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Published online 27 April 2005
Published in Agron J 97:734-740 (2005)
DOI: 10.2134/agronj2004.0172
© 2005 American Society of Agronomy
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Agronomic Modeling

Evaluating a Leaf-Level Canopy Assimilation Model Linked to CERES-Maize

J. I. Lizasoa,*, W. D. Batchelorb, K. J. Bootea, M. E. Westgatec, P. Rochetted and A. Moreno-Sotomayore

a Agronomy Dep., Univ. of Florida, Gainesville, FL 32611-0500
b Dep. of Agricultural and Biological Engineering, 100 Howell Hall, Mississippi State Univ., Mississippi State, MS 39762
c Dep. of Agronomy, Iowa State Univ., Ames, IA 50011
d Centre de recherche et de développement sur les sols et les grandes cultures, Agric. and Agri-Food Canada, Sainte-Foy, QC G1V 2J3, Canada
e School of Natural Resource Sciences, Univ. of Nebraska, Lincoln, NE 68583-0728

* Corresponding author (jlizaso{at}ufl.edu)

Received for publication June 23, 2004.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUMMARY
 REFERENCES
 
The simple approach of calculating crop growth rate as the product of intercepted light and radiation use efficiency may not adequately represent plant growth under stress conditions. We developed a photosynthesis and respiration model for maize (Zea mays L.) and linked it to CERES-Maize v.3.7, calling the new model CERES-PR. The purpose of this work was to evaluate CERES-PR simulation of photosynthesis at three levels of integration: instantaneous leaf assimilation, hourly canopy assimilation, and seasonal crop growth under conditions where water and N supply were not limiting growth. Instantaneous leaf assimilation measured in field plots were obtained in the central portion of the 13th leaf on three dates during the grain filling to test the model at the leaf level. Carbon dioxide fluxes measured above the canopy with the eddy correlation technique were used to test the model at the canopy level. The progression of leaf area index (LAI) and aboveground biomass from experiments planted at latitudes ranging from 21 to 45° N was used to evaluate the seasonal simulation of crop growth. CERES-PR was in close agreement with measured values. A sensitivity analysis indicated that the temperature function affecting leaf assimilation have a large impact in the simulated growth and grain yield. The new model provides opportunities to simulate plant processes more realistically under stress. Our future efforts will focus on developing new modules to simulate energy balance and stomatal conductance to incorporate into CERES-PR leaf-level C, water, and N balances.

Abbreviations: DOY, day of year • LAI, leaf area index • PAR, photosynthetically active radiation • RMSE, root mean square of the error • RUE, radiation use efficiency • VPD, vapor pressure deficit


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUMMARY
 REFERENCES
 
MANY CROP SIMULATION MODELS, including CERES-Maize (Jones and Kiniry, 1986), calculate daily potential growth rate (g DW plant–1 d–1) as the product of the canopy-intercepted photosynthetically active radiation (PAR, MJ PAR plant–1 d–1) and the radiation use efficiency (RUE, g DW MJ–1). As environmental conditions deviate from optimum, the species-specific RUE value is multiplied by appropriate stress factors. This simple RUE approach has proven useful for predicting crop growth and yield under a range of environmental conditions.

The RUE approach assumes that canopy-captured PAR is the main constraint for crop growth under field conditions (Christy et al., 1986). The RUE itself encompasses two major plant physiological processes of photosynthesis and respiration. The concept of multiplying RUE by stress factors essentially includes effects of all growth-limiting factors other than light, such as temperature, water, and N. No interaction among stresses is considered and usually only the most limiting stress is used in the calculation of daily plant growth. Although simple and convenient, the RUE approach has limitations that reduce the accuracy of simulations under stress. Photosynthesis and respiration exhibit different responses to and interactions with environmental conditions. For example, photosynthetic rate in maize increases with temperature up to a maximum around 35°C, then decreases at higher temperatures (Oberhuber and Edwards, 1993; Naidu et al., 2003). The rate of dark respiration, however, increases exponentially with temperature (Oberhuber and Edwards, 1993). At low light intensity, the optimum temperature for photosynthesis is substantially lower than at saturating light intensity (Oberhuber and Edwards, 1993). Because of these limitations, Loomis and Amthor (1999) proposed that models simulating photosynthesis and respiration directly replace RUE-based models.

In a companion paper we developed a canopy photosynthesis and respiration model and linked it to CERES-Maize v3.7 (Lizaso et al., 2005). The resulting model is called CERES-PR. CERES-PR conforms to the minimum data set requirements of DSSAT models (www.icasa.net/standards/pdf/icasafls.pdf), thus requiring only daily records of solar radiation (MJ m–2), maximum and minimum temperature (°C), and rainfall (mm). Under these restrictions, CERES-PR simulates daily crop assimilation and respiration rates in response to incident light, leaf age, and air temperature. In theory, this overcomes the limitations of the RUE approach. The purpose of the present paper is to evaluate the performance of CERES-PR for simulating instantaneous leaf assimilation rates, hourly canopy assimilation, and in-season growth dynamics under conditions where water and N supply are not limiting growth.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 SUMMARY
 REFERENCES
 
Model Description
CERES-PR is a version of CERES-Maize that simulates instantaneous leaf gross assimilation as affected by light intensity, air temperature, and leaf aging (Lizaso et al., 2005). Photosynthetic contributions are aggregated over all leaf positions for sunlit and shaded leaf classes, integrating for the entire canopy on an hourly time step and accumulated during the day to compute daily gross assimilation. Canopy maintenance respiration (Wilkerson et al., 1983) and growth respiration (Penning de Vries and van Laar, 1982) are subtracted from gross assimilation, to compute the potential daily growth rate (g plant–1). These calculations replace the radiation use efficiency approach in the current version of CERES-Maize. CERES-PR also includes a new leaf area model (Lizaso et al., 2003a), and a new algorithm to estimate the photosynthetically active radiation component in the incident solar radiation (Lizaso et al., 2003b).

We compared the assimilation rates simulated by CERES-PR against field measurements using independent data sets at three levels of integration: instantaneous leaf assimilation, hourly canopy assimilation, and seasonal crop growth. Model simulations were compared with instantaneous leaf assimilation reported by Moreno-Sotomayor et al. (2002), with hourly canopy assimilation measured by Rochette et al. (1996), and with seasonal growth data (leaf area and aboveground biomass) reported by various authors (Rochette et al., 1996; Westgate et al., 1997; Hoogenboom et al., 1999; Boedhram et al., 2001).

Instantaneous Leaf Assimilation
Leaf photosynthesis was evaluated in field grown plants during grain filling. The maize hybrid Pioneer 3394 was seeded on 18 May 1995 at Mead, NE, at a rate of 6.4 seeds m–2 on north–south rows separated by 76 cm. The field was sprinkler-irrigated according to evapotranspiration estimates from the High Plains Climate Center (www.hpccsun.unl.edu; verified 31 Jan. 2005), and 120 kg N ha–1 were applied following soil analysis recommendations when the fourth leaf was completely expanded (V4, Ritchie et al., 1997).

Photosynthetic rate was measured (Model 6400, Li-Cor, Lincoln, NE, USA) on the mid-third in length of leaf 13 under ambient CO2 at weekly intervals during grain filling. Before the first reading, the leaf was equilibrated in the leaf chamber for 20 min at about 2000 µmol quanta m–2 s–1 using the built-in light source. Subsequently, light intensity was decreased gradually waiting 3 to 5 min before making a new measurement at the next desired light level. The chamber temperature was maintained stable across readings using the device controller. Additional details of this experiment are provided elsewhere (Moreno-Sotomayor et al., 2002).

The CERES-PR photosynthesis model does not consider the effect of water deficit or atmospheric evaporative demand on assimilation. Thus, simulated gross assimilation is expected to overestimate field measured values in some cases (Bunce, 2003). To compare model-simulated light response curves with the field measurements it was necessary to ascertain the impact of vapor pressure deficit on the simulated values. Boedhram (1998), using the same irrigated cultivar (P3394) planted the same year in a nearby field, calculated a correction factor to adjust leaf assimilation measurements in maize for effect of vapor pressure deficit above 1 kPa. When N was not limiting the correction factor (FVPD) was:

[1]
where VPD (kPa) is the vapor pressure deficit. The simulated gross assimilation was multiplied by FVPD to generate a VPD-corrected assimilation curve that was used as a reference to compare against measured values.

Daily Canopy Assimilation
Carbon dioxide fluxes measured above the canopy with the eddy correlation technique and estimated at the soil surface were used to test the model at the canopy level. Hybrid Pride K 127 was seeded on 24 May 1993 at Nepean, ON, Canada at a population density of 6.4 plants m–2 in rows separated 75 cm. Fertilizers (8.8 kg N ha–1, 35.2 kg P2O5 ha–1, 17.6 kg K2O ha–1) were incorporated before planting, and 123.3 kg N ha–1 were applied in bands after emergence.

Sensible heat and water and CO2 fluxes were measured hourly following the eddy correlation technique. An open-path fast-response sensor (Brach et al., 1981; Chahuneau et al., 1989) at 20 Hz frequency monitored fluctuations of water vapor and CO2. A sonic anemometer–thermometer (Model DAT-310, Kaijo Denki Ltd., Tokyo) measured changes in air temperature and vertical and horizontal wind speed. The eddy correlation instruments were located on a tower 3 m above the canopy. The tower was located 120 m from the east side of the field.

Soil respiration was measured weekly at 30 randomly selected sites in the field using a 3-L plexiglass chamber connected to a portable CO2 analyzer (Model LI-6200) (Rochette et al., 1997). Hourly fluxes of soil surface CO2 were estimated as a function of soil temperature at 7 cm depth from a regression equation derived from the weekly measures. Twenty plants were randomly sampled weekly to determine leaf area and aboveground biomass. Rochette et al. (1996) provided additional details of this experiment.

Seasonal Crop Growth
The ability of CERES-PR to simulate crop growth through the growing season was tested using several data sets from the literature covering a wide range of latitudes (45–21° N lat), and where water and N were not limiting. The experiments were conducted in Ontario (Rochette et al., 1996), Minnesota (Westgate et al., 1997), and Nebraska (Boedhram, 1998). In addition, we tested against three experiments conducted in Florida and Hawaii, which are distributed with the DSSAT 3.5 software (Hoogenboom et al., 1999).

To compare measured and simulated leaf area index (LAI) and aboveground biomass, we calculated the root mean square of the error (RMSE) as:

[2]
where Si and Oi are the simulated and observed values for LAI and biomass, respectively, and n is the number of observations.

Sensitivity Analysis
The stability of CERES-PR (Lizaso et al., 2005) and the overall impact of uncertain parameters were examined by varying the value of single parameters within a range of ±30%, and observing the relative change in aboveground biomass and grain yield. We studied the changes in the following parameters:

Parameters associated with the simulation of light capture:

Parameters associated with the simulation of C assimilation and respiration:

Parameters associated with temperature effects:


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
SUMMARY
 REFERENCES
 
Instantaneous Leaf Assimilation
Measurements of instantaneous leaf photosynthesis in irrigated and fertilized field-grown maize were compared with the CERES-PR simulated light response curves (Fig. 1). In 1995, Moreno-Sotomayor et al. (2002) evaluated leaf assimilation rates in the same portion of 13th leaf on tagged plants. Measurements used the built-in light source, starting near 2000 µmol m–2 s–1 and then continued at decreasing light intensity. The procedure was repeated on three dates during grain filling, which made it possible to evaluate the impact of leaf aging on assimilation.



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  		Fig. 1. Measured and simulated instantaneous leaf assimilation on leaf 13th of hybrid P3489 grown in Mead, NE, in 1995. Each data point is the average and standard error of three to five consecutive measurements. Corrections for vapor pressure deficit (VPD, broken line) above 1 kPa were obtained with a linear relationship developed by Boedhram (1998).

 
The photosynthesis module in CERES-PR does not include the effects of soil water deficit or atmospheric evaporative demand (Lizaso et al., 2005). After potential assimilation is calculated and converted into potential growth rate, the information is linked into the current CERES, which calculates the impact of water, or N stresses on daily growth. Light response curves simulated with CERES-PR for 13th leaf of hybrid P3489 overestimated instantaneous leaf assimilation on the three dates (Fig. 1). To explore how much of the deviation between simulated and measured values could be attributed to the unaccounted effect of vapor pressure deficit (VPD), we adjusted the simulated values obtained with CERES-PR using the linear correction developed by Boedhram (1998). The correction factor was calculated from data collected the same year (1995) on the same cultivar (P3489) grown in a neighboring field under management similar to that of Moreno-Sotomayor et al. (2002). The correction factor (FVPD) assumes that leaf assimilation is not affected at VPD values of 1 kPa or less (FVPD = 1). At VPD values >1 kPa, leaf assimilation decreases linearly with VPD according to Eq. [1]. The corrected values for DOY 224, 231, and 237 are shown as dashed lines in Fig. 1. The close correspondence between the measured and corrected values on Days 231 and 237 implies that VPD had a substantial impact on leaf assimilation, as estimated by CERES-PR, on these 2 d. The VPD-corrected values for assimilation on DOY 224, however, were substantially lower than the measured values. The reason for the apparent overcorrection for VPD on this date is not known, but several issues need to be considered. The VPD correction developed by Boedhram (1998) assumes a linear relationship between leaf CO2 assimilation and VPD. Evidence presented by Kiniry et al. (1998) and Bunce (2003) supports this relationship. Sinclair and Muchow (1999), however, questioned the validity of this relationship and concluded there is likely to be no response of leaf assimilation in maize until VPD reaches values well above 2.5 to 3.0 kPa. Pettigrew et al. (1990) reported that adequate irrigation avoids the stomatal closure typically associated with high VPD. Table 1 shows that soil moisture was much more favorable before the photosynthesis measurements on Day 224 (Fig. 1) compared with Days 231 and 237. The difference in stomatal response to VPD on these dates is evident as transpiration rate on Day 224 was three times higher than on Days 231 and 237 at the beginning of the measurements (Fig. 2, PPFD around 2000 µmol m–2 s–1). These results indicate that leaf assimilation exhibits an integrated response to the three components of canopy water balance: the evaporative demand, the available soil water supply, and the ability of the plants to extract soil moisture and maintain transpiration flux in response to atmospheric demand. Thus, a simple correction for leaf assimilation by one of the components of the system (i.e., VPD) may be insufficient to simulate leaf assimilation accurately under some field conditions. Therefore, our future efforts will focus on developing a complete stomatal conductance model that integrates soil moisture supply, evaporative demand for water, and the concurrent effects of light and CO2.


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  		Table 1. Cumulative amount of water (mm) received by the crop as rainfall or irrigation in the previous days before photosynthesis measurement in the study of Moreno-Sotomayor et al. (2002).

 


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  		Fig. 2. Relationship between transpiration rate and photosynthetic photon flux density for the field measurements depicted in Fig. 1 (Moreno-Sotomayor et al., 2002).

 
Daily Canopy Assimilation
The daily progression of net photosynthetic rates simulated with CERES-PR was compared with field measurements obtained in Ontario, Canada, using the eddy correlation technique (Rochette et al., 1996). The daily input of solar radiation was used to estimate the incident PAR and the daily value was partitioned into hourly segments following a sinusoidal function. Figure 3 shows the sinusoidal simulation of canopy intercepted PAR and the corresponding net CO2 assimilation for five dates, as the crop approached maximum leaf area (DOY 220). There was close agreement with the measured intercepted light (RMSE 0.11–0.24) and the concomitant net assimilation (RMSE 0.18–0.44). Inaccuracies of the simulated intercepted PAR or canopy net photosynthesis largely reflected uncertainties associated with the hourly fractioning of daily solar radiation. Simulated canopy net photosynthesis more closely followed intercepted PAR when hourly PAR measured in the field was used as input (Fig. 4). These simulations obtained without modifications of the model were in very close agreement with measured IPAR and photosynthesis data, as indicated by average reductions in RMSE of 62% for IPAR and 19% for net photosynthesis.



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  		Fig. 3. Daily progression of measured and simulated intercepted photosynthetically active radiation and canopy net assimilation of hybrid Pride K 127 grown in Nepean, ON, in 1993. Simulations used daily inputs of solar radiation that the model converts in hourly values of PAR following a sinusoidal function.

 


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  		Fig. 4. Daily progression of measured and simulated intercepted photosynthetically active radiation and canopy net assimilation of hybrid Pride K 127 grown in Nepean, ON, in 1993. Simulations used on-site measured hourly PAR values.

 
Seasonal Crop Growth
CERES-PR also was tested by comparing seasonal growth simulation with LAI and aboveground biomass. These evaluations included various hybrids and environmental conditions in experiments where water and N stress were minimized. The locations ranged in latitude from Ontario at 45° N to Hawaii at 21° N. Figure 5 shows that the new leaf area model (Lizaso et al., 2003a) implemented in CERES-PR accurately simulated leaf area, particularly around flowering when the canopy exhibits maximum growth. Shoot dry matter accumulation also was accurately simulated, except for the experiment in Ontario, where biomass was slightly underpredicted during grain filling. The leaf area and biomass simulations depicted in Fig. 5 are determined not only by the new photosynthesis and respiration model, but also by the partitioning rules in the current CERES-Maize. These partitioning rules were based on the RUE approach and may need to be examined.



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  		Fig. 5. Seasonal progression of measured and simulated leaf area index and shoot biomass of six hybrids planted within a latitudinal range of 45 to 21° N.

 
Sensitivity Analysis
The stability of CERES-PR was tested under conditions where water or N were not limiting growth. We evaluated the relative responses simulated in final aboveground biomass and grain yield as the value of individual model parameters were changed within the range of ±30%. The overall growth simulation exhibited very little variation when parameters associated with the calculation of photosynthesis and respiration were changed (Fig. 6, open symbols). These parameters included rp and rg used to calculate maintenance respiration, and ka used to estimate the effect of leaf age on leaf assimilation. In CERES-PR, the lifespan of each leaf is calculated in the leaf area module, and changes in the parameters of the leaf assimilation response to age within 20% have almost no effect on simulated growth and yield. When parameter ka was reduced 30%, final biomass decreased 1% and grain yield 2%. These results indicated stable photosynthesis and respiration modules.



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  		Fig. 6. Sensitivity analysis of CERES-PR to relative changes in model parameters associated with light capture (closed symbols), photosynthesis and respiration (open symbols), and temperature (gray symbols). Parameters reported are as follows: {delta} (average leaf angle); H (potential canopy height); X (parameter dictating leaf angle distribution according to Campbell, 1986); rp (hourly maintenance respiration per unit of gross assimilation); rg (hourly maintenance respiration per unit of dry weight growth); ka (slope parameter dictating reduction of leaf assimilation with age); ast (temperature effect on light saturated assimilation, Asat); and rmt (temperature effect on maintenance respiration).

 
Changes in parameters associated with the calculation of light capture (closed symbols) also had limited effect on the simulated final biomass and yield. It has been widely recognized that leaf-angle distribution has a limited effect on light extinction and photosynthesis (e.g., Campbell, 1986; Goudriaan, 1988). The lack of response to changes in the X parameter supports this concept.

The only exception was parameter {delta}. Parameter {delta}, average leaf angle of expanded or almost fully expanded leaves (>80% of final leaf size) is used to calculate growth of canopy width. Increasing {delta} simulates more erect leaves and canopy width will increase more slowly. Since leaf growth in maize terminates at silking, a high value of {delta} will simulate a canopy that never closes, and thus fraction of absorbed PAR will remain relatively low throughout the season, thereby reducing the simulated seasonal biomass.

Temperature effects on assimilation and maintenance respiration are simulated in CERES-PR using polynomial functions. The response of the light saturated assimilation parameter (Asat) and maintenance respiration was varied over a range of ± 30% to examine the relative growth responses to temperature. CERES-PR was most sensitive to changes in the assimilation response to temperature (ast, Fig. 6). A reduction of 30% in the overall temperature function resulted in a 6.5% reduction in biomass and 12.5% reduction in yield.

Growth respiration is calculated in CERES-PR following Penning de Vries and colleagues approach (Penning de Vries and van Laar, 1982; Penning de Vries et al., 1989). The procedure calculates a respiratory cost associated with the transport and biosynthesis of various components. Table 2 shows the maize organ composition used in CERES-PR for the purpose of calculating growth respiration. In CERES-PR, we maintain the composition of each organ constant through the growing season. Although this may be an acceptable assumption for an initial approximation, future model improvements should consider changes in plant composition with crop phenology.


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  		Table 2. Maize plant composition used to calculate growth respiration in CERES-PR according to Penning de Vries and van Laar (1982).

 

   SUMMARY
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUMMARY
REFERENCES
 
We have developed and tested CERES-PR, a new version of CERES-Maize, which explicitly simulates leaf photosynthesis and respiration. Instantaneous leaf assimilation is calculated in hourly steps for each leaf and integrated over the whole canopy and daylight hours. Leaf assimilation is computed as a function of light intensity, air temperature, and leaf age. Canopy daily maintenance and growth respiration are simulated and subtracted from daily gross assimilation to estimate potential daily growth rate.

Researchers and scientists around the world use CERES-Maize. In many locations, and particularly in developing countries, availability of detailed model inputs limits adoption of crop simulation models (Matthews and Stephens, 2002). CERES-PR conforms to the standards of DSSAT suite of models, thus requiring only a minimum set of daily weather inputs (solar radiation, maximum and minimum temperature, and rainfall). This restriction should greatly improve CERES-PR applicability among the DSSAT community and current and future CERES-Maize users.

We examined CERES-PR performance at three levels of integration: (i) instantaneous leaf assimilation, (ii) hourly canopy assimilation, and (iii) seasonal growth. This multi-level evaluation used independent field measurements under conditions where water and N were not limiting plant growth. Values simulated by CERES-PR consistently exhibited close agreement with measured values. Sensitivity analysis revealed that the simulated canopy growth is very responsive to the temperature function affecting leaf assimilation. Therefore, special attention should be devoted to the accurate simulation of leaf temperature.

CERES-PR does not simulate leaf-level fluxes of water vapor and CO2. Our next task will be to develop and incorporate a formal stomatal conductance and energy balance model that provides the opportunity to simulate fluxes of CO2 and water vapor in and out of the leaf. The current calculations of assimilation will be complemented with transpiration and thus, extended into stress conditions and elevated CO2. With these linked components, the model will utilize the fundamental mass balances of C, water, and N to update partitioning of dry matter at each growth stage.


   ACKNOWLEDGMENTS
 
This research was supported by the Biological and Environmental Research Program (BER), U.S. Department of Energy, through the Great Plains Regional Center of the National Institute for Global Environmental Change (NIGEC) under Cooperative Agreement no. DE-FC03-90ER61010.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUMMARY
 REFERENCES
 




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J. I. Lizaso, W. D. Batchelor, K. J. Boote, and M. E. Westgate
Development of a Leaf-Level Canopy Assimilation Model for CERES-Maize
Agron. J., April 27, 2005; 97(3): 722 - 733.
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