). However, most of the studies do not include modifications due to internal crop
processes (biotic processes), such as the appearance
of the reproductive organs with associated different
energy demand depending on the biomass composition. This occurrence can significantly modify the
proportion between P and R in mature ecosystems.
Unfortunately, studies aimed at investigating the
constancy of CUE under different environmental conditions (Gifford, 1994; Tjoelker et al., 1999; Cheng
et al., 2000) have been conducted only during the
early stages of plant life and under controlled environmental conditions, without including the reproductive
stage. We are aware only of the research carried out
by Whitfield et al. (1989) who investigated R and P
over the entire crop cycle of field-grown sunflower.
They showed that the relationship between the cumulative dark respiration and gross assimilation was linear before anthesis, while it became curvilinear during
post-anthesis in both well-irrigated and water-stressed
treatments, as a consequence of the increased respiratory load due to heads. When considering the differences between Whitfield et al. (1989) experiment and
ours, the estimated numerical values of CUE are comparable and, of even greater significance, is the common conclusion shared, i.e. the highlighted importance
of monitoring all the phenological stages, especially
for crops having high lipids and proteins content. Our
results, though, confirm the constancy of CUE for cereals like wheat and sorghum.
Wheat and chickpea showed higher CUE values
than sorghum and sunflower. This might be explained
33
on the ground that those crops are generally well
adapted to cool seasons and maintain a relatively high
photosynthetic rate at low temperature. This higher
assimilation capacity is enhanced also by the low
and more diffused radiation regimes occurring during
winter and spring seasons. These conditions favour a
larger penetration of light inside the canopy (Denmead
et al., 1993), while photosynthesis proceeds mostly
in non-saturated light conditions, thus leading to an
overall increase in radiation use efficiency (Lawlor,
1995) and high P values of the canopy. Since during night-time, canopy, roots and the soil microbial
population, would be exposed to cool temperature,
maintaining low R values, the overall result might
well be an increase in CUE as well.
A third significant outcome is the apparent absence,
or
limited
impact, of the temperature influence on
P / R ratio
of crops
(Fig. 6).
The average
P / R ratio was constant at 2.58,
with temperature variation between 16.0 and 34.2 ◦ C,
for sorghum, sunflower (at pre-anthesis) and chickpea, independently of the N content, ageing, and plant
size. Post-anthesis
sunflower continued to hold a con stant P / R ratio, although with a lower value than
pre-anthesis as a consequence of biomass composition
rather than temperature. Only in wheat the P / R
ratio tended to decrease with temperature increase,
probably due to the low temperatures occurred during
most of its crop cycle, also associated with diffuse radiation conditions. Indeed, our temperature range was
quite lower than the one utilised in a controlled
exper
iment by Gifford (1994), where a constant P / R
ratio was found. Therefore, such an issue calls for further investigation.
In terms of absolute values, after
photo converting
synthesis from net to gross, the P / R ratio found
in our crops is comparable to that reported by Gifford
(1994, 1995) and predicted by Dewar (1996).
The behaviour of CUE to increasing temperature,
observed in this work at canopy scale for most of the
crops (Fig. 6), does not match the most common way
to conceive respiration as exponential function of temperature observable at leaf scale. The idea that plant
respiration is strictly temperature-dependent is indeed
based on short-term experiments, as largely explained
by Gifford (1994), Amthor (1989), and confirmed in
our study (Fig. 7). The contrasting results of dark respiration response to temperature at canopy and leaf
34
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
scales demonstrate the relevance of accounting for the
hierarchical scale of the ecosystem (O’Neill et al.,
1986).
5. Conclusions
A conservative long-term CUE, over a crop cycle
and under variable environmental conditions, would be
of enormous advantage in carbon balance modelling
and productivity predictions.
The four crops investigated in this work have shown
their CUE, expressed as the slope of the regression
between cumulative day-time net photosynthesis
(
P)
and cumulative night-time respiration ( P ), as follows: (i) wheat and sorghum had a constant and strictly
linear CUE (r 2 = 0.99 for both crops) over their entire cycle with values of 3.35 and 2.28, respectively.
Sorghum retained the same regression value for both
the contrasting nitrogen treatments (N0 and N1 ); (ii)
sunflower and chickpea also had a constant and strictly
linear CUE (r 2 = 0.99 for both crops), but only up
to anthesis, with values of 2.08 and 2.83, respectively,
with sunflower retaining the same regression value
for both its two nitrogen treatments (N0 and N1 ). After anthesis, sunflower CUE decreased significantly
from the pre-anthesis value and for both nitrogen treatments (1.10 for N0 and 1.34 for N1 ), which is quite
indicative of a strong dominance of the respiratory
costs due to the lipids composition of the reproductive
biomass. Equivalent investigation after anthesis could
not be conducted in chickpea due to the interruption of
the experiment caused by a heavy thunderstorm; (iii)
when the above relationships are examined in terms
of growth efficiency, expressed as the slope of the regression
between cumulated biomass and corresponding R, the type of response is strictly analogous to
the one of CUE.
The
P / R ratio of sunflower, sorghum and
chickpea was constant with variation in air temperature over the measured range between 16.0
and 34.2 ◦ C. It decreased with temperature increase
only in wheat, but in a range of quite low values
(11.0–21.0 ◦ C). Furthermore, the leaf-scale respiration
response to temperature was insufficient to explain
the corresponding behaviour at canopy scale, pointing at the necessity of always taking into account the
hierarchical scale of the investigated system.
These findings indicate that the assumption of an invariant CUE over the whole crop cycle remains overall
valid, under different ranges of nitrogen levels, variable field thermal regimes, and for different species,
provided that the possible modifications introduced by
the different respiratory costs of biomass composition
during the reproductive stage are taken into account.
These modifications were absent for wheat and grain
sorghum, remarkable for sunflower and, unfortunately,
not assessable for chickpea.
Acknowledgements
This work was supported by Ph.D. Program of Bari
University and the CIHEAM-IAM-Bari Co-operative
Research Program. The authors are grateful to C.
Ranieri, R. Laricchia and A. Divella for their technical
assistance during field measurements.
References
Amthor, J.S., 1986. Evolution and applicability of a whole-plant
respiration model. J. Theor. Biol. 122, 473–490.
Amthor, J.S., 1989. Respiration and Crop Productivity. Springer,
New York, 215 pp.
Amthor, J.S., Baldocchi, D.D., 2001. Terrestrial higher plant
respiration and net primary production. In: Roy, J., Saugier, B.,
Mooney, H.D. (Eds.), Terrestrial Global Productivity. Academic
Press, London, pp. 33–59.
Baldocchi, D.D., 1994. A comparative study of mass and energy
exchange rates over a closed C3 (wheat) and open C4 (corn)
crop: CO2 exchange and water use efficiency. Agric. For.
Meteorol. 67, 291–321.
Ball, J.T., 1987. Calculations related to gas-exchange. In: Zeiger,
E., Farquhar, G.D., Cowan, I.R. (Eds.), Stomatal Function.
Stanford University Press, Stanford, CA, pp. 445–476.
Biscoe, P.V., Scott, R.K., Monteith, J.L., 1975. Barley and its
environment. III. Carbon budget of the stand. J. Appl. Ecol.
12, 269–293.
Byrd, G.T., Sage, R.F., Brown, R.H., 1992. A comparison of dark
respiration between C3 and C4 plants. Plant Physiol. 100, 191–
198.
Cheng, W., Sims, D.A., Luo, Y., Coleman, J.S., Johnson, D.W.,
2000. Photosynthesis, respiration and net primary production
of sunflower stands in ambient and elevated atmospheric CO2
concentrations: an invariant NPP:GPP ratio? Global Change
Biol. 6, 931–941.
Choudhury, B.J., 2001. Modelling radiation- and carbon-use
efficiencies of maize, sorghum, and rice. Agric. For. Meteorol.
106, 317–330.
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
Connor, D.J., Hall, A.J., 1997. Sunflower physiology. In: Sunflower
Technology and Production, Agronomy Monograph no. 35.
American Society of Agronomy, Crop Science Society of
America, Soil Science Society of America, Madison, USA,
pp. 113–182.
Connor, D.J., Sadras, V.O., 1992. Physiology of yield expression
in sunflower. Field Crops Res. 30, 333–389.
Demetriades-Shah, T.H., Fuchs, M., Kanemasu, E.T., Flitcroft, I.,
1992. A note of caution concerning the relationship between
cumulated intercepted solar radiation and crop growth. Agric.
For. Meteorol. 58, 193–207.
Denmead, O.T., Dunin, F.X., Wong, S.C., Greenwood, E.A.N.,
1993. Measuring water use efficiency of Eucalyptus trees with
chamber and micrometeorological techniques. J. Hydrol. 150,
649–664.
Dewar, R.C., 1996. The correlation between plant growth and
intercepted radiation: an interpretation in terms of optimal plant
nitrogen content. Ann. Bot. 78, 125–136.
Dewar, R.C., Medlyn, B.E., McMurtrie, R.E., 1999. Acclimation
of the respiration/photosynthesis ratio to temperature: insight
from a model. Global Change Biol. 5, 615–622.
Dugas, W.A., Fritschen, L.J., Gay, L.W., Held, A.A., Matthias,
A.D., Reicosky, D.C., Steduto, P., Steiner, J.L., 1991. Bowen
ratio, eddy correlation, and portable chamber measurements
from irrigated spring wheat. Agric. For. Meteorol. 56, 1–20.
Farrar, J.F., 1985. The respiratory source of CO2 . Plant Cell
Environ. 8, 427–438.
Farrar, J.F., Williams, J.H.H., 1991. Control of the rate of
respiration in roots: compartmentation, demand, and the supply
of substrate. In: Emes, M.J. (Ed.), Compartmentation of Plant
Metabolism in Non-photosynthetic Tissues. Soc. Exp. Biol.
Sem. Ser., vol. 42. Cambridge University Press, Cambridge,
pp. 167–188.
Garcia, R., Kanemasu, E.T., Blad, B.L., Bauer, A., Hatfield, J.L.,
Major, D.J., Reginato, R.J., Hubbard, K.G., 1988. Interception
and use efficiency of light in winter wheat under different
nitrogen regimes. Agric. For. Meteorol. 44, 175–186.
Gifford, R.M., 1994. The global carbon cycle: a viewpoint on the
missing sink. Aust. J. Plant Physiol. 21, 1–5.
Gifford, R.M., 1995. Whole-plant respiration and photosynthesis
of wheat under increased CO2 concentration and temperature:
long-term vs. short-term distinctions for modelling. Global
Change Biol. 1, 385–396.
Held, A.A., Steduto, P., Orgaz, F., Matista, A., Hsiao, T.C., 1990.
Bowen ratio/energy balance technique for estimating crop net
CO2 assimilation, and comparison with a canopy chamber.
Theor. Appl. Climatol. 42, 203–213.
Hocking, P.J., Steer, B.T., 1983. Distribution of nitrogen during
growth of sunflower (Helianthus annuus L.). Ann. Bot. 51,
787–799.
Högberg, P., Nordgren, A., Buchmann, N., Taylor, A.F.S., Ekblad,
A., Högberg, M.N., Nyberg, G., Ottosson-Löfvenius, M., Read,
D.J., 2001. Large-scale forest girdling shows that current
photosynthesis drives soil respiration. Nature 411, 789–792.
Hurlbert, S.H., 1984. Pseudoreplication and the design of
ecological field experiments. Ecol. Monogr. 54, 187–211.
Körner, C., Scheel, J.A., Bauer, H., 1979. Maximum leaf diffusive
conductance in vascular plants. Photosynthetica 13, 45–82.
35
Lambers, H., 1985. Respiration in intact plants and tissues:
its regulation and dependence on environmental factors,
metabolism and invaded organisms. In: Douce, R., Day, D.A.
(Eds.), Higher Plant Cell Respiration. Encycl. Plant Physiol.
(NS), vol. 18. Springer-Verlag, Berlin, Germany, pp. 418–473.
Landsberg, J.J., Waring, R.H., 1997. A generalised model of
forest productivity using simplified concepts of radiation-use
efficiency. For. Ecol. Manage. 95, 209–228.
Lawlor, D.W., 1995. Photosynthesis, productivity and environment.
J. Exp. Bot. 46, 1449–1461.
Loomis, R.S., Connor, D.J., 1992. Crop Ecology: Productivity and
Management in Agricultural Systems. Cambridge University
Press, Cambridge, 538 pp.
Lund, C.P., Riley, W.J., Pierce, L.L., Field, C.B., 1999. The effects
of chamber pressurization on soil-surface CO2 flux and the
implications for NEE measurements under elevated CO2 . Global
Change Biol. 5, 269–281.
Luo, Y., Sims, D.A., Thomas, R.B., Tissue, D.T., Ball, J.T., 1996.
Sensitivity of leaf photosynthesis to CO2 concentration is an
invariant function for C3 plants: a test with experimental data
and global applications. Global Biogeochem. Cy. 10, 209–222.
Luo, Y., Hui, D., Cheng, W., Coleman, J.S., Johnson, D.W., Sims,
D.A., 2000. Canopy quantum yield in a mesocosm study. Agric.
For. Meteorol. 100, 35–48.
McCree, K.J., 1988. Sensitivity of sorghum grain yield to ontogenic
changes in respiration coefficient. Crop Sci. 28, 114–120.
Mitchell, R.A.C., Lawlor, D.W., Young, A.T., 1991. Dark
respiration of winter wheat crop in relation to temperature and
simulated photosynthesis. Ann. Bot. 67, 7–16.
Monteith, J.L., 1994. Validity of the correlation between
intercepted radiation and biomass. Agric. For. Meteorol. 68,
213–220.
O’Neill, R.V., De Angelis, D.L., Waide, J.B., Allen, T.F.H.,
1986. Hierarchical Concept of Ecosystems. Princeton University
Press, Princeton, NJ, 253 pp.
Pavlik, B.M., 1983. Nutrient and productivity relations of the
dune grasses Ammophila arenaria and Elymus mollis. I. Blade
photosynthesis and nitrogen use efficiency in the laboratory and
field. Oecologia 57, 227–232.
Penning de Vries, F.W.T., 1975. The use of assimilates in
higher plants. In: Cooper, J. (Ed.), Photosynthesis and
Productivity in Different Environments. Cambridge University
Press, Cambridge, NY, pp. 459–480.
Ranty, B., Cavaliè, G., 1982. Purification and property of ribulose
1,5-bisphosphate carboxylase from sunflower leaves. Planta
155, 388–391.
Rochette, P., Desjardins, R.L., Pattey, E., Lessard, R., 1996.
Istantaneous measurements of radiation and water use
efficiencies of a maize crop. Agron. J. 88, 627–635.
Ryan, M.G., 1991. Effects of climate change on plant respiration.
Ecol. Applic. 1, 157–167.
Sage, R.F., Pearcy, R.W., 1987. The nitrogen use efficiency of C3
and C4 plants. I. Leaf nitrogen, growth, and biomass partitioning
in Chenopodium album (L.) and Amaranthus retroflexus (L.).
Plant Physiol. 84, 954–958.
Saigusa, N., Yamamoto, Y., Murayama, S., Kondo, H., Nishimura,
N., 2002. Gross primary production and net ecosystem change
36
R. Albrizio, P. Steduto / Agricultural and Forest Meteorology 116 (2003) 19–36
of a cool-temperate deciduous forest estimated by the eddy
covariance method. Agric. For. Meteorol. 112, 203–215.
Sinclair, T.R., Muchow, R.C., 1999. Radiation use efficiency. Adv.
Agron. 65, 215–265.
Steduto, P., 1993. Water vapour and CO2 fluxes of post-anthesis
maize in the field under two soil-water regimes: leaf vs. canopy
scale. Ph.D. Dissertation, University of California, Davis, 180
pp.
Steduto, P., Hsiao, T.C., 1994. Radiation use efficiency of maize
under well watered and water deficit conditions: cumulative
vs. finite increment approach. In: Proceedings of the 3rd
European Society of Agronomy Meeting, Abano-Padova, Italy,
18–22 September 1994. ESA, BP52, Colmar Cedex, France,
pp. 418–419.
Steduto, P., Çetinkökü, Ö., Albrizio, R., Kanber, R., 2002.
Automated closed-system canopy-chamber for continuous
field-crop monitoring of CO2 and H2 O fluxes. Agric. For.
Meteorol. 111, 171–186.
Suyker, A.E., Verma, S.B., 2001. Year-round observations of the
net ecosystem exchange of carbon dioxide in a native tallgrass
prairie. Global Change Biol. 7, 279–289.
Tjoelker, M.G., Oleksyn, J., Reich, P.B., 1999. Acclimation of
respiration to temperature and CO2 in seedlings of boreal
tree species in relation to plant size and relative growth rate.
Global Change Biol. 49, 679–691.
Wagner, S.W., Reicosky, D.C., Alessi, R.S., 1997. Regression
models for calculating gas fluxes measured with a closed
chamber. Agron. J. 89, 279–284.
Waring, R.H., Landsberg, J.J., Williams, M., 1998. Net primary
production of forests: a constant fraction of gross primary
production? Tree Physiol. 18, 129–134.
Whitfield, D.M., Connor, D.J., Hall, A.J., 1989. Carbon dioxide
balance of sunflower subjected to water stress during
grain-filling. Field Crops Res. 20, 65–80.