effects of ozone on the light use of rice (oryza sativa l.) plants

E L S E V I E R Agriculture, Ecosystems and Environment 53 (1995) 1-12

Agriculture Ecosystems & Environment

Effects of ozone on the light use of rice ( Oryza sativa L.) plants

Kazuhiko Kobayashi a'*, Masumi Okada b aNational Institute of Agro-Environmental Sciences, 3-1-1 Kannondai, Tsukuba, Ibaraki 305, Japan

aTohoku National Agricultural Experiment Station, Akahira, Shimo.kuriyagawa. Morioka, lwate 020-01, Japan

Accepted 24 August 1994

Abstract

Effects of ozone on rice growth processes were addressed in terms of light use of plants exposed to ozone in field exposure chambers in experiments in 1987, 1988 and 1989. Incident, reflected and transmitted light fluxes were measured with light sensors set above and below the rice canopy in the exposure chambers. Light-use efficiency (LUE) was calculated from the total dry weight and the accumulated amount of light absorbed by the rice canopies. The results showed increase of light absorption with the increase of leaf area index (LAI) during the vegetative growth, but light absorption was almost constant after heading despite the decrease of LAI due to senescence. While no effects of ozone on light absorption were found, the LUE was decreased by ozone. A quadratic function was fitted to the relationship between mean ozone concentration and LUE during the vegetative growth, and a linear function was fitted to the relationship for the reproductive growth. The effect of ozone on LUE was much greater in the reproductive than in the vegetative stage. Some mechanisms were discussed with regard to the enhancement of the ozone impact on LUE in the reproductive stage.

Keywords: Ozone; O~. za sativa (rice); Light-use efficiency

1. Introduction

It has been well established that ozone depresses crop growth and yield. For rice (Oryza sativa L.), as reviewed in a previous paper (Kobayashi et al., 1995), many studies have shown reduction of growth and yield by ozone (e.g. Nakamura, 1979; Kats et al., 1985). Reduction of photosynthetic rate has been suggested as the primary cause of the rice growth depression (Nak- amura, 1979). However, other causes (e.g. leaf loss by ozone damage) might account for the growth reduction. Reduced leaf area index (LAI) has been identified as the major cause of decreased dry matter production of broad bean ( Viciafaba L.) exposed to SO2 ( Kropff, 1990). Major causes of the reduced growth and yield

* Corresponding author.

0167-8809/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved SSDIOI 67-8 8 0 9 ( 9 4 ) 0 0 5 6 0 - 5

(Kobayashi et al., 1995) could be identified by analysing the growth data.

As useful measures of crop performance, Monteith (1977) identified the amount of radiation intercepted by the plant canopy and the efficiency of use of the intercepted radiation for growth. Since then, there have been many studies based on these measures (Russel et al., 1989), although there are only two for the effect of ozone on crop plants.

Unsworth et al. (1984) studied effects of ozone on light use of soybean plants exposed to ozone in open- top chambers, and reported both reduced light-use efficiency and light interception. Leadley et al. (1990) found no effect of ozone on light interception of soybean exposed to ozone in open-top chambers but reduced.

2 K. Kobayashi, M. Okada/Agriculture, Ecosystems and Environment 53 (1995) 1-12

With respect to the light use of rice, there have been a number of studies (Murata et al., 1968; Hayashi, 1972; Kishida, 1973; Hirota et al., 1978; Yamagishi et al., 1980; Horie and Sakuratani, 1985). Nevertheless, none is available on changes in the light use of rice plants caused by air pollution.

The framework (i.e. intercepted or absorbed radiation and its use for growth) can very easily fit in a simple crop growth simulation model (Russel et al., 1989). With rice, Horie (1988) has developed a growth model on the basis of the absorbed light and the efficiency of its use. The effect of ozone on rice growth and yield (Kobayashi et al., 1995) could be modelled by analysing the light use of the rice plants.

The objectives of this study are twofold: (1) to address the effects of ozone on rice growth in terms of the effects on the light use of the crop plants; (2) to obtain the parameters for modelling the impact of ozone on rice growth processes.

The 'light-use efficiency' in this paper is defined as the ratio of dry matter increase to the amount of light absorbed by the crop canopy. This should be differen- tiated from the light-utilization efficiency (quantum efficiency), which is the initial slope of a curve for the light intensity/net photosynthetic rate (e.g. Acock, 1991 ). The light-use efficiency is abbreviated hereafter as LUE.

2. Materials and methods

Rice plants were grown in field exposure chambers (Kobayashi et al., 1994), and were exposed to ozone throughout most of the growing seasons in 1987, 1988 and 1989 (Kobayashi et al., 1995). The cultivar 'Koshi-hikari' was used for the experiments in 1987 and 1989, and the cultivar 'Nippon-bare' for the experiment in 1988. The plant culture was performed accord- ing to common agronomic practices. Plant samples were harvested on a regular basis to measure dry weight and leaf area.

Ozone concentration in the chambers was controlled to preassigned constant proportions to the ambient ozone level for the 7 h from 09:00 to 16:00 h Japanese Standard Time. The target proportions were 0.5 (A ×0.5) , 1.0 (AX 1.0), 1.5 (AX 1.5), 2.0 (A x2.0) and 2.75 (A × 2.75) (treatment names in parentheses). The actual ozone concentration was somewhat lower

than the target level for the vegetative stage in 1987 and 1988, when the ozone exposure began 15 days (1987) and 21 days (1988) after transplanting. This was not the case in 1989, when the ozone dispensing began immediately after transplanting. In the reproductive stage, the ozone concentration was close to the target level for all the three seasons (Kobayashi et al., 1995).

Incident, reflected and transmitted light fluxes in the rice canopies were measured throughout the ozone exposures. Since only a limited number of light sensors were available, the light measurement was performed in only four (1987) or three (1988) of the five chambers, but in all five chambers in 1989. For the incident light flux measurement in a chamber, three IKS-25 (Koito Kogyo, Takanawa, Minato-ku, Tokyo, Japan) sensors were set at approx. 0.4 m above the canopy for the 1987 and 1988 experiments, and only one sensor was used for the 1989 experiment. The light flux reflected by rice plants and paddy surface in a chamber was measured with a sensor set downward at approx. 0.4 m above the rice canopy for all the three years. The light transmitted through rice plants was measured below the canopy as follows. Six IKS-25 sensors were used to measure the transmitted light in 1987 and 1988. In 1989, the canopy light transmission was measured in the same way as in 1987 and 1988 in two out of the five chambers, but in the other chambers three IKS-25 sensors plus one IKS-225 bar sensor were used to measure the canopy light transmission. In an IKS-225 bar sensor, ten IKS-25 sensor-heads are arranged in a line. Incident light flux outside the chambers was measured with an IKS-25 sensor at an adjacent paddy field. All the sensors used in the light measurements had been calibrated with a transfer-standard IKS-25 sensor before the commencement of the measurements each year. The transfer-standard was calibrated with an LI- 190S quantum sensor (LI-COR, Lincoln, NE, USA), and was not used for any other measurements than the calibrations.

The light measurement was performed once per min- ute and averaged hourly. The hourly averages were summed up to the daily integral of light incident, reflected and transmitted by the canopy. On the calculation, outputs of the individual sensors were checked on an hourly basis and erroneous data were discarded.

The severe lodging in the 1987 experiment precluded the measurements of reflected and transmitted light 100

K. Kobayashi, M. Okada / Agriculture, Ecosystems and Environment 53 (1995) 1-12 3

35O

3OO

~o 250

~ '200

"~ 150

~ I00

~ so

0 3OO

the IKS-25 sensor response " ~ A

400 500 600 700 800 900 1000 11 O0 1200

Wave length (nm)

Fig. 1. Spectral response of the IKS-25 light sensor. Also shown is the spectral response of an 'ideal' sensor for photosynthesis active photon flux density.

days after transplanting (DAT) and thereafter. Severe lodging was prevented in the 1988 and 1989 experiments, but the rice plants had more or less leaned over by the final harvest. This might have affected somewhat the measurements of canopy light properties.

dent solar radiation is in the range 305-715 nm (Sak- uratani, 1986), the sensor may be used to measure incident photon flux density if calibrated against a standard photon sensor. However, spectral irradiance of solar radiation reflected or transmitted by a plant canopy could markedly differ from that of incident radiation. A rice canopy has shown a sharp distinction in reflectance and transmittance between the wave bands shorter and longer than 750 nm (Munakata and Shi- bayama, 1985). Because of the spectral response of the IKS-25 sensor in the range longer than 700 nm (Fig. 1 ), the canopy radiative properties measured with the light sensor could greatly deviate from those measured with an ideal PAR sensor.

Considering the spectral response of the sensor as noted above, the light flux density measured with the IKS-25 sensor was calibrated with the standard PAR sensor, LI-190S, and was expressed in mol s-~ cm -2 in the PAR range, i.e. 400-700 nm. The calibration should have minimized the error due to the spectral response in the incident PAR flux. However, much precaution is needed in comparing the canopy reflectance and transmittance from the light sensor with the results from other types of sensors.

2.1. The light sensor 2.2. Reflectance

The type IKS-25 light sensor was intended for meas- uringphotosynthetically active radiation (PAR) (400- 700 nm) on a quantum basis. However, the spectral response turned out to be deviating from the intended one, and canopy reflectance calculated from the sensor output could be an intermediate value between an ideal PAR sensor and an ideal pyranometer (K. Kobayashi, unpublished observations, 1991). The spectral response of the sensor is shown in Fig. 1. The response curve was calculated as the spectral transmittance of the sensor filter multiplied by the spectral response of the photodiode. The spectral transmittance of the filter was measured with a spectroradiometer (Opto- Research, Ogikubo, Tokyo, Japan) for each 10 nm interval. The specifications of the spectral response of the photodiode was obtained from its manufacturer (Hamamatsu Photonics, Hamamatsu, Shizuoka, Japan) for each 20 nm interval. As shown in Fig. 1, the sensor has the maximum response at 680 nm, and has smaller but considerable responses in the 700-800 nm and 1000-1500 nm ranges. Since about half the inci-

Canopy reflectance, % is calculated as follows:

3 ' = S r / S i n c

where Sr is the daily amount of light reflected by the canopy, and Si,c is the daily light incidence upon the canopy. In order to avoid accidental interference from the shadows of the chamber structures with the incident light measurement, the measurements were averaged across the chambers, and the average was used for Si,c in the above calculation. The reflectance was smoothed with locally weighted linear regression (Cleveland, 1979) to reduce random variations.

In order to estimate canopy reflectance before the commencement of the light measurement, the relationship between LAI and canopy reflectance was examined for the vegetative growth. The LAI was smoothed by cubic splines using the CSSCV routine of the IMSL library (IMSL, 1987), and the following function (Kishida, 1973) was fitted to the relationship between the smoothed LAI (L) and the smoothed reflectance

(3'):


y = yf - (yf - yo)exp( - KrL)

where yf is the reflectance at canopy full cover, 3'0 is the reflectance of paddy soil/water, K v is a coefficient. An optimization program (Kobayashi, 1981 ) with the simplex algorithm was used to estimate the parameters Yf, 3'0 and Kv. Canopy reflectance before the commencement of the light measurement was then estimated from the smoothed LAI using the above relationship between LAI and canopy reflectance. Can- opy light reflection was calculated on a daily basis from the estimated or smoothed reflectance and the incident light in the chambers.

2.3. Transmittance

Canopy transmittance (~') is calculated as:

~'= S,/ Si,c

where St is the daily amount of light transmitted by the canopy, and Si,~ the daily amount of light incident above the canopy. The observed transmittance of the rice canopy was smoothed with the locally weighted linear regression as noted above for reflectance, and the smoothed values were used for further calculation.

In order to estimate canopy transmittance before the commencement of the light measurement, a relationship between LAI (L) and transmittance (r) was assumed:

r = exp ( - KL)

where K is the light extinction coefficient. With ~" and L observed on a regular basis throughout the growing season, the value of K was determined and examined for a seasonal change as follows. LAI was smoothed by the cubic splines ( IMSL, 1987). From the smoothed LAI (L) and canopy transmittance (~-), the canopy light extinction coefficient (K) was calculated for each measurement of LAI as:

K = - (log;,)/L

Seasonal change of the parameter K with the change of L was examined, and a function was fitted to the relationship between the two. The function was used to estimate the light extinction coefficient (K) when light measurement had not been performed, particularly before the initiation of the light measurement. The light transmittance ~" was then estimated from the estimated

K and smoothed LAI (L) for the duration when light measurement was lacking.

2.4. Absorption

From the canopy reflectance (y) and transmittance (~'), canopy light absorptance (a ) was calculated as (Kishida, 1973):

or= 1 - y - ( 1 - yo)~"

where 3'0 is the reflectance of the paddy surface. The amount of light absorbed by the rice canopy

Sabs) was calculated on a daily basis as:

Sab s = o~Sin c

where Sine is the daily amount of light incident upon the rice canopy, and a is light absorptance. Sine is calculated from daily incident light and the light transmittance of the chamber cover smoothed with the locally weighted linear regression. Missing data for the incident light were estimated from the weather monitoring data at the National Institute of Agro-Environ- mental Sciences (NIAES). The monitoring station of NIAES is located approx. 500 m north-east of the field exposure chambers.

The daily amount of light absorption was aggregated into seasonal integral of light absorption, and the effect of ozone on the amount of light absorption by the rice canopy was examined.

2.5. Light-use efficiency

Total dry weight was log-transformed and smoothed using cubic splines (IMSL, 1987), and then plotted against cumulative absorbed light. A segmented linear model was fitted to the relationship between total dry weight (W) and the accumulated light absorption (see below). The segmented linear model is given as:

W = •vAabs

before heading, and

W= EvA, + ~r(Aab s - -Ah)

after heading, where Ev is the light-use efficiency (LUE) during vegetative growth, Er is LUE during reproductive growth, A~s is accumulated light absorption, and Ah is light absorption accumulated until the heading date. On the basis of the experimental results


which showed an almost constant canopy light absorptance after heading, the canopy absorptance on the heading date was used in the calculation of A~b~ thereafter.

The parameters ~ and er were estimated with the least square method. The segmented model has an inflection point at the heading date. The slopes, ev and ~, of the linear model represent LUE for vegetative and reproductive stages, respectively.

The effect of ozone on the LUE was examined for vegetative and reproductive growth stages. The poly- nomial regression was performed with the REG procedure of the Statistical Analysis Systems Institute Inc. (SAS, 1988) on the relationship between LUE and the average ozone concentrations for the respective growth stages.

3. Results

3.1. Reflectance

The seasonal change of the smoothed canopy reflectance for each ozone treatment is shown in Fig. 2 for 1987 (Fig. 2(a) ) , 1988 (Fig. 2(b)) and 1989 (Fig. 2 (c)) . As mentioned earlier, the canopy reflectance for the 1987 experiment was not measured on and after 100 DAT because of the severe lodging for all the ozone treatments.

During the vegetative growth, canopy reflectance increased with increasing LAI, and approached an asymptote at approx. 0.14 around the heading date. About 10 days after heading, the reflectance increased again toward the final harvest, despite the decrease of

0.16

0.14

0.12

0.1

0.08

j O ~

/ he in

0.16 . . . . ~' J

0.12 -.~r ' c: Ax l .0

0.1 • • Ax2.0

0.08 i ~ ' - -~ - -AX2.75

i 0.16-I + ' ' t ' t ' 4 ' Ii ~-~ o '

0.14

0.121 ~ "

0,11 i he ng

0 08 20 40 60 80 100 120 140 160

DAT

Fig. 2. Seasonal changes of canopy reflectance in 1987 (a), 1988 (b) and 1989 (c).


0.16 I . . . . . E - ~1~5 '

o O 0 - -, 0 .14 •

. ,~dD.~r~ ' i ~ • ~ "

6 .12 A . ~ ~

e / ~ I ' - I © 1987 -

i . / i ~ / • 1988 I 0.1 l . , i ~ " - A 1 9 8 9 I '

J ""edeqn ! I 0.08 t , t • ~ , ~ _ t • J

0 2 4 6 8 10

LAI

relationship between LAI (L) and reflectance (y) was described by the equation (Kishida, 1973):

7 = 7r - ( Yr - 7o)exp( - Kz, L)

where, Yr is the maximum canopy reflectance, 70 is the reflectance of the paddy surface, and K v is a constant. The parameter values were estimated as 3,f=0.169, 70 = 0.086, and K v = 0.185.

Fig. 3 also shows that the same relationship holds across the different ozone levels. There was no effect of the ozone treatment on the seasonal amount of light reflected by the rice canopy.

Fig. 3. Relationship between LAI and canopy reflectance.

LAI. Maximum reflectance reached the range 0.15- 0.17.

In Fig. 3, the canopy reflectance is plotted against LAI. Across the three years, among which the reflectance per se differed due to the difference in LAI, the

3.2. Transmittance

Fig. 4 depicts the seasonal changes of canopy transmittance for the 1987 (Fig. 4 (a ) ) , 1988 (Fig. 4 (b ) ) and 1989 (Fig. 4 (c ) ) experiments. The transmittance decreased rapidly with increasing LA! at the initial

8 ::1=

0 . 7 ~ , T , ~ , t , ~ , ~ , ~ ,

.... . . . . . . . . . . . . . •

0.5 i 0 . 4 ~ " heading : ....... :, .....

o,2 ~ i ~ ~ i o . 3 I . . . . . . . ~ .... . . . . . '~

. . . . .

o.8- i ' i , 0 . 7

0 , 5 I lk ! heading i [ - 0.4

0.3

0.2

0.1

0.9

0.8

0.7

0.6

0.5

0.4

0.3

0.2

0.1

0 2 0 4 0 6 0 8 0 1 0 0 1 2 0 1 4 0 1 6 0

D A T

- - . o - - - A x 0 . 5

4 - - A x l . 0

- ~ - A x 1 . 5

- ~ A x 2 . 0

- - ~ - - A x 2 . 7 5

Fig. 4. Seasonal changes of canopy transmittance in 1 9 8 7 ( a ) , 1 9 8 8 ( b ) a n d 1 9 8 9 ( c ) .


stage of vegetative growth. By the date of heading, the transmittance decreased to 0.10-0.15 with some variation among the plots and years. Slight to no change occurred thereafter in spite of the decrease of LAI due to leaf senescence and abscission.

The light extinction coefficient K decreased with increasing LAI during the vegetative growth (Fig. 5). The relationship between LAI (L) and K can be described by the exponential function:

K = Koexp( - ckL)

where Ko and cK are constant parameters. The above equation was log-transformed, and then the linear model

logK= logKo-ckL

was fitted to the data. The significance of the above relationship and the difference in the parameters between the cultivars 'Koshi-hikari ' for the 1987 and 1989 experiments, and 'Nippon-bare' for the 1988 experiment, were tested using the GLM (generalized linear model) procedure of SAS (SAS, 1988). The result is shown in Table 1. The relationship between LAI and the light extinction coefficient was statistically significant, and was significantly different among the two cultivars (Table 1 ). Since the interaction between LAI and cultivar was not significant, the relationships for the two cultivars should have a common slope, CK. Ozone had no effects on the light extinction coefficient. The parameters Ko and CK were thus determined as Ko = 0.541 (for 'Koshi-hikari ' ) , Ko = 0.484 (for 'Nip- pon-bare' ), Ck = 0.0706 (for both cultivars).

After heading, the canopy transmittance remained almost constant or even decreased (Fig. 4) despite the

Table 1 Effects of LAI and cultivar on the canopy light extinction coefficient

Source of d.f. Mean square F P > F variation

Model 3 0.1286 58.65** 0.0001 Error 75 0.0022

Type lI mean square"

LAI 1 0.3364 153.47"* 0.0001 Cultivar 2 0.0254 11.59"* 0.0011 LAI × Cultivar 1 0.0053 2.41Ns 0.1245

d.f., degrees of freedom. **Significant at p = 0.01 level; NS, not significant. aType II mean square indicates the additional effect of the term to the effects of all other terms.

decrease of leaf area due to leaf senescence (see Fig. 1 of Kobayashi et al., 1995). This resulted in a more rapid increase of the coefficient K than expected from the above relationship between LAI and K.

The seasonal integral of transmitted light showed no effect of the ozone treatment on light transmission.

3.3. Absorption

Seasonal change of canopy absorptance is shown in Fig. 6 for 1987 (Fig. 6 (a ) ) , 1988 (Fig. 6 ( b ) ) , and 1989 (Fig. 6 ( c ) ) experiments. The absorptance increased rapidly as LAI increased during the early vegetative growth, and then attained an asymptote of approx. 0.75 around the heading stage. After heading, the absorptance remained more or less at the same level

0.7

E 0 .6

:_~

0 .5

c 0 .4

~ 0 3

0 . 2

, T , • • [ , i

• A

, • . t . i . . . .

2 4 6 8 10

LAI

! D a t a

~> 1 9 8 7

• 1 9 8 8

• 1 9 8 9

F i t t ed e q n s .

1 9 8 7 & 1 9 8 9

. . . . 1 9 8 ~

Fig. 5. Relationship between LAI and the light extinction coefficient.


¢, 0 ¢,-

g 0 m

<

T- t 0.7 : o6Iy , 0.5

I 0 . 3 L heading

0 . 8 1 - ~ + r ~ _ + ~ L _ 4 ~ ~ + . o o°7!EBl: 0.5~

0.4 i 0.3 heading I

0 8 ~ ! ~ ' ~ ! - ~ t ~ : + 7C!~ 0.7 ~ •

0.6 ~ J

0.5~ 0.4 Ii "~

0.3 ~ 1

0.2

0.1 i heading

0 I . . . . . ! . . . . . .

20 40 60 80 100 120 140 160 D A T

- - -o- - - Ax0.5

~q Ax1.0

- - i A x 1 . 5

• Ax2 .0

- - ~, - - Ax2 .75

Fig. 6. Seasonal changes of canopy absorptance in 1987 (a), 1988 (b) and 1989 (c).

except for the final stage when lodging or leaning was observed.

The seasonal integral of absorbed light for the three years did not show any effects of ozone (Fig. 7). In this figure, the absorbed light for 1987 was based on the measurements through 99 DAT, after which severe lodging prohibited the light measurement. For other years, the calculation was performed for the whole growing seasons.

3.4. Light-use efficiency

The segmented linear model fitted rather well to the relationship between cumulative light absorption and total dry weight (Fig. 8) although, for some plots, the inflection point was set about 10 days after the heading date.

There was a marked difference between vegetative and reproductive growth phases with respect to LUE and its response to the increased ozone (Fig. 9). LUE was much higher before heading than after heading.

The relationship between the mean LUE (~, g mol - ~ ) and the mean ozone concentration (O--'~, nl 1 - ~ ) for the vegetative growth was best described by a quadratic function:

~ = e v - Cv O--~ z (1)

1 8 0 0 [ - ~ • • , ' - ' r •

1700 ,,.

~ 18°°i

Q- 1 5 0 0 eo o

1400 ' • ~ e ~ <

1300 ~ ' J- ' 0 20 40 60 80 100 120

Seasonal mean ozone concentrat ion (nl I ~)

~:, 1987 ! I

• 1 9 8 8 I

• 1 9 8 9 i

Fig. 7. Relationship between the seasonal mean ozone concentration and the absorbed light.

K. Kobayashi, M. Okada /Agriculture, Ecosystems and Environment 53 (1995) 1-12 9

1600

~'E1400

1200

~ 1000

~" 800

"5 600

"~ 400 J::

~o 200

o

Z

1

0 500 1000 1500 2000 Absorbed photon (mol m -2)

Data Ax08)

Data (Ax2.75)

Model (Ax0.5)

L- - -_- M°d_e! (Ax2 .75 ) j

Fig. 8. Relationship between cumulative light absorption and smoothed total dry weight for A X0.5 and A X 2.75 treatments in the 1989 experiment.

1.2 ~ r ~ ~ ' - ' - ' vegetat ive 1.1 • • eqn. 1

1 I ~ © 1987 ~ " • 1988

°,9 1 " • 1989 o~ 0.8 . ~D b v " " reproduct ive ~, 0.7 ,~ "" [] ~ ..... ean. 2

• "~r. c 1987 0.6 • - . 0 5 • "-. • 1988

• 1989 0.4 L_, I . . . . .

0 20 40 60 80 100 120

Mean ozone concentrat ion (rll I 1)

Fig. 9. Relationship between mean ozone concentration and the light- use efficiency (LUE).

where the parameter values are ¢v = 1.057 and cv = 1.302 X 10 -2. For the reproductive growth, the relationship was described by a linear function:

~ : E r - - C r O c (2)

where ¢r=0.908 and cr=3.733X10 -3. Thus, the effect of ozone was much greater in the reproductive growth than in the vegetative growth (Fig. 9). The year-to-year variation in the effect of ozone on LUE is not apparent from the figure.

4. Discussion

Light transmission and reflection by rice canopy have been most comprehensively studied by Kishida (1973). He measured both short wave radiation and

PAR transmitted and reflected by rice canopies throughout the growing seasons for 3 years, and calculated absorptance of the rice canopy. The canopy absorptance reached a maximum of 0.70 and 0.90 for short wave radiation and PAR, respectively, at or after the heading stage. The change of absorptance thereafter was negligible for short wave radiation (see Figs. 42- 44 of Kishida, 1973).

Hirota et al. (1978) also measured light use of rice and soybean canopies for short wave radiation and PAR simultaneously for three growing seasons. Their results showed that the rice canopy absorptance reached a maximum of approx. 0.75 and 0.90 for short wave radiation and PAR, respectively.

Despite the initial intention to use the IKS light sensors to measure PAR, the canopy light absorptance obtained in this study was much closer to that for short wave radiation rather than for PAR reported in the above studies. This may be due to the spectral property of the light sensors, which have considerable response outside the PAR range (400-700 nm) of wavelength (Fig. 1). Therefore, the measurements of the light absorption and, hence, the LUE calculated from the light measurements may not be compared directly with the values reported by others (e.g. Russel et al., 1989). Nevertheless, the response of the canopy light charac- teristics to the ozone exposure may be meaningful on a relative basis.

This study indicated LUE as a major light character- istic affected by the ozone exposure. The depression of LUE can be accounted for by reduced photosynthetic rate, which has been reported in many papers with rice

1 o K. Kobayashi, M. Okada ~Agriculture, Ecosystems and Environment 53 (1995) 1-12

(Taniyama et al., 1976; Nakamura and Saka, 1978; Kouchi, 1980; Mayumi and Yamazoe, 1983) as well as other crop species as reviewed by Reich (1987) and Darrall (1989). Monteith (1977) has demonstrated the close relationship between photosynthetic rate and LUE, and Sinclair and Horie (1989) have modelled the relationship explicitly. Charles-Edwards (1982) described the relationship analytically in his Eq. 4.21. Murata (1981) found a close relationship between maximum photosynthetic rate and LUE corrected for the effect of incident light intensity across a number of crop species. Reduced photosynthesis by ozone should, therefore, cause the depressed LUE.

In fact, Unsworth et al. (1984) found that LUE of soybean plants exposed to ozone in open-top chambers decreased at higher ozone levels. Their results also showed that higher ozone treatment caused earlier abscission, and thus reduced light interception. But the effect of reduced light interception accounted for only a small portion of yield loss due to ozone. Reduced LUE was more important factor for the yield loss (Unsworth et al., 1984).

Leadley et al. (1990) found no effect of ozone on light interception by soybean plants in an open-top chamber experiment which was quite similar to that of Unsworth et ai. (1984). Reduced LUE was the primary factor in the impact of ozone on soybean growth (Lead- ley et al., 1990).

The above papers and the result of this present study suggest that the reduced growth and yield from ozone exposure may primarily be attributed to the depression of LUE.

The effect of ozone on LUE was much greater in reproductive growth than in vegetative growth. Such seasonal change of ozone impact on crop growth has not been well studied.

Asakawa et al. ( 1981 ) exposed potted rice plants to ambient air in a greenhouse at different growth stages and compared the growth of the plants to that in a charcoal-filtered greenhouse. The major air pollutant in the experiment was photochemical oxidants, whose main phytotoxic component is ozone. The authors con- cluded that the effect of air pollution on rice yield was greatest during the panicle development rather than the tillering or grain filling stages (Asakawa et al., 1981 ), although their experimental design precluded an exact comparison between the growth stages.

Unsworth et al. (1984) suggested that the enhanced reduction of LUE later in the growing season might be responsible for the yield loss of soybean by ozone. On the other hand, Leadley et al. (1990) reported that no difference was found between the vegetative and reproductive stages with regard to the effect of ozone on LUE of soybean plants. However, the unusually low LUE (approx. 0.7 g MJ- 1 ) which they reported for the unstressed plot during the vegetative growth implies the impacts of other stresses (e.g. soil moisture deficit).

The above studies including this study have not been specifically designed to address the seasonal change in ozone impact, and hence the conclusions are inherently indirect guesses. Heagle et al. ( 1991 ) studied the effect on soybean yield of ozone exposures in four different growth stages. Their results showed that the ozone exposure during the latter half of a growing season reduced soybean yield the most.

With the same experiment as Heagle et al. (199l) , Miller et al. (1991) showed the accumulative nature of the ozone impact on soybean leaf photosynthesis. The net photosynthesis of individual leaves was pro- gressively suppressed after the commencement of the ozone exposure (see Fig. 1 of Miller et al., 1991 ). Later in the reproductive growth, leaf net photosynthesis declined due to senescence in both control and ozone- exposed plants. Nevertheless, the senescence depressed the photosynthesis of the ozone-damaged leaves even further, and the net photosynthesis in such leaves was almost depleted at the end of the measurements when the leaves of the control plants still showed a significant level of photosynthesis (Miller et al., 1991 ).

The greater reduction of LUE after rather than before the heading shown in this study might also be a result of the cumulative impact of ozone throughout the growing season. During the vegetative growth, new leaves are successively formed over older leaves. Despite the ozone damage accumulated in the older leaves, the canopy photosynthesis is mainly sustained by the upper leaves which are formed later and have not been exposed to ozone for as long as the older ones. The impact of ozone on canopy photosynthesis may thus be moderated during the vegetative growth. After the flag leaves are fully expanded, however, no new leaves are formed and the leaves on top of the canopy are exposed to ozone throughout the rest of the growing season while serving as a major source of photosynthate for seed growth. Thus, the accumulating ozone impact on

K. Kobayashi, M. Okada /Agriculture, Ecosystems and Environment 53 (1995) 1-12 11

the photosynthesis o f the upper leaves would progres-

sively curb canopy dry mat ter product ion and hence

the L U E may be reduced much more than in vegetative

growth. There are, of course, other possibil i t ies than that

noted above for the mechan i sms of the greater ozone impact on growth and yield in the later growing season as shown by Heagle et al. (1991) . Since seed growth is main ly supported by the photosynthate produced in

the reproduct ive growth, it is l ikely that the ozone

impact in the growth phase is more harmful than in the

other with respect to seed yield depression (Mil le r et

al., 1991 ). Further studies are needed on the effect o f

ozone on seed growth processes inc luding part i t ioning of current and stored photosynthate to the seeds.

In conclus ion, the growth decl ine of rice plants is

main ly ascribed to reduced LUE, and the reduct ion of L U E is part icularly ev ident after heading. Further study

should be directed to the causes of the decline of L UE or canopy photosynthesis dur ing the reproductive

growth.

Acknowledgements

Fund ing for this study was supplied by the Environ- ment Agency of the Japanese government . We thank

all the staff of the Fa rm M a n a g e m e n t Divis ion of the

Nat ional Insti tute of Agro -Env i ronmen ta l Sciences for their excel lent technical assistance.

References

Acock, B., 1991. Modeling canopy photosynthetic response to carbon dioxide, light interception, temperature and leaf traits. In: K.J. Boote and R.S. Loomis (Editors), Modeling Crop Photo- synthesis--From Biochemistry to Canopy. Crop Science Society of America/American Society of Agronomy, Madison, WI, pp. 41-55.

Asakawa, F., Tanaka, H. and Kusaka, S., 1981. Differential impacts among the growth stages of photochemical oxidants on growth and yield of rice cultivars of early and late maturity. Jpn. J. Soil Sci. Plant Nutr., 52: 289-296, in Japanese.

Charles-Edwards, D.A., 1982. Physiological Determinants of Crop Growth. Academic Press, North Ryde, Australia.

Cleveland, W.S., 1979. Robust locally weighted regression and smoothing scatter plots. J. Am. Stat. Assoc., 74: 829-836.

Darrall, N.M., 1989. The effect of air pollutants on physiological processes in plants. Plant Cell Environ., 12: 1-30.

Hayashi, K., 1972. Efficiencies of solar energy conversion in rice varieties. Bull. Natl. Inst. Agric. Sci., D23: 1-67, in Japanese with English summary.

Heagle, A.S., Miller, J.E., Rawtings, J.O. and Vozzo, S.F., 1991. Effect of growth stage on soybean response to chronic ozone exposure. J. Environ. Qual., 20: 562-570.

Hirota, O., Takeda, T., Murata, Y. and Koba, M., 1978. Studies on utilization of solar radiation by crop stands. II. Utilization of short wave and soybean plant populations. Jpn. J. Crop Sci., 47: 133-140, in Japanese with English summary.

Horie, T., 1988. The effects on rice yields in Hokkaido. In: M.L. Parry, T.R. Carter and N.T. Kon'jin (Editors), The Impact of Climatic Variations on Agriculture. Vol. 1 : Assessments in Cool Temperate and Cold Regions. Kluwer, Dordrecht, pp. 809-825.

Horie, T. and Sakuratani, T., 1985. Studies on crop-weather relationship model in rice. (1) Relation between absorbed solar radiation by the crop and the dry matter production. J. Agric. Meteorol., 40:331-342, in Japanese with English summary.

IMSL Inc., 1987. User's Manual: Math/Library Version 1.0. IMSL Inc., Houston.

Kats, G., Dawson, P.J., Bytnerowicz, A., Wolf, J.W., Thompson, C.R. and Olszyk, D.M., 1985. Effects of ozone or sulfur dioxide on growth and yield of rice. Agric. Ecosyst. Environ., 14: 103- ll7.

Kishida, Y., 1973. Agro-meteorological studies on utilization of radi- ant energy under cultivated field conditions. (I) Introduction and spectral radiation balance of plant community. Bull. Natl. Kyu- shu Agric. Exp. Stn., 17: 1-79, in Japanese with English summary.

Kobayashi, K., 1981. A subroutine for function minimization by the simplex method. Bull. Comput. Centre Res. Agric. For. Fish., A17: 51-71, in Japanese.

Kobayashi, K., Okada, M. and Nouchi, I., 1994. A paddy field chamber system for exposing rice (Omza sativa L.) plants to ozone. New Phytol., 126: 317-325.

Kobayashi, K., Okada, M. and Nouchi, I., 1995. Effects of ozone on dry matter partitioning and yield of Japanese cultivars of rice (O~.za sativa L.). Agric. Ecosyst. Environ., in press.

Kouchi, H., 1980. Studies on relationships between ozone absorption rate and stomatal diffusion resistance of plant leaf. J. Jpn. Soc. Air Poll ut., 15:1 (}9-117, in Japanese with English summary.

Kropff, M.J., 1990. The effect of long-term open-air fumigation with SO2 on a field crop of broad bean ( Viciafaba L. ) III. Quantitative analysis of damage components. New Phytol., 115: 357-365.

Leadley, P.W., Reynolds, J.F., Flagler, R.B. and Heagle, A.S., 1990. Radiation utilization efficiency and the growth of soybeans exposed to ozone: a comparative analysis. Agric. For. Meteorol., 51: 293-308.

Mayumi, H. and Yamazoe, F., 1983. Effects of photochemical air pollution on plants. Bull. Natl, Inst. Agric. Sci., B35: 1-71, in Japanese with English summary.

Miller, J.E., Persley, W.A., Vozzo, S.F. and Heagle, A.S., 1991. Response of net carbon exchange rate of soybean to ozone at different stages of growth. J. Environ. Qual., 20: 571-575.

Monteith, J.L., 1977. Climate and the efficiency of crop production in Britain. Phil. Trans. R. Soc. London Ser. B, 281: 277-294.

12 K. Kobayashi, M. Okada / Agriculture, Ecosystems and Environment 53 (1995) 1-12

Munakata, K. and Shibayama, M., 1985. A spectro-radiometer for field use. I. Design and sample data. Jpn. J. Crop Sci., 54: 15- 21, in Japanese with English summary.

Murata, Y., 1981. Dependence of potential productivity and efficiency for solar energy utilization on leaf photosynthetic capacity in crop species. Jpn. J. Crop Sci., 50: 223-232.

Murata, Y., Miyasaka, A., Munakata, K. and Akita, S., 1968. On the solar energy balance of rice population in relation to the growth stage. Jpn. J. Crop Sci. 37: 685-691, in Japanese with English summary.

Nakamura, H., 1979. Investigation on injury to rice plants from photochemical oxidants. Bull. Natl. Inst. Agric. Sci., D30: 1-68, in Japanese with English summary.

Nakamura, H. and Saka, H., 1978. Photochemical oxidants injury in rice leaves. 3. Effect of ozone on physiological activities in rice plants. Jpn. J. Crop Sci., 47: 707-714, in Japanese with English summary.

Reich, P.B., 1987. Quantifying plant response to ozone: a unifying theory. Tree Physiol., 3: 63-91.

Russel, G., Jarvis, P.G. and Monteith, J.L., 1989. Absorption of radiation by canopies and stand growth. In: G. Russell, B. Mar- shall and P.G. Jarvis (Editors), Plant Canopies: Their Growth,

Form and Function. Cambridge University Press, Cambridge, pp. 21-39.

Sakuratani, T., 1986. Diurnal and seasonal changes in solar spectral radiation at Kannondal, Tsukuba. Bull. Natl. Inst. Agro-Environ. Sci., l: 37-50.

Sinclair, T.R. and Horie, T., 1989. Leaf nitrogen, photosynthesis, and crop radiation use efficiency: a review. Crop Sci., 29: 90- 98.

Statistical Analysis Systems Institute Inc., 1988. SAS/STAT User's Guide, Release 6.03 Edition. Statistical Analysis Systems Insti- tute Inc., Cary, NC.

Taniyama, T., Yamashita, K. and Koike, T., 1976. Studies on the mechanism of injurious effects of toxic gases on crop plants. XIII. Effects of ozone in the air on the apparent photosynthesis of corn, rice, and peanut plants. Proc. Crop Sci. Soc. Jpn., 45: 9- 16, in Japanese with English summary.

Unsworth, M.H., Lesser, V.M. and Heagle, A.S., 1984. Radiation interception and the growth of soybeans exposed to ozone in open-top field chambers. J. Appl. Ecol., 21: 1059-1079.

Yamagishi, T., Okada, K., Hayashi, T., Kumura, A. and Murata, Y., 1980. Cycling of carbon in a paddy field. Jpn. J. Crop Sci., 49: 232-242.

effects of ozone on the light use of rice (oryza sativa l.) plants

Documents