Open-System Chamber for Measurements of Gas Exchanges at Plant

Feb 8, 2006 - The control of temperature rise inside the chamber, which should be kept low, and the accurate measurement of the air flow are two cruci...
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Environ. Sci. Technol. 2006, 40, 1950-1955

Open-System Chamber for Measurements of Gas Exchanges at Plant Level GIOVANNI ALTERIO,* PASQUALE GIORIO, AND GIUSEPPE SORRENTINO CNR - ISAFOM, Consiglio Nazionale delle Ricerche, Istituto per i Sistemi Agricoli e Forestali del Mediterraneo, Via Patacca 85, 80056 Ercolano (Napoli), Italia

Gas exchanges of whole canopy can be studied by covering entire plants with a chamber and using portable infrared gas analyzers (IRGAs) to measure CO2 and H2O exchanged with the air blown through the chamber enclosure. The control of temperature rise inside the chamber, which should be kept low, and the accurate measurement of the air flow are two crucial aspects for realistic and precise estimation of photosynthesis and transpiration. An automated open-system plant chamber (clear flexible balloon enclosure) for small plants was developed to ameliorate such a technique. The temperature rise is here predicted by heat balance analysis inside the chamber. The analysis shows that when as much as 500 W m2 of solar radiation is converted to sensible heat, a flow rate of 0.98 mol s-1 (≈20 L s-1) of air blown into a cylindershaped enclosure (0.8 m high, 0.5 m wide) is adequate to limit temperature increase to 2 K. An improved calibration for the measurement of the chamber airflow was obtained by combining the use of a Pitot tube anemometer with the classical CO2 injection approach. The concentration increase due to the injection of CO2 at a known rate into the chamber was predicted by the air flow calculated from the “Pitot” air velocity. The turbulent regime of air assured that a single-point Pitot measurement was enough for a good estimation (slope ) 0.99; R2) 0.999) of the actual air flow. The open-system chamber was tested on potted sunflower (Helianthus annuus, L.) and maize (Zea mays, L.) plants under variable solar radiation, temperature, and air humidity during the daytime. As expected, similar rates of maximal leaf-area based photosynthesis (about 40 µmol m-2 s-1) were observed in the two species confirming the reliability of our system. The consistency of data also resulted from the typical relationships observed between photosynthetic rate and light.

Introduction In the past, most research on plant gas exchanges has focused attention at leaf level or at canopy level. Since most commercially available equipment has been designed for leaf measurements, leaf photosynthesis has been studied in more detail than canopy photosynthesis. Whole-canopy carbon dioxide exchange measurements are important, * Corresponding author e-mail: +390815746606; fax: +390817718045. 1950

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[email protected];

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because it is difficult to extrapolate single-leaf measurements to canopy level. Measurement of whole-canopy net CO2 exchange rate (NCER) facilitates instantaneous estimation of light conversion efficiency and provides a tool for quantitative assessment of the impact that environmental changes have upon biological processes. However, a better understanding of the major environmental and/or physiological sources of variation in whole-canopy NCER is fundamental for refining the method for taking such measurements. Strategies for flux measurements should be developed to cover the full range of environmental conditions and spatial and temporal variability (1). Whole-canopy NCER studies started many decades ago in fruit trees but were limited to a single tree (2, 3) using a nonmovable bulky apparatus. Numerous studies of small plants’ gas exchanges have been conducted over the past 40 years, often with the assistance of sophisticated mobile laboratories in the field (4). Musgrave and Moss (5) made one of the first attempts to enclose plants’ stands in the field to measure gas exchange. Studies such as those of Acock et al. (6), Drake et al. (7), Gent et al. (8), and Jones et al. (9) have used various configurations and techniques on agronomic and natural plant stands. To obtain further environmental control for plant-stand gas exchange measurements, sunlit chambers have been developed for use in greenhouses (6, 10), while a variety of smaller chambers, with more rigorous environmental control and electrical lighting, have been developed for use in the laboratory (11-14). A whole-canopy open-system chamber system is essentially similar to a leaf chamber: outside air is continuously blown at a known flow rate into the enclosure (e.g., a plastic balloon) where gas exchanges occur. The difference of both water vapor and CO2 concentration between incoming and exiting air, measured by infrared gas analyzers, allows the estimation of transpiration and photosynthesis. The advantages and disadvantages of chambers for monitoring canopy gas exchanges and factors that should be considered in designing an open system are summarized by Garcia et al. (15). Two major disadvantages of the openchamber system regard the air flow measurement and the temperature rise into the enclosure. In fact, air flow through the enclosure has to be accurately monitored because error in this measurement is directly translated into an error in the estimated gas-exchange rates. On the other hand, sensible heat input to a chamber will cause a rise in temperature that could make the environment within the chamber unrepresentative of the surrounding environment. In recent studies, the lightweight clear plastic “balloon” system, such are that of Corelli-Grappadelli and Magnanini (16), and Giuliani et al. (17), has allowed inexpensive whole-canopy NCER measurements with portable CO2 analyzers. To improve the optical proprieties of the enclosure, a “Milar” whole-canopy chamber for diurnal measurements of whole-canopy NCER was used by Francesconi et al. (18, 19), and by Lakso, et al. (20). However recent studies, such those of Corelli-Grappadelli and Magnanini (16) and Giuliani et al. (17), did not take into account the heat balance analysis inside the canopy chamber, and the calibration of the air measurement system, which is blown into the chamber, is unclear. We developed an automated open-system chamber for (steady-state) gas-exchange measurements of large herbaceous species to refine and improve exiting measurements techniques. In particular, we present a heat-balance analysis inside the chamber and an improved calibration of the measurement system of the air flow, which is blown into the chamber. Our experimental data agree well with theoretical 10.1021/es052094o CCC: $33.50

 2006 American Chemical Society Published on Web 02/08/2006

FIGURE 1. Scheme of the whole-plant open-system chamber for gas exchange measurements. results of heat-balance analysis and show that the calibration of the air flow measurement system allows estimation of precise CO2 exchange.

Materials and Methods A schematic diagram of our whole-plant open chamber is shown in Figure 1. During measurement, air is pumped through the system by an alternating current (AC) blower (Orieme, Milano, Italy, model OIC122M) mounted at the wall of a carrying case. Since incoming CO2 concentration must be stable at the inlet port of the chamber, air is sucked in through the filtered inlet located at 3 m above the ground, and then is blown into the plastic balloon through a PVC rigid duct, the diameter φ of which is 0.074 m. An autotransformer (Orieme, Milano, Italy, model OS SCS) is used to regulate the blower and to get variable air velocity up to 8.8 m s-1, which corresponds to 37 dm3 s-1. The inlet air velocity is measured inside this PVC rigid duct by a Pitot tube anemometer (Dwyer, Michigan City, IN, model 167-6-CF), which serves as flow meter. Two model-T Copper-Constantan thermocouples (Omega Engineering, Stamford, CT) measure the air temperature respectively in the entrance (designated Reference section in Figure 1) and at the exaust (designated Analysis section in Figure 1). Since there is no thermocouple inside the chamber it is assumed that exaust gas has the same temperature as air that has been thoroughly mixed within the enclosure. The Pitot tube is connected to a LVDT differential pressure transducer for very low-pressure measurement (Lucas Schaevitz, Hampton, VA, model P3061) to calculate the air velocity V and the air flow rate (21). The air flow rate determines the boundary layer thickness around leaves which, in turn, influences the transfer of mass (CO2 and H2O) and energy (heat) between the leaves and ambient air. Therefore to obtain a uniform environment inside the chamber, ideally, the air flow rate should be about 2-3 chamber volumes/minute (22). The pressure transducer and the thermocouples are connected to distributed signal conditioning and I/O modules (National Instruments Corporation, Austin, TX, model 6B11 and 6B12) that transmit data to a portable personal computer, which serves as a data-logger. A “homemade” control program, which has been written with Labwindows CVI (National Instruments Corporation), runs on a personal computer and checks the functioning of the system and records, by a scanning frequency of 1 Hz, the air volume flow into the chamber, the light intensity, and the air temperature.

In the operative conditions (which correspond to air speed variable between 2 and 8.8 m s-1), the flow inside the PVC rigid duct is turbulent since the Reynolds number is Re ) FVD/µ ) 10 125, where F and µ are air density and viscosity, while L is the diameter of the duct (23). Two miniature diaphragm pumps (KNF, Trenton, NJ, model NMP9) are used to pump small air volumes (800 cm3 min-1) from the inlet and the outlet gas of the chamber (Reference and Analysis) to a portable infrared gas analyzer (IRGA; LI-COR, Lincoln, NE, model LI-840) to measure the molar fractions of CO2 and H2O at a frequency of 1 sample every minute. The chamber volume is determined by plant size: a big chamber reduces uncertainty from spatial variability associated with biological process, and from disturbances of the canopy near the chamber covering. The size of the enclosure was limited by the easiness of construction and handling, and by power requirements for air exchange and mixing of enclosed air. In this case the volume is about 150 dm3 and its cover is made by transparent, low-density polyethylene film (0.025 mm thick): when the blower is on, the chamber shape is almost a vertical cylinder (0.8 m high, 0.5 m wide). Polyethylene was used because of its low cost, its good spectral characteristics, and because of practical advantages of working with it. This material is not the most appropriate choice with respect to CO2 and H2O permeability, but it is cheaper than Mylar, which has better permeability characteristics. An external Quantum Sensor (LI-COR, model LI-190) continuously measured incident photosynthetically active radiation (PAR) over the 400-700 nm waveband. The quantum sensor was placed horizontally on top of a support stake near the chamber.

Analysis of the Open Chamber Environment Heat Balance Inside the Canopy Open Chamber. Maintenance of chamber air temperature is a critical design consideration, since a sensible heat input to the chamber will cause a rise in temperature that could make the environment inside the chamber unrepresentative of the surrounding environment. It is important to know the minimum flow rate necessary to limit the temperature increase within the chamber, compared to the external air, which has to be kept as low as 2 K to avoid any overheating of the plant (15). The energy input to the open chamber is the net radiation Q received at the chamber surface: this VOL. 40, NO. 6, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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available energy is partitioned into latent heat (LE) which is the heat involved in the transpiration in plant tissues and sensible heat (H). Sensible heat H warms the air, so temperature inside the chamber must be considered. In fact, chamber covering material can trap thermal radiation resulting in an increase in temperature of the chamber and its contents. The energy budget of the open chamber can be written as follows:

Q ) H + LE We can approximate the heat balance inside the chamber stating that the total heat input (Q) is converted only in sensible heat (H) in the chamber (LE ) 0) and, hence, it is balanced by conduction through the chamber (qcond) and by forced convection from ventilation through the walls of the chamber (qconv)

Q ) H ) qcond + qconv

(1)

As no crop evaporation has been taken into account in the formula 1, the sensible heat transfer is proportional to the temperature differential between inside and external air of the chamber (23)

Q)

∆T k fMcp + Nu Aw Aplan D

(

)

(2)

where Q is total heat input; ∆T is the temperature differential across inside and outside of the open chamber; Aplan is the open chamber plan-form area; f is the air flow; M is the molecular weight of air; cp is specific heat at constant pressure of air; Nu is Nusselt number; k is the thermal conductivity of air; D is the characteristic linear dimension of open chamber; and Aw is the wall area of the open chamber. To calculate Nusselt number, when the blower is on, the chamber shape is almost a vertical cylinder, hence its diameter can be chosen as the characteristic linear dimension of chamber [D ≈ 0.50 m]. Extending a procedure devised in aeronautical engineering (24), the open chamber plan-form area Aplan is introduced. In general, Aplan is defined as the area of the open chamber plan-form, projected onto a plane of reference which is usually the ground plane. In this case, the plan-form area is the area of a circle whose diameter is the diameter D: it follows that Aplan ≈ 0.20 m2. The chamber can be also considered like a pipe, hence, Nusselt number can be calculated by using formulas which are used to evaluate heat transfer in pipes (23):

[ (DL) ] Re

Nu ) 0.023 1 +

0.7

0.8

Pr0.33

where L is the height of chamber (L ≈ 0.80 m), Re is the Reynolds number, and Pr is Prandtl number. Assuming a low wind speed inside the chamber, V ≈ 2 m s-1, the minimum flow rate f necessary to limit the temperature increase within the chamber is calculated from eq 2:

QAplan k - Nu Aw ∆T D f) Mcp

(3)

If it is conservatively assumed that 500 W m-2 of net radiation (Q) was converted to sensible heat (H), then the system (Aw ≈ 1.7 m2) would require a minimum flow rate f of 0.98 mol s-1 (≈20 L s-1) to limit the temperature increase (∆T) to 2 K, with no evaporation. Any evapotranspiration will reduce the temperature rise for a given flow rate. Alteration of Light Spectra Inside the Chamber. It is important to know the spectral characteristics of the cover 1952

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FIGURE 2. Turbulent velocity profiles, V ) V(r), across the PVC rigid duct (O ) 0.074 m) measured with the Pitot tube. of the chamber which influences the reduction of incident solar radiation intercepted by the enclosed plants, the increase of diffused solar radiation inside the chamber, and the glass house effect. To provide cover material identification and characterization in a variety of environments, the transmittance spectra of the polyethylene film was checked with a portable, scalable, high-performance, lab-quality near-infrared (NIR) spectroradiometer (Analytical Spectral Devices, model FSP 350-2500 P). First, the radiance of a white reference panel (Spectralon) was measured. Then, the polyethylene film was disposed over the white panel and its radiance was measured. Spectral transmittance was obtained by dividing the latter by the former radiance measurements. The spectrum of polyethylene film indicates overall high transmittance and a number of absorption bands. Radiation intensity decreased 11.5% over the 300-1100 nm wavelength range, while the spectral composition was essentially unchanged: there is no absorption band between 400 and 700 nm which is the band of photosynthetically active radiation (data not shown). Calibration of the Air Flow Rate Measurement System. The flow rate measurement was carried out by two different methods. (a) Calculating the Flow Rate from the Velocity Profile Across the PVC Rigid Duct. Since air velocity varies between the center and the pipe walls because of air viscosity, accurate positioning of the Pitot tube is necessary to take reliable readings. The volumetric airflow rate Φ can be directly determined by integration from the velocity profile across the duct V(r) measured by Pitot tube:

Φ ) 2π

∫

r)R

r)0

V(r) r dr

where r is the radial distance which varies from the centerline (r ) 0) to the duct wall (r ) R). Four turbulent velocity profiles across the duct, which were measured with the Pitot tube, are reported in Figure 2. Since the data set is usually limited to a finite number of values V(r), the exact analytic integral cannot be performed. However, a numerical estimate can be used to approximately evaluate the flow rate. In this case the flow rate can be estimated using the trapezoidal rule (25): n-1

∑V r i

Φ ) 2πR

i)1

n

i

(4)

FIGURE 3. Relationship between inviscid flow rate (Φ ) VA where V(r) is the air velocity measured with the Pitot at the center of conduct and A is the cross sectional area of the duct) and flow rate obtained by numerical integration of the velocity profiles shown in Figure 2.

FIGURE 4. Comparison between actual ∆CO2 measured by the IRGA and the ∆CO2 calculated by solving eq 5 and using the flow rate calculated from eq 4. where n is the number of interval in which the radius has been divided. The integrated air flow rates calculated by eq 4 are compared in Figure 3 with the “inviscid” single point flow rates which are calculated considering the air without viscosity (e.g., Φ ) VA, where V is the air velocity measured by Pitot in the center of the duct and A is the cross sectional area of the duct). The slope of the regression line in Figure 3 is more or less equal to one, indicating that the inviscid single point measurement can be used to estimate the actual flow rate. (b) Calculating the Flow Rate by CO2 Injections of Known Concentration and Flow. Calculation of flow rate Φ can also be done by injection of CO2 of known concentration and flow according to the following equation:

Φ)

known added CO2flux ∆CO2

(5)

Air was added at several flow rates and at a constant CO2 concentration of 20 000 µmol mol-1 to the inlet air stream of the chamber to mimic a gas exchange. By solving eq 5 for ∆CO2 using Φ obtained from eq 4, an estimated CO2 differential was calculated which predicted the actual ∆CO2 measured by the IRGAs (Figure 4). The relationship reported in Figure 4 actually indicates that the (IRGA) measured ∆CO2 was 1.2 times the ∆CO2 estimated from the CO2-injection procedure. This calibration was used to correct our measurements of ∆CO2. The results indicate that the system is particularly reliable regarding the air flow measurement as it is based on a Pitot tube which showed a good correspondence with Φ obtained with the approach of the CO2 injection technique.

Experimental Setup Our open-system chamber was tested on potted plants of sunflower (Helianthus annuus, L.) and maize (Zea mays, L.) grown in the open on a sandy-loam soil at the headquarter of CNR-ISAFOM institute in Ercolano (Southern Italy) where the experiment took place under typical Mediterranean

climate. The plants were kept well irrigated and no symptoms of any biotic or abiotic stress were observed. Measurements were carried out in summertime and were run for 7-8 h through the day to provide an adequate range of air temperature, relative humidity, and light intensity: during this experimental period plants were at starting of the flowering phase hence there was no appreciable vegetative growth. The measurements were made under clear conditions, but at times, the weather did not allow measurements under clear conditions for an entire day at every period. Plant leaf area was estimated in sunflower by applying an empirical equation (26) to linear measurement of width and length of all plant leaves. In the case of maize, a triangular shape for the leaf lamina was assumed to accordingly calculate the area. Three sets of temperature data were recorded: ambient air, incoming and outgoing chamber air, leaf surface temperature on a reference sunflower or maize in open air and on the enclosed potted plants. Thermometer readings were checked for uniformity before use. We imposed the air flow rate calculated by eq 3, that is 20 L s-1, to limit temperature increase ∆T inside the open chamber to 2 K. Carbon Dioxide and Water Vapor Gradients. As said above, in an open system, photosynthesis and transpiration are computed from the differences in carbon dioxide (∆CO2) and water vapor concentrations (∆H2O) between in-chamber conditions (AN - Analysis, cf. Figure 1) and pre-chamber conditions (REF - Reference), and assuming that the exit gas has the same concentration as air that has been thoroughly mixed within the enclosure. On these assumptions, the equations are (27)

A)

φ ∆CO2 φ ([CO2]REF - [CO2]AN) ) S S

(6)

E)

φ ∆H2O φ ([H2O]AN - [H2O]REF) ) S S

(7)

where A ) photosynthetic rate [µmol m-2 s-1]; E ) transpiration rate [mmol m-2 s-1]; φ ) air flow rate [mol s-1]; [CO2] ) carbon dioxide concentration [µmol mol-1]; [H2O] ) water vapor concentration [mmol mol-1]; and S ) canopy leaf area [m2]. Note that in this way both deltas (∆) in eqs 6 and 7 are positive for plants which are normally photosynthesizing and transpiring.

Results and Discussion Typical scatter of raw data for the diurnal course of ∆CO2, ∆H2O, photosynthetically active radiation (PAR), and the humidity of analysis air are reported in Figure 5 for maize, and Figure 6 for sunflower. In all our experimental measurements the ∆CO2 and ∆H2O are acceptably high to obtain a good resolution of whole gas exchanges measurement. Whole plant NCER and transpiration rate calculated by using the eqs 6 and 7 from raw data of Figure 5 (maize) and 6 (sunflower) are reported in Figure 7. In both species, NCER follows the time course of PAR (cf. with Figures 5 and 6) which was lower and variable for sunflower during the early afternoon compared with maize. Maize plant (Figure 5) with a PLA (plant leaf area) of 0.47 m2 showed a maximum ∆CO2 of 20 µmol mol-1 in mid-afternoon (16:00), whereas for the sunflower plant (Figure 6) it was 15 µmol mol-1 with a PLA of 0.35 m2. This explains why both species plants had similar NCER (about 40 µmol m-2 s-1) at mid-afternoon and showed the same time-course when PAR was similar in the late afternoon. Sunflower (C3 species) showed photosynthetic rates comparable with that of maize (C4 species) as reported VOL. 40, NO. 6, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 5. Time course of carbon dioxide and water vapor concentration differential (top) and PAR and RH of Analysis air (bottom) measured at 1-min intervals during the afternoon of doy ) 217 (doy ) day of year), on a maize plant with plant leaf area (PLA) of 0.47 m2. Whole plant open chamber air flow rate was set at 20 dm3 s-1.

FIGURE 8. Response curves of photosynthetic assimilation rate (A, µmol m-2 s-1) to the photosynthetically active radiation (PAR, µmol m-2 s-1) for both maize and sunflower as obtained from data of Figures 5-7.

FIGURE 9. Experimental temperature differential between inside and external air of the chamber (maize plant was inside the chamber).

FIGURE 6. Time course of carbon dioxide and water vapor concentration differential (top) and PAR and RH of Analysis air (bottom) measured at 1-min intervals during the afternoon of doy ) 219 (doy ) day of year), on a sunflower plant with plant leaf area (PLA) of 0.35 m2. Whole plant open chamber air flow rate was set at 20 dm3 s-1.

ship observed between A and PAR in both species (Figure 8). We showed that a sunflower plant had a net CO2 exchange rate A (µmol m-2 s-1) similar to a maize plant under similar condition as it would have expected. Influence of Evaporation on the Thermal Balance Inside the Chamber. As said above, we imposed the air flow rate calculated by eq 5 that is 20 L s-1 in order to limit temperature increase ∆T inside the open chamber, with respect to the ambient temperature air, to 2 K. The magnitude of the temperature increase measured in the chamber resulted acceptable (Figure 9) as it did not exceed a threshold of 1.3 K under sunny conditions, when, even at high ambient air temperatures, transpiration prevents large increase in leaf temperature. Equation 1 states the heat balance of the open chamber without concerning crop evaporation. On the other hand, if we take into account the latent heat of vaporization of the water vapor in air (qevap)

Q ) H + LE ) qcond + qconv + qevap

(8)

Using the definition of rate of evaporation, E, eq 8 becomes

Q)

MH2OEScrop λ ∆T k fMcp + Nu Aw + Aplan D Aplan

(

)

(9)

where MH2O ) molecular weight of water; Scrop ) crop (maize) surface area; and λ ) latent heat of vaporization of water. From eq 9 we can calculate the temperature increase ∆T within the chamber in our experimental situation FIGURE 7. Net CO2 exchange rate A (µmol m-2 s-1) and transpiration rate E (mmol m-2 s-1) for maize and sunflower expressed on leaf area basis, calculated from the data of Figures 5 and 6 using eqs 6 and 7. in the literature (28). The max differentials observed in maize of 20 µmol mol-1 for CO2 and 6 mmol mol-1 for H2O (Figure 5) are comparable with those reported by Lakso et al. (20). These results makes us confident on the reliability of our system which was further confirmed by the typical relation1954

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∆T )

(QAplan - MH2OEScrop λ)

(fMc

p

k + Nu Aw D

)

(10)

In Figure 7 we read, for the maize, a mean value for E ) 5 mmol m-2 s-1, then from eq 10 we get that the temperature increase inside the open chamber with respect to the ambient air temperature is ∆T ≈ 1 K. This analytical result is consistent with our experimental results which indicated that the magnitude of the temperature increase in the chamber

resulted acceptable as it did not exceed a threshold of 1.3 K. At high ambient air temperatures under sunny conditions, air flow rate set by heat balance considerations was sufficient to limit the temperature increase. At the same time, there was no detrimental effect on the ∆CO2 which remained in the range 4-22 µmol mol-1 (Figures 5 and 6).

Acknowledgments This work was financially supported within the framework of Coordinated CNR-project “Agenzia 2000” No. CNRC003DE7 of the Italian National Council of Research. We are grateful to Dr. Eugenio Magnanini (University of Bologna, Italy), Prof. Stefano Poni (Catholic University of Piacenza, Italy), and Dr. Guido Bongi (CNR-ISAFOM, Perugia, Italy) for their useful suggestions.

Literature Cited (1) Allen, L. H., Jr.; Baker, J. T.; Boote, K. J. The CO2 fertilization effect: higher carbohydrate production and retention as biomass and seed yield. In Global Climate Change and Agricultural Production; Bazzazz, F., Sombroek, W., Eds.; Wiley and Sons: Chichester, 1996; pp 65-100. (2) Heinicke, A. J.; Childers, N. F. The daily rate of photosynthesis during the growing season of 1935, of a young apple tree of bearing age. Cornell Univ. Agric. Exp. Sta. Memoir 1937, 201, 3-52. (3) Sirois, D. J.; Cooper, G. R. The influence of light intensity, temperature and atmospheric carbon dioxide concentration of the rate of apparent photosynthesis of a mature apple tree. Maine Agric. Exp. Sta. Bull. 1964, 626. (4) Field, C. B.; Mooney, H. A. Measuring photosynthesis under field conditions: past and present approaches. In Measurement Techniques in Plant Science; Hashimoto, Y., et al., Eds.; Academic Press: San Diego, CA, 1990; pp 185-205. (5) Musgrave, R. B.; Moss, D. N. Photosynthesis under field conditions: I. A portable, closed system for determining net assimilation and respiration of corn. Crop Sci. 1961, 1, 37-41. (6) Acock, B.; Charles-Edwards, D. A.; Hearn, A. R. Growth response of a Chrysantheum crop to environment: I. Experimental techniques. Ann. Bot. (London) 1977, 41, 41-48. (7) Drake, B. G.; Leadley, P. W. Canopy photosynthesis of C3 and C4 plant communities exposed to long-term elevated treatment. Plant Cell Environ. 1991, 14, 853-860. (8) Gent, M. P. N.; Kiyomoto, R. K. Canopy photosynthesis and respiration in winter wheat adapted and unadapted to Connecticut. Crop Sci. 1992, 32, 425-431. (9) Jones, P.; Allen, L. H.; Jones, J. W.; Valle, R. Photosynthesis and transpiration responses of soybean canopies to short- and longterm CO2 treatments. Agron. J. 1985, 77, 119-126. (10) Hand, D. W. A null balance method for measuring crop photosynthesis in an airtight, daylit controlled-environment cabinet. Agric. Meteorol. 1973, 12, 259-270. (11) Bugbee, B. G. Steady-state canopy gas exchange: system design and operation. HortScience 1990, 27, 770-776. (12) Dutton, R. G.; Jiao, J.; Tsujita, M. J.; Grodzinski, B. Whole plant CO2 exchange measurements for nondestructive estimates of growth. Plant Physiol. 1988, 86, 355-358.

(13) Gerbaud, A.; Andre, M.; Rechaud, C. Gas-exchange and nutrition patterns during the life cycle of an artificial wheat crop. Physiol. Plant. 1988, 73, 471-478. (14) Knight, S. L.; Akers, C. P.; Akers, S. W.; Mitchell, C. A. Minitron II systems for precise control of the plant growth environment. Photosynthetica 1988, 22, 90-98. (15) Garcia, R. L.; Norman, J. M.; McDermitt, D. K. Measurement of canopy gas exchange using an open chamber system. Remote Sensing Rev. 1990, 5 (1), 141-162. (16) Corelli Grappadelli, L.; Magnanimi, E. A whole tree system for gas-exchange studies. HortScience 1993, 28 (1), 41-45. (17) Giuliani, R.; Nerozzi, F.; Magnanini, E.; Corelli Grappadelli, L. Influence of environmental and plant factors on canopy photosynthesis and transpiration of apple trees. Tree Physiol. 1997, 17, 637-645. (18) Francesconi, A. H. D.; Lakso, A. N.; Nyrop, J. P.; Barnard, J.; Denning, S. S. Carbon balance as a physiological basis for the interactions of European Red Mite and Crop Load on “Starkrimson Delicious” Apple trees. J. Am. Soc. Hortic. Sci. 1996, 121 (5), 959-966. (19) Francesconi, A. H. D.; Lakso, A. N.; Denning, S. S. Light and temperature effect on whole-canopy net carbon dioxide exchange rate of apple trees. In International symposium on integrating canopy, rootstocks and environmental physiology in orchard system, Wenatchee, Washington, 17-25 July; Acta Hortic. 1997, 451, 287-294. (20) Lakso, A. N.; Mattii, G. B.; Nyrop, J. P.; Denning, S. S. Influence of European red-mite on leaf and whole-canopy carbon-dioxide exchange, yield, fruit size, quality, and return cropping in starkrimson-delicious apple trees. J. Am. Soc. Hortic. Sci. 1996, 121, 954-958. (21) Anderson, J. D. Fundamentals of Aerodynamics; McGraw-Hill: New York, 1991. (22) Bjo¨rkman, O.; Holmgren, P. Adaptability of the photosynthetic apparatus to light intensity in ecotypes from exposed and shaded habitats. Physiol. Plant. 1963, 16, 889-914. (23) Kreith, F. Principles of Heat Transfer; Dun-Donnelley Publishing Corporation, 1973. (24) Roskam, J.; Lan, C. E. Airplane Aerodynamics and Performance; Darcorporation: Lawrence, KS, 1997. (25) Chapra, S. C.; Canale, R. P. Numerical Methods for Engineers with Personal Computer Applications; McGraw-Hill: New York, 1985. (26) Giorio, P.; Sorrentino, G.; Caserta, P.; Tedeschi, P. Leaf area development of field-grown sunflower plants (Heliathus annuus, L.) irrigated with saline water. Helia 1996, 19 (24), 17-28. (27) Field, C. B.; Ball, J. T.; Berry, J. A. Photosynthesis: principles and field techniques. In Plant Physiological Ecology: Field Methods and Instrumentation; Pearcy, R. W., et al., Ed.; Chapman & Hall: London, 1989. (28) Connor, D. J.; Sadras, V. O. Physiology of yield expression in sunflower. Field Crops Res. 1992, 30, 333-389.

Received for review October 21, 2005. Revised manuscript received January 9, 2006. Accepted January 9, 2006. ES052094O

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