TROPICS Vol. 13 (1) Issued October 30, 2003

Diurnal CO2 exchange variation in evergreen leaves of the tropical tree, durian (Durio zibethinuszibethinus Murray)

1)* 2)† 3) 3) Kazuharu OGAWA , Akio FURUKAWA , Ahmad Makmom ABDULLAH and Muhamad AWANG

1)Laboratory of Forest Ecology and Physiology, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan 2)Environmental Biology Division, The National Institute for Environmental Studies, Tsukuba, Ibaraki 305-8506, Japan 3)Department of Environmental Sciences, Universiti Putra Malaysia, 43400 UPM Serdang, Malaysia

*Author to whom correspondence should be addressed. †Present address: Department of Biological Sciences, Faculty of Science, Nara Women's University, Nara 630-8506, Japan

ABSTRACT Diurnal variation of in situ CO2 exchange was investigated during the stage where young and old leaves co-exist in three shoots of tropical evergreen trees of Durio zibethinus Murray growing in an experimental field of Universiti Putra Malaysia. The quantitative proportion of young to old leaves and specific leaf area differed among the three samples. The dark respiration rates in the nighttime and

daytime were related exponentially to air temperature. The Q10 ranged between 1.72 and 1.78 for the nighttime dark respiration, and 2.16 and 4.07 for the daytime dark respiration. The relationship between net photosynthetic rate and photosynthetic photon flux density was graphed

using a hyperbolic function, where as the specific leaf area decreased the asymptotic rates tended to decrease. CO2 exchange per day was effected by leaf age. The total dark respiration (sum of nighttime and daytime dark respiration) was high and net photosynthesis was low in the shoot where the proportion of young leaves was high. The photosynthetic efficiency of different aged-leaves, which was defined as the ratio of net photosynthesis to dark respiration, ranged from 32 to 152%. Photosynthetic efficiency was low in the shoot with a high proportion of young leaf area, because of low net photosynthesis and high dark respiration. Characteristics of leaf photosynthesis were discussed with respect to leaf physiology and phenology.

Key words: Durio zibethinus Murray, in situ CO2 exchange, photosynthetic production, Q10, young and old leaves.

INTRODUCTION

CO2 exchange of leaves plays a key role in the carbon economy of woody species. However, the study of photosynthetic characteristics of tropical trees is still fragmentary and in most cases the techniques used for measurements of leaf gas exchange are inadequate, because a lack of leaf temperature control has led to variable results (cf. Bazzaz and Pickett, 1980; Mooney et al., 1980; Medina and Klinge, 1983). Ogawa et al. (1995a) developed an open gas-exchange system which tracked ambient air temperature while continually measuring CO2 gas-exchange of fruits of a tropical evergreen tree, Durio zibethinus Murray. D. zibethinus is well known for its large fruits, which can reach 17 cm in diameter and 384 g dry wt. (Ogawa et al. 1995a). It takes about 4 months for the fruits to mature and fruiting often occurs twice a year (Idris 1990; Smith et al. 1992). Ogawa et al. (1995a) provided experimental evidence that photosynthetic assimilates equivalent to 125% of the fruit dry mass is translocated to the fruit from other organs until fruit maturation (Ogawa et al. 1996). Therefore, it is expected that the photosynthetic production by leaves should be high in D. zibethinus in comparison with woody species bearing smaller fruits. Ogawa et al. (1995b) inferred the photosynthetic production by leaves using phenological information on leaf survival strategies. However, physiological data, such as CO2 exchange, of D. zibethinus leaves is lacking.

In this paper, the CO2 measurement system developed by Ogawa et al. (1995a) was used for three shoots of D. zibethinus. The purpose of the measurements was to obtain fundamental information, such as the temperature dependence of respiration and light dependence of photosynthesis, on the basis of the results of diurnal changes in CO2 exchange rate of leaves. New leaves on the evergreen trees of D. zibethinus emerged during the stage of co-existence of newly emerged leaves and old leaves. The quantitative proportions of newly emerged leaves to old leaves differed among the three samples. Therefore, the effect of leaf age on respiration and photosynthesis were assessed. Furthermore, characteristics of photosynthetic production of leaves of D. zibethinus were discussed and compared to published data on photosynthesis and respiration. 18 K. OGAWA, A. FURUKAWA, A. M. ABDULLAH and M. AWANG

MATERIALS AND METHODS

Plant materials Experiments were conducted on three shoots, sample Nos. 1 and 2 from tree No. 1 and sample No. 3 from tree No. 2 of durian (Durio zibethinus Murray) growing in an experimental field station of University Putra Malaysia (UPM) in Selangor, Malaysia. The sample trees, which were derived from the same clone, were planted widely enough to receive full sunlight. The stem diameter at breast height was 27.4 and 34.1 cm in tree Nos. 1 and 2, respectively. The shoots sampled were located on the lower crown surface, but were exposed to full sunlight. The shoots consisted of ten young and twelve old leaves in sample No. 1, six young and twenty-two old leaves in sample No. 2, and ten young and twenty-four old leaves in sample No. 3. Leaves were classified as young or old leaves according to their appearance, i.e., light green for young and dark green for old leaves. The young leaves were almost fully expanded.

Gas measuring apparatus

In situ CO2 exchange of a whole shoot was measured with an open gas exchange system (cf. Ogawa et al. 1995a). Each shoot was enclosed in a cylindrical assimilation chamber, 18 cm in height and 33 cm in diameter. The assimilation chamber had a thermomodule and a fan in the lower part with two aluminium fin-plates. The inside wall of the chamber was covered with a transparent FEP Teflon film (Du pont, Wilmington, DE). Air temperature was measured outside and inside the chamber with platinum resistance thermometers. The chamber temperature was adjusted to match the outside temperature using a temperature controller (MC-A04A/S, Koito, Tokyo,

Japan). The ambient air was taken 11 m above the ground and passed through two air buffers to stabilize the CO2 concentration. The air was fed into the assimilation chamber at a rate of 5.0 l min-1 with an air flow meter (RK1250, Koflock, Kyoto, Japan) and air pump (DM-707ST, Enomoto, Tokyo, Japan). Before the chamber and ambient air were measured with the infrared gas analyzer (EGA, ADC, Herts, UK), the moisture in the air was removed with a perma-pure drier (ZBJ02502-72P, Fuji Electric, Tokyo, Japan) by pressing the air samples with an air pump (APN-085VX-1, Iwaki, Tokyo, Japan). In addition, the air passing through the perma-pure drier was sent to two glass tubes containing a drying agent of magnesium perchlorate. Sample gases were alternatively drawn into the gas analyzer at three-minute intervals. Switching was done using two solenoidal valves (SAB 352-6-0; CKD, Komaki, Japan) which were controlled with two timers (H3BA; Omron, Kyoto, Japan).

The data from the CO2-analyzer and thermometers were recorded with a chart recorder (LR4100, Yokogawa, Tokyo, Japan). The integrated value of photosynthetic photon flux density was measured with two quantum sensors (LI-190SA, Li- Cor, Lincoln, NE), one on the chamber and the other outside the crown. The values were stored in a data logger (LI-1000, Lincoln, NE) at one-hour intervals in August and 30-minute intervals in September.

Gas measurement procedures

The CO2 exchange was measured continuously for whole days during the periods of August 6 to 10, 1993 for sample No. 1, August 10 to 13 for sample No. 2, and September 17 to 28 for sample No. 3. Dark respiration during the day was measured by covering the assimilation chamber with aluminum foil in the morning, and the measurement was conducted for entire days from August 9 to 10 for sample No. 1, August 12 to 13 for sample No. 2, and September 24 to 28 for sample No. 3.

In this study, CO2 exchange rate was calculated for 30-minute intervals using three-minute interval data. Night was defined as the period when the integrated value of photosynthetic photon flux density outside the crown was zero.

After the measurement of CO2 exchange, the leaf area of young and old leaves in each shoot was measured with an area meter (AAC-100, Hayashi Denko, Tokyo, Japan). The dry mass of these leaves was determined after oven-drying at 85℃ for 24 h. The quantitative characteristics of the shoots are summarized in Table 1. In this study, rates of photosynthesis and respiration were expressed by leaf area, and the respiration of twigs was disregarded, because the dry mass ratio of leaves to twigs was more than 5.5.

Determining the temperature dependence of respiration and light dependence of photosynthesis with curve fitting The dependence of respiration r on temperature θ was graphed using the following exponential equation (eg. Butler & Landsberg 1981; Jarvis & Leverenz 1983; Hagihara & Hozumi 1991; Paembonan et al. 1991): CO2 exchange in tropical evergreen leaves 19

r = r0 exp (kθ) ¸

where r0 and k are coefficients specific to each sample.

The temperature coefficient Q10 is commonly used to quantitatively express chemical reactions of biological processes in relation to temperature. The Q10 value indicates how much physiological function increases with a temperature increase of

10℃. The Q10 value is about 2 in physiologically relevant temperature ranges (eg. Negisi 1970, 1977; Landsberg 1986; Fitter

& Hay 1987). Considering equation 1, we can estimate the Q10 of respiration as follows:

Q10 = exp (10k) ¹

The relationship between the net photosynthetic rate pn and the photosynthetic photon flux density PPFD was graphed using a light response model for photosynthesis (Thornley 1976; Charles-Edwards 1981),

º p = bPPFD r n ―――――1+aPPFD － where a, b and r are coefficients specific to each sample. The coefficients a indicates the reciprocal of PPFD at which one- b half of the asymptotic rate, ―a －r, is realized, the coefficient b stands for the gradient of saturating curve of Equation 3 at the origin or the maximum quantum yield, and the coefficient r represents a constant dark respiration rate at PPFD=0. The curve fittings in equations 1 and 3 were performed by the least squares method.

RESULTS

Specific leaf area The specific leaf area SLA ranged from 1.54 to 1.61 dm-2 g-1 in young leaves, and 0.58 to 0.91 dm-2 g-1 in old leaves (Table 1). Therefore, SLA indicates leaf age. In old leaves, SLA was much lower in sample No. 1 than in sample Nos. 2 and 3. The young leaves can be regarded as immature leaves, and the old leaves consist of mature and senescent leaves.

Table 1. Quantitative characteristics of shoots. The amounts per shoots, which were enclosed by the assimilation chamber, are given. Y, Young leaves; O, Old leaves; T, Young and old leaves. Leaves Twigs Sample Number Area Dry mass Specific leaf area Dry No. YO Y O T Y/T Y O T Y/T Y O T mass [dm2] [dm2] [%] [g] [%] [dm2 g-1] [g] 1 10 12 05.61 03.26 08.88 63.2 03.65 03.88 07.52 48.5 1.539 0.843 1.180 1.25 2 0622 01.11 09.88 10.99 10.1 00.69 10.82 11.51 06.0 1.613 0.914 0.956 2.05 3 10 24 01.36 13.07 14.42 09.4 00.85 22.45 23.30 03.6 1.602 0.582 0.619 3.61

Diurnal change in CO2 exchange rate

Figure 1 shows an example of the daily change in CO2 exchange rate per unit leaf area, air temperature inside the assimilation chamber and photosynthetic photon flux density PPFD at the chamber top in sample No. 2. In this figure, net

CO2 release rate is expressed as a negative value. The net photosynthetic rate changed in a similar way to PPFD. The dark respiration rates in nighttime and daytime were similar in their response to the air temperature inside the assimilation chamber. The respective highest values of net photosynthesis, respiration rates in nighttime and that in daytime were 2.93, 1.15 and 2.57 µmol m-2 s-1 in sample No. 1, and 3.73, 0.953 and 1.93 in sample No. 2, and 3.01, 0.439 and 0.904 in sample No. 3, respectively.

Temperature dependence of nighttime dark respiration The nighttime dark respiration rate was plotted against the air temperature inside the assimilation chamber for each shoot on the semi-log coordinates (Fig. 2). The nighttime dark respiration rate increased exponentially with an increase in air temperature in all shoots. This relationship was described by equation 1, where the values of r0 and k were determined to be 20 K. OGAWA, A. FURUKAWA, A. M. ABDULLAH and M. AWANG

0.162 µmol m-2 s-1 and 0.0577℃-1 in sample No. 1, 0.156 µmol m-2 s-1 and 0.0554℃-1 in sample No. 2, and 0.0846 µmol m-2 s-1 and 0.0540℃-1 in sample No. 3, respectively.

1400

] 1200 -1 s

-2 1000 800 mol m

µ 600 400

PPFD [ 200 0

45

] 40 ℃

35

30

Temperature [ 25

20 ] -1

s 4 -2 3 Fig. 1. An example of daily change in CO2 exchange

mol m 2 rate, air temperature inside the assimilation µ chamber and photosynthetic photon flux 1 density on the assimilation chamber in 0 sample No. 2. CO2 uptake and release rates -1 are expressed as positive and negative

exchange rate [ values, respectively. During the period after 2 -2 0:00 12:00 0:00 12:00 0:00 12:00 0:00 12:00 the time indicated by the arrow, daytime CO August 10 11 12 13 dark respiration was measured.

Sample No. 1

1 ] -1 s -2 0.2 16 18 20 22 24 26 28 30 32 mol m µ [ Sample No. 2

1

0.2 16 18 20 22 24 26 28 30 32 1 Sample No. 3 Nighttime dark respiration rate

Fig. 2. Effects of air temperature inside the assimilation chamber on nighttime dark 0.1 respiration rate in sample Nos. 1, 2 and 3. 16 18 20 22 24 26 28 30 32 The straight lines are approximations by Temperature [℃] equation 1. CO2 exchange in tropical evergreen leaves 21

Sample No. 1

1 ] -1

s 0.4 -2 20 25 30 35 40

mol m Sample No. 2 µ

1

0.4 20 25 30 35 40 1 Sample No. 3 Daytime dark respiration rate [

Fig. 3. Effects of air temperature inside the assimilation chamber on daytime dark

0.1 respiration rate in sample Nos. 1, 2 and 3. 20 25 30 35 40 The straight lines are approximations by Temperature [℃] equation 1.

The values of temperature coefficient Q10 in the nighttime dark respiration, which were estimated to be 1.78 in sample No. 1, 1.74 in sample No. 2, 1.72 in sample No. 3, were almost the same among the shoots.

Temperature dependence of daytime dark respiration The temperature dependence of daytime dark respiration rate is illustrated on semi-log coordinates in Fig. 3. Similar to the nighttime dark respiration, the daytime dark respiration rate was exponentially related to the air temperature inside the -2 -1 assimilation chamber in all samples. The values of r0 and k in equation 1 were determined to be 0.0247 µmol m s and 0.140℃-1 in sample No. 1, 0.102 µmol m-2 s-1 and 0.0830℃-1 in sample No. 2, and 0.0473 µmol m-2 s-1 and 0.0771℃-1 in sample No. 3, respectively.

Similar to the nighttime dark respiration, the Q10 of the daytime dark respiration was estimated on the basis of equation

2 as follows: 4.07 in sample No.1, 2.29 in sample No. 2, and 2.16 in sample No. 3. The Q10 value in sample No. 1, where the proportion of young leaf area was higher, was considerably higher than that of sample No. 2. The Q10 value of the daytime dark respiration was higher than that of the nighttime dark respiration in all samples.

Light dependence of net photosynthesis The relationship between the net photosynthetic rate and the photosynthetic photon flux density was graphed using a light response model for photosynthesis in equation 3 (Fig. 4). The values a, b and r in equation 3 were 0.00164 (µmol m-2 s-1)-1, 0.00719 and 0.465 µmol m-2 s-1 in sample No. 1, 0.00379 (µmol m-2 s-1)-1, 0.00174 and 0.610 µmol m-2 s-1 in sample No. 2, and 0.0121 (µmol m-2 s-1)-1, 0.0362 and 0.395 µmol m-2 s-1 in sample No. 3, respectively. -2 -1 While the light saturation of pn was not even 1000 µmol m s in sample No. 1 where the area proportion of young -2 -1 b leaves was higher, it was below 1000 µmol m s in sample Nos. 2 and 3. From equation 3, the asymptotic rate ―a －r was computed to be 3.93 µmol m-2 s-1 in sample No. 1, 3.97 in sample No. 2, and 2.60 in sample No. 3.

Daily carbon balance The daily carbon balance for each shoot is listed in Table 2. Daily respiration loss was higher in sample No. 1 having a high proportion of young leaf area than in sample Nos. 2 and 3 having a high proportion of old leaf area. However, the ratio of daily daytime dark respiration to daily total dark respiration did not differ significantly among samples, ranging from 70 to 80%. The daily net photosynthesis was lower in sample No.1 than in sample Nos. 2 and 3. The ratio of daily net photosynthesis to 22 K. OGAWA, A. FURUKAWA, A. M. ABDULLAH and M. AWANG daily total dark respiration, which indicates the efficiency of photosynthesis by leaves, was low in sample No. 1 in comparison with that of sample Nos. 2 and 3 (Table 2).

4 Sample No. 1 3

2

1

0

] -1 -1 0 200 400 600 800 1000 1200 1400 s -2 4 Sample No. 2

mol m 3 µ 2

1

0

-1 0 200 400 600 800 1000 1200 1400 4

Net photosynthetic rate [ Sample No. 3 3

2

1

0 Fig. 4. Response of net photosynthetic rate to -1 photosynthetic photon flux density in 0 200 400 600 800 1000 1200 1400 sample Nos. 1, 2 and 3. The smooth Photosynthetic photon flux density [µmol m-2 s-1] curves represent equation 3.

Table 2. Daily carbon balance in shoots. Dark respiration Net Gross Ratio Sample Nighttime (R ) Daytime (R ) Total (R +R ) photosynthesis (P ) photosynthesis (P +R ) R /(R +R ) P /(R +R ) No. n d n d n n d d n d n n d [mol m-2 day-1] [%] 1 0.0293 0.1073 0.1366 0.0432 0.1505 78.631.6 2 0.0237 0.0605 0.0842 0.0772 0.1377 71.891.7 3 0.0131 0.0303 0.0434 0.0656 0.0959 69.8 151.2

DISCUSSION

Leaf age difference in CO2 exchange Sample No. 1, having a high proportion of young leaf area, showed high respiratory loss per day compared with sample Nos. 2 and 3, having a high proportion of old leaf area. Namely, the respiratory activity was higher in young leaves, because of the increase in constructive respiration relating to the energy requirement for the growth of living tissues (Thornley 1970; McCree 1974; Yokoi et al. 1978; Kimura et al. 1978). Koike (1987, 1990) also reported a similar phenomenon of high respiration at the early stage of leaf development in deciduous trees. In evergreen trees, the net photosynthetic rate per a leaf area of young leaves is often close to zero even though the leaves are fully expanded (Kursar & Coley 1992; Miyazawa et al. 1998). The net photosynthetic rate continues to increase with time after full leaf expansion (Kursar & Coley 1992), reaches its steady-state level at leaf maturation (Miyazawa et al. 1998), and then decreases from year to year (Larcher 1995). Therefore, sample No. 1 with a high proportion of young leaf CO2 exchange in tropical evergreen leaves 23 area showed the lowest value of net photosynthesis per day. However, the gross photosynthesis, which is defined as the sum of net photosynthesis and daytime dark respiration, was the highest in sample No. 1 and the lowest in sample No. 3 (Table 2). This result suggests that the photosynthetic activity itself is higher in the shoots having a high proportion of young leaf area. The low ratio of net photosynthesis to dark respiration in sample No. 1 (Table 2) resulted from high respiratory activity since this shoot had a high proportion of young leaf area.

Comparison of CO2 exchange rate in other tropical trees Few published data exist for dark respiration of attached leaves in tropical forests, although Meir et al. (2001) reported values in nighttime for tropical trees of 0.11-0.78 µmol m-2 s-1 (at 25℃) in Brazil, and 0.22-1.19 µmol m-2 s-1 in Cameroon. In this study, the dark respiration rates, corrected to 25℃ on the basis of equations 1, were in the range from 0.327 to 0.687 µmol m-2 s-1 for the nighttime, and 0.325 to 0.823 µmol m-2 s-1 for the daytime. This range of nighttime dark respiration rates is similar to the previously reported range.

According to Meir et al. (2001), the Q10 values of the nighttime dark respiration of attached leaves range between 1.5 and

4.1 with a mean of 2.3 in tropical trees growing in Brazil, and between 1.6 and 3.1 with a mean of 2.0 in Cameroon. The Q10 values of the nighttime dark respiration in this study were almost the same as the range of Q10 values reported by Meir et al. (2001). The maximum rates of net photosynthesis have been found to be above 10 µmol m-2 s-1 or higher in attached individual leaves of tropical canopy trees (Zotz & Winter 1993; Furukawa et al. 2001). In the tropical species growing in gap or open sites, the maximum rates of net photosynthesis at the individual leaf level were reported between 2.6-3.5 µmol m-2 s-1 (Newell et al. 1993) and 1.9-11.0 µmol m-2 s-1 (Ishida et al. 1999). The asymptotic rate of net photosynthesis in this study (2.60-3.97 µmol m-2 s-1) is not high compared with the above-mentioned published data, however gas-exchange rates obtained at the leaf level are not easily compared with those at the shoot level. Ogawa et al. (1995b) pointed out that D. zibethinus has lower leaf longevity or a higher turn-over rate than many other tropical trees. They inferred that the lower leaf longevity is advantageous for newly emerged leaves to frequently reach their highest photosynthetic production potential. Considering the result that the asymptotic rate of net photosynthesis is not so high, it is not possible that D. zibethinus leaves inherently possess high photosynthetic capacity for producing big fruits. Therefore, it is concluded that the phenological characteristic of lower leaf longevity, rather than physiological functions such as photosynthetic capacity, plays an substantial role in raising leaf photosynthetic production enough to allow for the production of the big fruits of D. zibethinus.

ACKNOWLEDGMENTS We thank Professor A. Hagihara, University of the Ryukyus, for his helpful advice, Mr. J. Shamsuddin, Universiti Putra Malaysia (UPM), for generously supporting our research, and the staff of the experimental field station at UPM for access to their facilities. This work is part of the Malaysia-Japan joint research project between Forest Research Institute of Malaysia (FRIM), UPM and National Institute for Environmental Studies (NIES), Japan. This work was supported by a Global Environmental Research Program Grant (No. E-4) from the Environmental Agency.

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Received 19th May 2003 Accepted 29th Sep. 2003