Effects of nitrogen nutrition on responses of rice seedlings to carbon dioxide

Agriculture, Ecosystems and Environment 72 (1999) 1±8

Effects of nitrogen nutrition on responses of rice seedlings to carbon dioxide Weerakoon M. Weerakoona, David M. Olszykb,*, Dale N. Mossc a Rice Research Institute, Department of Agriculture, Batalagoda, Sri Lanka United States Environmental Protection Agency, National Health and Environmental Effects Research Laboratory, Western Ecology Division, Corvallis, OR 97333, USA c Department of Crop and Soil Sciences, Oregon State University, Corvallis, OR 97331, USA

b

Received 9 December 1997; accepted 30 July 1998

Abstract Global atmospheric CO2 concentration is increasing, likely increasing the productivity of crops as higher CO2 enhances plant photosynthesis. Responsiveness to nitrogen supply is an essential trait of modern rice cultivars, and may play a role in the response of rice cultivars to CO2. To determine the relationship between these two important production variables on young rice plants, seedlings of Oryza sativa L. `IR72' and `KDML 105' were exposed for 28 days after sowing to CO2 levels of 373, 545, 723 and 895 mmol molÿ1, and 3 levels of nitrogen fertility. There were large increases in leaf CO2 assimilation and biomass production whereas leaf nitrogen concentration dropped sharply as CO2 increased from 373 to 545 mmol molÿ1, with little additional effect from higher levels of CO2. Root and shoot biomass, and tiller number per plant increased with increasing nitrogen supply and with increasing atmospheric CO2 concentration. The biomass response to CO2 was slight at low N supply, but became dramatically greater as the N supply increased. Mean root/shoot ratio increased slightly as atmospheric CO2 concentration increased, but decreased sharply as nitrogen fertility rate increased. These results suggest that careful attention to nitrogen fertilization will be necessary for rice farming to get the full bene®t of any future increases in atmospheric CO2. # 1999 Published by Elsevier Science B.V. All rights reserved. Keywords: Oryza sativa L.; Biomass; Carbon dioxide; Nitrogen; Photosynthesis; Rice

1. Introduction Global atmospheric carbon dioxide (CO2) concentration at the Mauna Loa Observatory increased from 315 mmol molÿ1 in 1959 to >355 mmol molÿ1 in the mid 1990s (Keeling and Whorf, 1992; Keeling et al., 1995) and is projected to reach 700 mmol molÿ1 dur*Corresponding author. Tel.: +1-541-754-4397; fax: +1-541754-4799; e-mail: [email protected]

ing the mid 21st century (Conway et al., 1988). As atmospheric CO2 increases, the productivity of many crops, including rice (Oryza sativa L.), may increase (Kimball, 1983; Imai et al., 1985; Cure and Acock, 1986; Baker et al., 1990b; Ziska et al., 1996). A primary direct effect of higher atmospheric CO2 on plants is increased net photosynthesis (Atkinson, 1996). In rice, the increased photosynthetic rate with elevated CO2 results in increased biomass and yield (Baker et al., 1990a, b; Seneweera et al., 1996; Ziska

0167-8809/99/$ ± see front matter # 1999 Published by Elsevier Science B.V. All rights reserved. PII: S0167-8809(98)00166-2

2

W.M. Weerakoon et al. / Agriculture, Ecosystems and Environment 72 (1999) 1±8

et al., 1996, 1997). However, the productivity of modern rice cultivars also depends on their responsiveness to soil nitrogen (N) supply. Excess vegetative growth in rice tends to dilute the leaf N concentration which, in turn, reduces light saturated CO2 assimilation because of the heavy demand for N in growing leaves to produce ribulose bisphosphate carboxylate (Dingkuhn et al., 1992). Therefore, an increase in biomass production in rice seedlings from higher atmospheric CO2 concentration may act as a sink for N and could lead to a decreased leaf N concentration in newly formed leaves if insuf®cient N fertilizer has been applied. Conversely, insuf®cient N fertilizer could inhibit the potential increase in biomass with elevated CO2. Because of the heavy demand for N as a structural component of the photosynthetic apparatus in growing leaves, the interaction of CO2 and plant N content may differ during the vegetative stage, when new leaves are being produced, and the grain ®lling stage, when new leaves are not being produced. Thus, the relationship between important production variables: atmospheric CO2 and N nutrition, were determined on rice seedlings. The hypotheses tested in this paper were that plants growing at low N fertility would be less responsive to elevated CO2, and that plants growing under elevated CO2 would have decreased leaf N concentrations. The study determined the effect of multiple levels of both CO2 and N fertilizer on growth and dry matter partitioning of two rice cultivars during seedling vegetative growth, and the effect of leaf N concentration on leaf C assimilation (A) at different CO2 concentrations in vegetative rice plants. 2. Materials and methods Two 28-day experiments were conducted sequentially inside a glasshouse during June±September, 1992 at the U.S. Environmental Protection Agency's facility in Corvallis, OR, USA. Seeds of `IR72' and `KDML105' rice were soaked in tap water for 36 h and allowed to germinate on moist ®lter paper for two days. Four germinating seeds were planted in each 6.4 cm diameter, 25 cm tall plastic containers ®lled with a silt loam soil. Twenty-seven containers of each cultivar were placed in each of eight exposure cham-

bers (1.06 m length  0.76 m width  0.97 m height), constructed of wood frames covered with transparent Te¯on ®lm (FEP, 2  10ÿ3 thick, E.I. Dupont, Wilmington, DL). Soil moisture was maintained at ®eld capacity for three days during seedling establishment. Thereafter, plants were grown under a ¯ooded condition, using North Carolina State University phytotron nutrient solution in reverse osmosis water (pH  6.4), but excluding N. An NH4NO3 fertilizer was applied ®ve days after sowing (DAS) directly to the plant containers at 12.3 mg (N12), 24.5 mg (N24) or 36.5 mg (N36) of N per container. Seedlings were thinned to one plant per container at 4 days-after-sowing (DAS). Each nitrogen treatment was applied to nine containers per cultivar in each exposure chamber. Beginning 2 DAS, CO2 was injected into the exposure chambers using mass ¯ow controllers (Model 825, Edwards High Vacuum International, Wilmington, MA). Chamber CO2 concentrations were monitored with infra-red gas analyzers (Model 6251, Lambda Inst., Lincoln, NE), linked to a sequential sampling system (Model SAMS 6±12, Scanivalve, San Diego, CA) and an HP3052A data acquisition system, equipped with an HP9816 computer, which maintained average CO2 concentrations of 373 (ambient), 545, 723 and 895 mmol molÿ1 (coef®cient of variability is 1% across CO2 levels, chamber and experiments) in the individual treatments. Each CO2 treatment was replicated in two chambers in each experiment. Air temperatures in the exposure chambers depended on greenhouse air temperature, which, although controlled to a set point, nevertheless varied somewhat, depending on conditions outside the glasshouse. Air temperature in the exposure chambers were monitored continuously using thermistors (Model ON 405-PP, Omega Engineering, Stamford, CT) located in the exit air stream of each chamber. Average daily maximum and minimum temperatures were 35.4 and 26.38C. However, mid-day maximum temperatures reached 388C on 17 and 22 DAS in the ®rst experiment and on 6, 11 and 16 DAS in the second experiment. Relative humidity (RH) inside the exposure chambers was not controlled and varied with air temperature. The RH in the exit air streams of two chambers was monitored continuously using thin-®lm capacitance sensors (Model HMP-23U, Vaisala, Woburn,

W.M. Weerakoon et al. / Agriculture, Ecosystems and Environment 72 (1999) 1±8

MA, calibrated with a Model HMK 11 calibrator). The RH varied between 40 and 50% during the ®rst ten days when the plants were small; it increased to 65± 75% as the plants grew. Photosynthetically active radiation (PAR) was monitored continuously inside two exposure chambers using quantum sensors (Model 190SB, Lambda Instrument, Lincoln, NE). Between 0600 and 1200 daily the solar radiation was supplemented with 1000 W high intensity discharge lamps (GE LUCALUX). The average maximum mid-day PAR inside the exposure chambers was about 800 mmol mÿ2 sÿ1. Three plants per cultivar and N treatment combination were sampled destructively from each treatment on 14, 21 and 28 DAS. Leaf number and tiller number per plant were counted on the samples and leaf area using a leaf area meter (Model LI 3100, Lambda Inst., Lincoln, NE) was measured. Leaf dry weight, sheath and culm dry weight, and root dry weight for each plant were measured after drying for 72 h at 708C. For cultivar IR 72, the leaf blade C and N contents were determined on a composite sample of the dried leaf green blades from each treatment from 21 and 28 DAS, using an elemental analyzer (Carlo Erba CHINSO, model EA1108, Milan, Italy). Single leaf CO2 assimilation(A) was measured at the CO2 concentration on cloudless days using a portable, closed, gas exchange system (Model 6200, Lambda Instrument, Lincoln, NE) with a 250 ml cuvette. When a leaf was inserted into the cuvette, the CO2 concentration in the cuvette was adjusted to slightly above the set-point concentration of the chamber in which the plants were growing. Then, each leaf was allowed to acclimatize for about 20±30 s inside the cuvette and the measurement was taken when the cuvette CO2 concentration had decreased to the growth CO2 concentration. The system was calibrated before each series of gas exchange measurements using CO2 free air and a standard gas containing 950.1 mmol molÿ1 CO2. The cuvette gaskets and the system was checked for general leaks for each set of measurements. Blanks (chamber but no leaf) were not run, so it was not possible to determine speci®cally if there were any unaccounted leaks in the system that might have affected the rates. During leaf A measurements light was supplied by a 250 W HID lamp at an intensity of about 900 mmol mÿ2 sÿ1 (PAR). Thus, the leaves were near

3

light saturation and the assimilation data approximate the maximum photosynthetic capacity of the leaves in the CO2 concentration at which they were grown. Because humidity and air temperature inside the leaf chamber were not controlled, leaf A values measured with lower PAR, below 800 mmol mÿ2 sÿ1, higher leaf temperature, above 328C, and relative humidity of below 60% were removed from analysis. The A was measured at 3 days before the ®nal harvest, using the youngest most-fully-developed leaf of the main culm. Leaf area was calculated as average leaf width  3.5 cm cuvette width. Because of the time required to make replicated measurements of A in all of the different N and CO2 combinations, measurements were made only on cultivar IR 72. Statistical analysis were conducted using CO2 as the main factor, with cultivars and N as subfactors in a split-split plot design. There were no signi®cant differences in response between the two experiments or between the two cultivars. Therefore, for analysis of biomass production, and of nitrogen and carbon partitioning, the data of the two experiments and two cultivars were combined. Analysis of variance (ANOVA) was performed using STATGRAPHICS statistical graphics system. Mean comparisons were made using Duncan's Multiple Range Test at p < 0.05. Data were analyzed separately for each of the three sampling dates. The data for 14 DAS are not included here because none of the plant morphological or biomass variables were signi®cantly different among treatments. 3. Results and discussion The A rates, averaged across CO2 concentrations, increased incrementally and signi®cantly as the nitrogen fertility rate increased. Average A rates were 22.0, 28.2 and 31.5 mmol CO2 mÿ2 leaf sÿ1 in the N12, N24 and N36 treatments, respectively. The A rates averaged over nitrogen treatments increased 50% with a relatively small elevation in atmospheric CO2 concentration, from 20.4 mmol mÿ2 sÿ1 at 373 mmol molÿ1 to 30.0 mmol mÿ2 sÿ1 at 545 mmol molÿ1. There were no further signi®cant increases in A rates with exposure to still higher atmospheric concentrations of 723 and 895 mmol molÿ1 CO2. Overall, the A rates in this paper are similar in magnitude and pattern of response to CO2

4

W.M. Weerakoon et al. / Agriculture, Ecosystems and Environment 72 (1999) 1±8

to those reported by others for rice (i.e. Baker et al., 1990b; Ziska and Teramura, 1992; Ziska et al., 1996). Thus, the data are useful, especially to evaluate response at different nitrogen levels across CO2 concentrations, even though leaks were possible in the system. It is not readily apparent why A in rice seedlings should be nearly saturated at the 723 and 895 mmol molÿ1 CO2 concentrations, as reports of A rates for many other crops show a continuing response to CO2 concentrations, often to well beyond 1000 mmol molÿ1 (Kimball, 1983). Dilution of leaf nitrogen with the higher elevated CO2 in these experiments may play a role in the lower A rates. In Fig. 1., A of IR 72 rice leaves decreased with decreased leaf nitrogen as reported previously by Sinclair and Horie (1989), especially at higher CO2 concentrations. Fig. 2 clearly shows that, as the CO2 concentration increased, the nitrogen concentration, and, hence,

Fig. 1. The mid-day CO2 assimilation (A) at 25±28 days after sowing of the uppermost, fully-expanded leaves of rice plants as a function of the leaf nitrogen (N) content. Symbols are the CO2 concentrations during growth for individual plants. The assimilation measurements were made using the same CO2 concentration in the measurement cuvette as the concentration at which the plants were grown. Leaf N at zero assimilation was from Dingkuhn et al. (1992). Light intensity at the time of measurement was about 1250 mmol PAR mÿ2 sÿ1. The lower curve is an approximate relationship between A and leaf N for ambient (373 mmol moleÿ1) CO2 , and the upper curve an approximate relationship between A and leaf N is for elevated (545, 723, 895 mmol molÿ1) CO2

Fig. 2. Leaf blade nitrogen (N) concentration for IR 72 rice at 28 days after sowing as a function of the growth CO2 concentration for the three rates of N fertilizer application. Each symbol is the mean of 12 values [two experiments  two blocks (of chambers) per experiment  three plants].

capacity for A, decreased. Decreased partitioning of N to leaves when grown at high CO2 (Weerakoon, 1994), could decrease leaf protein complexes, thus decreased RUBP carboxylase activity could affect leaf assimilation. Elevated CO2 affected other plant responses. By 21 DAS, total plant dry weight was 50% greater at 545 compared with 373 mmol molÿ1 CO2 (Table 1). There were no signi®cant differences in total plant dry weight between 545 mmol molÿ1 and higher CO2 concentrations, nor any signi®cant interaction between atmospheric CO2 and N on total dry weight. By 28 DAS, there was an interaction between atmospheric CO2 and N fertility level on total dry weight (Fig. 3). In a N-limited environment (N12), the change in total dry weight in response to increasing CO2 was small. However, total dry weights were 20% greater in the N24 and 45% in the N36 treatments with 895 compared with 373 mmol molÿ1 CO2. The greatest response to increasing CO2 (across N levels) occurred between 373 and 545 mmol molÿ1 CO2 (Fig. 3). Biomass partitioning among plant organs was affected by atmospheric CO2 concentration and soil N. Table 1 shows effects of the single factors, CO2 or N, on organ dry weights at 21 DAS. At 545 compared

W.M. Weerakoon et al. / Agriculture, Ecosystems and Environment 72 (1999) 1±8

5

Table 1 Total plant and organ dry weights (g plantÿ1), root/shoot ratios, and leaf blade nitrogen concentration of rice seedlings grown at different CO2 concentrations and different rates of nitrogen fertilizer (see text), and measured at 21 days after sowing Parameter

CO2 (mmol molÿ1)a 373

Total plant dry weight Root dry weight Leaf sheath and culm dry weight Leaf blade dry weight Root/shoot ratio Leaf nitrogen (%)

0.54 0.09 0.19 0.26 0.20 4.24

Nitrogen fertilizerb

545 a a a a a a

0.81 0.18 0.29 0.34 0.27 3.77

723 b b b b a b

0.79 0.18 0.29 0.32 0.29 3.61

895 b b b b a b

0.81 0.18 0.30 0.33 0.28 3.63

N12 b b b b a b

0.66 0.18 0.23 0.25 0.37 2.84

N24 a a a a a a

0.79 0.16 0.29 0.34 0.25 3.89

N36 b b b b b a

0.75 0.12 0.28 0.35 0.19 4.71

b b b b c c

a

Means across nitrogen fertilization treatments based on 24 values [two experiments  two blocks (of chambers)/experiment  (two cultivars  three N levels/chamber)]. Data from three plants were pooled for each variety  N level value. b Means across CO2 treatments based on 32 values (two experiments  two blocks (of chambers) per experiment  four CO2 levels per experiment  two cultivars per chamber). Data from three plants were pooled for each cultivar value. In a row, means followed by different letters are significantly different at p < 0.05 according to Duncan's multiple range test.

Fig. 3. Rice seedling shoot dry weights at 28 days after sowing for the three nitrogen fertility treatments at each of the four growth CO2 concentrations. Each symbol is the mean of 24 values [two experiments  two blocks (of chambers) per experiment  two cultivars per chamber  three plants per cultivar].

with 373 mmol molÿ1 CO2, dry weights of leaves, leaf sheaths and culms, and roots were 25, 55 and 100% greater, respectively. There were no differences in organ dry weights between 545 mmol molÿ1 and higher CO2 concentrations. In the carbon limited treatment (373 mmol molÿ1 CO2) the carbon likely was preferentially ®xed near its source in the shoots,

the roots were small, and the root/shoot biomass ratio (root dry weight/leaf blade ‡ sheath and culm dry weights) was only 0.20. As the assimilate supply increased (higher CO2 treatments) the root/shoot ratio increased because additional carbon was available to the roots. Mean dry weights of leaves and of sheaths and culms also were greater at N24 compared with N12, but there were no differences in mean weights of those organs between N24 and N36. In contrast, root dry weights and the root/shoot ratio were progressively smaller as the N supply increased. By 28 DAS, dry weights of all plant organs were appreciably greater than at 21 DAS (Table 2). The effect of atmospheric CO2 was more pronounced on root weights than on the weights of other plant organs. At 373 mmol molÿ1 CO2, the rate of N fertility had no signi®cant effect on root dry weight in that carbon limited environment. However, in the carbon limited environment the root/shoot ratio decreased sharply as the nitrogen supply increased, from 0.54 at N12 to 0.30 at N36 treatments. At all the higher CO2 concentrations root dry weights were greater than in the ambient CO2, resulting in mean root/shoot ratios (averaged over nitrogen treatments), of 0.62, 0.52, and 0.47 in the 545, 745, and 895 mmol molÿ1 CO2 concentrations, respectively. Thus, although the greater carbon supply led to larger root systems, the data clearly show the preferential partitioning of carbon to the shoots as the plant nitrogen supply increased. These results are consistent with previous observations that there is a

6

W.M. Weerakoon et al. / Agriculture, Ecosystems and Environment 72 (1999) 1±8

Table 2 Organ dry weights (g plantÿ1) for rice plants grown at different CO2 concentrations and different rates of nitrogen fertilizer (see text), and measured at 28 days after sowing. Means followed by different letters are significantly different at p < 0.05 according to Duncan's multiple range test. Each mean for an individual CO2  N combination is for 24 values [two experiments  two blocks (of chambers) per experiment  two cultivar per chamber  three plants per cultivar] CO2 (mmol molÿ1)

Leaf blade N24

N12 373 545 745 895 Nitrogen means

0.33 0.34 0.34 0.34 0.33

Sheath and culm

a a a a a

0.54 0.57 0.56 0.56 0.56

N36 a a a a b

0.65 0.75 0.75 0.75 0.73

N12 a b b b c

0.43 0.46 0.53 0.54 0.49

Root

N24 a a a a a

0.62 0.73 0.85 0.90 0.78

N36 a ab d d b

N12

0.67 0.96 1.19 1.13 0.99

a b c c c

0.41 0.49 0.54 0.56 0.49

N24 a b b b a

0.48 0.67 0.70 0.76 0.65

N36 a b cb c b

0.40 0.74 0.73 0.84 0.68

a b b c c

leaf N and lack of a large increase in A for rice leaves at 723 and 895 mmol molÿ1 CO2. Tillering is strongly affected by N supply in all cereal crops, including rice (Yoshida, 1981). By 21 DAS, there were 45% more tillers produced at N24 and 55% more at N36 treatments, compared with N12 (Table 3). However, tiller development also is affected by A rate, and tiller number per plant increased with increased atmospheric CO2 concentration from 373 to 545 mmol molÿ1 CO2, but not with further increases to 723 and 895 mmol molÿ1CO2. The fact that there were no more tillers formed in the 723 and 895 mmol molÿ1 CO2 concentrations, compared with the 545 mmol molÿ1 concentration, could have been the result of deposition of carbon and nitrogen into tillers already formed, leaving the plants unable to respond to the still higher CO2 concentrations. The nitrogen supply interaction with

greater increase in root weight than other plant parts, and an increase in root/shoot ratio as CO2 concentrations increase (Imai et al., 1985; Baker et al., 1990a; Curtis et al., 1990; Christian and John, 1992; Olszyk et al., 1993). Baker et al. (1990b) also found that roots grew faster and penetrated deeper into the soil at high CO2 concentrations. Lamina dry weight did not increase with increased CO2 at N12 and increased only slightly at the higher N levels (Table 2). In contrast, the sheath ‡ culm weight increased greatly with elevated CO2 at the higher N levels. The increase in the sheath and culm dry weights primarily was from enhanced tillering with increased N supply. The growth of sheath and culm competes with leaf blades for N, but sheath and culm tissues are only slightly photosynthetically active. Thus, the relatively greater increase in sheath and culm weights with elevated CO2 appeared to contribute to the dilution of

Table 3 Tiller number per plant of rice grown at different CO2 concentrations and different rates of nitrogen (N) fertilizer (see text), and measured at 21 and 28 days after sowing (DAS) CO2 (mmol molÿ1)

21 DAS N12

21 DAS N24

21 DAS N36

28 DAS Mean all N

373 545 723 895 Nitrogen across CO2

2.7 3.0 3.3 3.5 3.1

3.4 4.7 4.9 4.8 4.5

3.5 5.1 4.9 5.4 4.8

4.2 5.1 4.9 5.0 4.8

a ab ab b a

a b b b b

a b b b b

a b b b

In a column (at different CO2 concentrations) and bottom row (main N effects across CO2 concentrations for 21 DAS), means followed by different letters are significantly different at p < 0.05 according to Duncan's multiple range test. Each mean for an individual CO2  N combination at 21 DAS is for eight values [two experiments  two blocks (chambers) per experiment  two cultivars per chamber], with data from three plants pooled for each cultivar. Each mean for a CO2 level across all N levels at 28 DAS is for 24 values [two experiments  two blocks (chambers) per experiment  (six cultivars and N levels per chamber)], with data from three plants pooled for each cultivar.

W.M. Weerakoon et al. / Agriculture, Ecosystems and Environment 72 (1999) 1±8

CO2 concentration also was apparent in the tillering patterns. There was no signi®cant increase in tiller number with increased CO2 concentration in the N12 treatments, but in the N24 and N36 treatments the tiller number increased by 39% and 46% when CO2 concentration was increased from 373 to 545 mmol molÿ1. Yoshida (1981) showed that tillering in rice increased linearly with the increases in plant nitrogen content up to 5%. Increased tiller number with increased CO2 concentration con®rms results of studies by Baker et al. (1990a) and Imai et al. (1985). In conclusion, these experiments showed that atmospheric CO2 concentration and plant nitrogen supply interact to affect rice. These results were for young rice plants grown under glasshouse conditions, and, thus, may not have direct applicability in terms of grain development and yield responses in the ®eld. However, the validity of these results was reinforced by related studies conducted in the ®eld also using cultivar IR 72 and three levels of nitrogen fertility, but only ambient and a high (700 mmol molÿ1) concentration of CO2 (Ziska et al., 1996). Those ®eld studies also showed that the photosynthetic and growth response of rice to elevated CO2 is limited by inadequate nitrogen fertilization. Acknowledgements This paper number is 10762 in the Oregon State University Agricultural Experiment Station technical paper series. These experiments were part of a study submitted by the senior author in partial ful®llment of the requirements for a Ph.D. degree at Oregon State University, Corvallis, OR. The information in this document has been funded in part by the U.S. Environmental Protection Agency (US EPA) under cooperative agreement number 817426 to the International Rice Research Institute, Los BanÄos, the Philippines (IRRI). It has been subject to the agency's peer and administrative review, and has been approved for publication as an EPA document. The authors thank the anonymous references and an Editor-in-Chief for improvements to an earlier version of this paper. Mention of trade names or commercial products does not constitute endorsement or recommendation for use.

7

References Atkinson, C.J., 1996. Global changes in atmospheric carbon dioxide: the influence on terrestrial vegetation. In: Yunus, M., M. Iqbal (Eds.), Plant Response to Air Pollution, Wiley, New York. 99±133. Baker, J.T., Allen, L.H. Jr., Boote, K.J., 1990a. Growth and yield responses of rice to carbon dioxide concentration. J. Agric. Sci. Cambridge 115, 313±320. Baker, J.T., Allen, L.H. Jr., Boote, K.J., Jones, P., Jones, J.W., 1990b. Rice photosynthesis and evapotranspiration in subambient, and superambient carbon dioxide concentrations. Agron. J. 82, 834±840. Christian, K., John, A.A., 1992. Responses to elevated carbon dioxide in artificial ecosystems. Science 257, 1672±1675. Conway, T.J., Trans, P., Waterman, L.S., Thoning, K.W., Masaric, K.S., Gammon, R.M., 1988. Atmospheric carbon dioxide measurements in the remote global troposphere 1981±1984. Tellus 40B, 81±115. Cure, J.D., Acock, B., 1986. Crop response to carbon dioxide doubling: a literature survey. Agric. For. Meteor. 38, 127±145. Curtis, P.S., Balduman, L.M., Drake, B.G., Whigham, D.F., 1990. Elevated atmospheric CO2 effects on below ground processes in C3 and C4 estuarine marsh communities. Ecology 71, 2001± 2006. Dingkuhn, M., De Datta, S.K., Javellana, C., Pamplona, R., Schnier, H.F., 1992. Effect of late season N fertilization on photosynthesis and yield of transplanted and direct-seeded tropical flooded rice. I. Growth dynamics. Field Crops Res. 8, 223±234. Imai, K., Coleman, D.F., Yanagisawa, T., 1985. Increase in atmospheric partial pressure of carbon dioxide and growth and yield of rice (Oryza sativa L.). Jpn. J. Crop Sci. 54, 413± 418. Keeling, C.D., Whorf, T.P., 1992. Atmospheric CO2±modern record, Mauna Loa. In: Thomas, A.B., Robet, J.S., Frederick, W.S. (Eds.), Trends '91±a compendium of data on global change; highlights. Carbon Dioxide Information Analysis Center, Environmental Science Division, Oak Ridge National Laboratory, Oak Ridge, TN, pp. 18±26. Keeling, C.D., Whorf, T.P., Wahlen, M., Van der Pflicht, J., 1995. Interannual extremes in the rate of rise of atmospheric carbon dioxide since 1980. Nature 375, 666±670. Kimball, B.A., 1983. Carbon dioxide and agricultural yield: assemblage and analysis of 430 prior observations. Agron. J. 75, 779±788. Olszyk, D., Wise, C., Weerakoon, W.M.W., 1993. Effect of CO2 and temperature on five rice cultivars. J. Agric. Meteor. 48, 787±790. Seneweera, S., Blakeney, A., Milham, P., Basra, A.S., Barlow, E.W.R., Conroy, J., 1996. Influence of rising atmospheric Co2 and phosphorus nutrition on the grain yield and quality of rice (Oryza sativa cv. Jarrah). Cereal Chem. 73, 239±243. Sinclair, T.R., Horie, T., 1989. Leaf nitrogen, photosynthesis, and crop radiation use efficiency: a review. Crop Sci. 29, 90±98. Weerakoon, W.M.W., 1994. The effects of enhanced atmospheric CO2 and N fertilization on growth and development of

8

W.M. Weerakoon et al. / Agriculture, Ecosystems and Environment 72 (1999) 1±8

rice (Oryza sativa L.). Ph.D. Thesis. Oregon State University. Yoshida, S., 1981. Fundamentals of Rice Crop Science. International Rice Research Institute, Manila. Ziska, L.H., Teramura, A.H., 1992. Intraspecific variation in the response of rice (Oryza sativa) to increased CO2±photosynthetic, biomass and reproductive characteristics. Phys. Plant. 84, 269±276.

Ziska, L.H., Weerakoon, W., Namuco, O.S., Pamplona, R., 1996. The influence of nitrogen on the elevated CO2 response of field-grown rice. Aust. J. Plant Physiol. 23, 45±52. Ziska, L.H., Namuco, O., Moya, T., Quilang, J., 1997. Growt and yield response of field-grown tropical rice to increasing carbon dioxide and air temperature. Agron. J. 89, 45±53.