the light environment in two woody and two herbaceous plant species

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1 Functional Ecology 2003 Phenological and morphological adaptations to Blackwell Science, Ltd the light environment in two woody and two herbaceous plant species K. KIKUZAWA Laboratory of Forest Biology, Graduate School of Agriculture, Kyoto University, Kyoto, Japan Summary 1. Leaf emergence, leaf longevity, light regime and photosynthetic rates were investigated in order to clarify the morphological and phenological adaptations to light conditions by avoiding self-shading in two herbaceous (Polygonatum odoratum and Polygonum sachalinensis) and two woody (Fagus crenata and Alnus sieboldiana) plants in artificially created open habitats in Japan. 2. Fagus and Polygonatum open their leaves simultaneously as a flush during a short period at the start of the growing season (simultaneous foliar phenology), while Alnus and Polygonum open their leaves one by one successively for a longer period (successive foliar phenology). 3. Light conditions at the level of single leaves, defined as photon flux density relative to that above the plant, were essentially the same throughout a growing season for simultaneous species. On the other hand, light conditions for the two successive species degraded with time. There were gradients of light from the distal to basal part of a shoot only in successive species. 4. Reflecting the abrupt decrease in irradiance with time, photosynthetic rates of individual leaves decreased quickly with time in successive species (Alnus and Polygonum), while those of simultaneous species (Fagus and Polygonatum) decreased slowly. Photosynthetic rates of the canopy as a whole, however, were maintained constant over the season in successive species by replacing leaves frequently. Canopy-level photosynthesis decreased slowly with time in the two simultaneous species. 5. Successive leaf emergence is adaptive in open habitats such as flood plains and canopy gaps, while simultaneous leafing is adaptive in light-limited habitats such as the forest understorey. Key-words: Canopy photosynthesis, flush leafing, leaf longevity, shoot angle, successive leafing Functional Ecology (2003) Ecological Society Introduction Canopy architecture of plants has been well analysed as an adaptive design for maximizing light capture by avoiding self-shading (Horn 1971; Kohyama 1991; Kohyama & Hotta 1990; King 1994; King et al. 1997; Valladares & Pearcy 1998). Much attention has been paid to morphological traits such as petiole development (Yamada et al. 2000) and the angle and size of petiole and leaf lamina (Pearcy & Yang 1996; Pearcy & Yang 1998) as a means to avoid self-shading. However, less is known about the relationship between avoidance of self-shading and the phenological traits of leaves. Of these, leaf longevity is important for survival in the shade of the forest understorey (Bentley 1979; Kikuzawa 1989; King 1994). Kikuzawa (1995) kikuzawa@adm.kais.kyoto-u.ac.jp and Kikuzawa et al. (1996) suggested a role of successive leafing in avoiding self-shading. However, these studies did not measure photosynthetic rates of each leaf at each time, so the full significance of leaf phenology in relation to light interception and photosynthetic rate of each leaf is unknown. In this paper I evaluate the significance of leaf emergence for the avoidance of self-shading and total canopy production by including light interception and photosynthesis of each leaf over time for species of contrasting foliar phenology. Two types of leaf emergence patterns have been observed in tree species (Kikuzawa 1983). One is the simultaneous type, where many leaves appear simultaneously as a flush within a single, short period. Shoots of this type also elongate within the same short period. The other is the successive type, where leaves appear one by one successively over an extended period during the growing season. The two types, along with some 29

2 30 K. Kikuzawa intermediate types, have been observed in temperate and tropical forests (Kikuzawa 1984; Kikuzawa 1988; Lowman 1992; Kikuzawa, Repin & Yumoto 1998). As all potential leaves appear at once at the start of a growing season, all leaves of the simultaneous type can carry out photosynthesis throughout the growing season. However, if many leaves are attached on a shoot, leaves in lower positions will be shaded by those in upper positions. This disadvantage of self-shading can be reduced by slanting shoots (Kikuzawa et al. 1996). By this means, all the leaves on a shoot can receive sunlight evenly and the photosynthetic performance of the shoot will increase, although inclining the shoot will also reduce the height growth of the plant and increase biomechanical support costs. In contrast, successive leafing is a method of avoiding self-shading. The first leaf on a shoot will enjoy full sunlight before the second leaf appears, which would otherwise have shaded the first leaf. The second leaf will enjoy full sunlight before the appearance of the third leaf, and so on. We can expect the following from the above arguments. Light conditions on each leaf of a shoot of simultaneous species are not so different from the top to the base of the shoot, and are relatively stable throughout a season, as all leaves appear on a slanting shoot within a short period and are maintained throughout the season. The photosynthetic capacity of each leaf is, accordingly, also expected to be relatively stable within a growing season, although capacity will decline with time due to leaf ageing. As all leaves are maintained throughout the season, the longevity of individual leaves in this type of species exceeds that in successive species (Kikuzawa 1983; Kikuzawa 1988). The maximum photosynthetic rate is predicted to be low in simultaneous species, as there is a trade-off between maximum photosynthetic rate and its duration (Koike 1988; Reich et al. 1991). In contrast, in successive species the terminal shoot will elongate upwards and can grow taller. However, gradients in light condition and photosynthetic ability will occur along a shoot. Irradiance and photosynthetic ability are initially high, and decline with time due to shading by upper leaves which appear later. Leaf longevity is expected to be short in species of this type. The maximum photosynthetic rate is predicted to be high, compensating for the rapid decline in photosynthetic rate. The leaf phenology and shoot architecture of tree species have been addressed previously (Kikuzawa 1995), but less is known about herbaceous plants, although similar syndromes concerning leaf phenology and architecture are expected. This paper aims to clarify the relationships between leaf emergence patterns and shoot inclination, and between light interception and photosynthetic rate in a comparison of pairs of herbaceous and woody species. The following questions are addressed. (1) Are shoot inclination greater and height growth smaller in simultaneous-leafing compared with successive-leafing species? (2) Are gradients of light along a shoot greater and the decline in irradiance more rapid in successive compared to simultaneous species? (3) Does leaf longevity in simultaneous species exceed that in successive species? (4) Is the maximum photosynthetic rate greater in successive than in simultaneous species? (5) Are gradients of photosynthetic rate along a shoot greater and the decline in photosynthetic rate with time more rapid in successive compared with simultaneous species? Materials and methods STUDY SPECIES Two herbaceous species were studied: Polygonatum odoratum Druce var. maximowiczii (Fr. Schm.) Koidz. (Liliaceae) and Polygonum sachalinensis Fr. Schm. (Polygonaceae); and two woody species: Fagus crenata Blume (Fagaceae) and Alnus sieboldiana Matsum. (Betulaceae). Each species was selected as a representative of simultaneous and successive leafing (Kikuzawa 1983). Polygonatum odoratum var. maximowiczii reaches m at maximum height, and is usually found in the understorey of deciduous broadleaved forests in the temperate region of Japan. Polygonum sachalinensis is usually found in moist, sunny sites such as landslides, flooded plains or roadsides in Hokkaido, the northern island of Japan, and reaches more than 1 m maximum height (occasionally 3 4 m). Fagus crenata usually reaches more than 20 m maximum height, and is a dominant tree in deciduous broadleaved forests in the temperate region of Japan. Alnus sieboldiana usually reaches 5 10 m maximum height. This species is naturally distributed in the southern part of central Japan, but is usually planted for landslide protection in central Japan. Generic names of plants are used here. STUDY SITES The two herbaceous species were studied in an experimental forest of Hokkaido Forest Research Institute in Bibai, in the central part of Hokkaido. Mean annual temperature is 7 C, the maximum occurring in July or August (21 22 C) and the minimum in January ( 9 C). Mean annual precipitation is about 1200 mm. August is the wettest month (149 mm) and May the driest (50 mm). The study was carried out on naturally growing plants in an open area of m. This area was created after clear-cutting of natural deciduous broadleaved forest about 5 years before the start of the study. Natural regrowth of herbaceous plants such as Polygonum and Polygonatum and other herbaceous plants from the remaining root systems occurred in the open area. Little regrowth of woody plants was found. In the spring of 1993 shoots of both species just appearing from the soil were selected and marked. About 20 shoots of each of the two species were selected. Shoots were situated c. 1 m apart and the effect of mutual shading was small.

3 31 Leaf emergence patterns and photosynthesis The two woody plants were studied in an artificially constructed open space (50 50 m) in the experimental sites of the Center for Ecological Research of Kyoto University, situated in Ohtsu, central part of Honshu, Japan. The mean annual temperature is 14 C, the maximum temperature occurring in August (26 C) and the minimum in January (3 C). Mean annual precipitation is about 1600 mm. June is the wettest month (230 mm) and December the driest (80 mm). In 1997, alluvial sandy soil was transported from Kyoto in order to make a flat plain, and the space was filled to c. 2 m depth. In spring 1999, year-old seedlings of Fagus were planted randomly on the space. The average distance between seedlings was 2 7 m. Seedlings were c. 0 5 m tall. Seedlings of Alnus grew from naturally dispersed seeds. Alnus seedlings 2 or 3 years old were selected for the study. Five seedlings were selected, about 1 m apart, and mutual shading among plants was small. The average seedling height was 0 54 m. MEASUREMENTS Studies on the two herbaceous plants were performed in 1993, and on the two woody plants in In spring 1993, 18 and 15 emerging shoots of Polygonatum and Polygonum, respectively, were marked by attaching tags. Leaves on each shoot were counted at c. 10-day intervals from June to August Photon flux density and photosynthetic rate of each leaf were measured five times from May to August. In spring 2000, buds on the terminal 1-year shoot of Alnus and Fagus were observed for leaf emergence. Eight buds on each of the terminal shoots on each of five selected individuals of Alnus, and buds on the terminal shoots on each of 10 individuals of Fagus, were observed. The number of leaves emerging from buds were counted at 1 2-week intervals from late April 2000 to November 2000 (Fagus) and January 2001 (Alnus) when all the leaves had fallen. The number of leaves that had already fallen was identified by the leaf scars remaining on the shoot. Leaves on a shoot were numbered in order of their appearance from the base to the tip of the shoot. The number and position of leaves already emerged, those fallen and those still attached to the shoot, and their order were identified. Timing of leaf emergence was estimated to be the mid-point between the previous observation and when a new leaf was first observed. Similarly, the timing of leaf fall was estimated to be the mid-point between two successive observations of pre- and post-leaf fall. Leaf longevity (days) was calculated as the difference between the timing of leaf fall and of leaf emergence. Photosynthetic rates were measured using opensystem portable photosynthetic apparatus between and h. Five to 11 shoots of each species were measured. For the two herbaceous species, a KIP system (Koito Inc., Tokyo) was used. Measurements were usually carried out on sunny days. In order to receive full sunlight and to obtain the potential photosynthetic rate, the leaf in the cuvette was forced to face the sun, or upper leaves were moved to avoid casting shade on the target leaf. Photon flux density (PFD) during photosynthesis measurement was µmol m 2 s 1. Leaf temperatures were not controlled and ranged from C. CO 2 concentration at the measurements ranged from µmol mol 1. The photosynthetic rate of the two woody plant species was measured using a portable IRGA (LiCor 6400, LI-COR Inc., Lincoln, NE). CO 2 concentration was controlled at 350 µmol mol 1 and PFD at 1500 µmol m 2 s 1, and the potential photosynthetic rate (P max ) was obtained. Leaf temperature ranged from C, depending on the season. To construct light photosynthesis relationships, the PFD was gradually changed from the maximum 2000 µmol m 2 s 1 to zero in 10 arbitrarily selected steps. Measurements were carried out on the fourth leaves of Alnus and Fagus on 10 June 2000 (Alnus) and 27 May 2001 (Fagus). The fourth leaves of Alnus were the youngest, fully expanded leaves at the time of measurement. Light photosynthesis relations were fitted to a nonrectangular hyperbola with four parameters (Johnson & Thornley 1984). Photon flux densities were measured using a light meter (Model LI-250 Light Meter, LI-COR). Measurements were usually carried out from to h on overcast days for Fagus and Alnus. The PFD at the top of the individual plant was measured at the same time. Relative photon flux density (RPFD) was obtained as the percentage of the PFD at each leaf to that of the top of the individual plant for Fagus and Alnus. As the study was carried out in open habitats, the latter was nearly the same as full sunlight. For Polygonum and Polygonatum, PFDs were measured on the same days as measurement of photosynthesis. The RPFD at each leaf was calculated as the percentage to the highest PFD of the individual. Photosynthetic rates at measured PFD were estimated by using the light photosynthesis relationships (estimated photosynthetic rate, P est ) in two woody species. Shoot angles were measured for the above-ground shoot in herbaceous plants, and for the terminal shoot and lateral current year shoots in woody plants. Length deviation (X cm) of the top of shoots from a vertical line, which extended from the base of the shoot, and length (Y cm) of the top of the shoots from the horizontal line, which also extended from the base, were measured. Angles of the shoot from the vertical line were calculated using the length of X and Y. Results LEAF EMERGENCE Shoots of Polygonatum appeared in mid-may. An average of 9 3 ± 3 0 leaves per shoot (n = 18) appeared within a 10-day period in late May, with the quick elongation of the shoot. No more new leaves emerged later in the season (Fig. 1a). In mid-august to early

4 32 K. Kikuzawa Fig. 1. Leaf emergence and leaf-fall patterns in two herbaceous and two woody species., number of leaves emerged on a shoot;, number of leaves actually attached to a shoot. Means ± SE are shown. (a) Polygonatum odoratum var. maximowiczii; (b) Polygonum sachalinensis; (c) Fagus crenata; (d) Alnus sieboldiana. September leaves became yellow and senesced. Mean leaf longevity was 86 3 ± 18 4 days (mean and SD; n = 186). The leaf-age structure of this species was restricted to two 10-day cohorts. These cohorts shifted through the growing season (Fig. 2a c). Shoots of Polygonum appeared and started to elongate in May. In mid-may one or two initial leaves were observed on a shoot. Leaves appeared successively until August (Fig. 1b). A total of 18 9 ± 7 0 leaves per shoot (n = 15), which was significantly greater than for Polygonatum (t = 5 3; P < 0 001), appeared during the growing season. From mid-june leaves at the lower position on the shoots started to fall. The number of leaves attached to the shoot reached c. 10 leaves per shoot in early June, was maintained until late August, and then declined. Leaf longevity was 72 ± 29 8 days (n = 285), which was significantly shorter than for Polygonatum (t = 5 6; P < 0 001). In late June branching was observed at the top of the shoot. Leaf-age ranges of Polygonum were usually wider than Polygonatum. By 9 June leaf ages ranged from 0 40 days; by 13 July, days; and by 19 August, days. The number of old leaves increased, and concomitantly the range of age class also increased with time (Fig. 2d f). Young age classes persisted to the later stages. Bud break of Fagus was observed in mid-april. Buds elongated and from three to 10 leaves per terminal bud appeared within a short period as a flush. Subsequently, few new leaves appeared. The mean number of leaves produced on a shoot was 4 4 ± 2 0 (n = 228). Leaves were retained until August, then turned yellow and had all fallen by the end of October (Fig. 1c). Mean leaf longevity was 157 ± 29 0 days (n = 998). Changes in leaf-age structure with time in Fagus were similar to those in Polygonatum. Ages increased with time, but the width of the age distribution was narrow (Fig. 2g i). Bud break of Alnus was observed in early April. The first leaf appeared on a shoot in mid-april, then leaves appeared successively. The total number of leaves produced on a shoot averaged 15 0 ± 5 4 (n = 40), which was significantly greater than for Fagus (t = 21 9; P < 0 001). On the lower shoots, new leaf emergence stopped by August or September, but on the terminal shoot it continued until early November. From mid- June leaves at the lower position on shoots started to fall (Fig. 1d). The number of leaves attached to the shoot reached approximately five in early June, was maintained until early November, and then declined. Mean leaf longevity was 69 4 ± 26 0 days (n = 600), which was significantly shorter than for Fagus (t = 60 7; P < 0 001). Leaf-age structures of Alnus were essentially the same within the season. At any time in the season, leaves in the youngest age class were

5 33 Leaf emergence patterns and photosynthesis Fig. 2. Leaf-age structures at different times in the growing season of two herbaceous and two woody species. Polygonatum odoratum var. maximowiczii: (a) 4 June; (b) 7 July; (c) 13 August Polygonum sachalinensis: (d) 9 June; (e) 13 July; (f) 19 August Fagus crenata: (g) 21 May; (h) 29 July; (i) 14 August Alnus sieboldiana: (j) 4 June; (k) 3 July; (l) 14 August Fig. 3. Histograms of shoot angles for two herbaceous and two woody species. (a) Polygonatum odoratum var. maximowiczii; (b) Polygonum sachalinensis; (c) Fagus crenata terminal shoot; (d) Fagus crenata lateral shoot; (e) Alnus sieboldiana terminal shoot; (f) Alnus sieboldiana lateral shoot. present. The proportion of old leaves increased slightly with time (Fig. 2j l). SHOOT ANGLE Shoot angles from the vertical line ranged from in Polygonatum (Fig. 3a). Mean shoot angle was 41 6 ± 13 2 (n = 41). At the time of shoot emergence, the shoot became arched and displayed flowers at the base of petioles. Shoot angles of Polygonum ranged from 0 40 (Fig. 3b) with a mean angle of 17 ± 8 5 (n = 45). In comparison with Polygonatum, the shoot angle of this species is small and the difference in shoot angle between the two herbaceous species was significant (t = 10 1; P < 0 001). In July the shoots of this species extended branches at the terminal tip. At this point the shoot angle in this species became greater and the architecture became more complex.

6 34 K. Kikuzawa Shoot angles of Fagus ranged from The terminal shoot (Fig. 3c) and lateral shoots (Fig. 3d) had a similar inclination. The mean angle was 71 2 ± 16 2 (n = 38). The angle of the terminal shoot of Alnus ranged from 0 15 (Fig. 3e). The mean angle was 11 4 ± 5 0 (n = 5), elongating upwards. Inclusion of lateral shoots did not greatly increase the shoot angle. Ranges were <60 and the average was 39 ± 7 3 (n = 20; Fig. 3f). The mean height growth within a season for Polygonatum was 37 8 ± 17 3 cm (n = 41), while that of Polygonum was 106 ± 42 0 cm (n = 45) (t = 9 6; P < 0 01). This difference was due partly to the arched shoot form of Polygonatum, but mainly to the longer growth period of Polygonum because of successive leafing. The mean height growth of Fagus was 7 5 ± 4 3 cm (n = 8), while that of Alnus was 78 8 ± 20 0 cm (n = 5). The difference between the two species was significant (t = 9 9; P < 0 001). RELATIVE PHOTON FLUX DENSITY Differences in RPFD among leaf orders were not significant in Polygonatum (two-way ANOVA, P > 0 05) or Fagus (two-way ANOVA, P > 0 05) (Fig. 4a,c). The trend did not change with time. In contrast, RPFDs on higher leaves of Polygonum and Alnus usually exceeded those on lower leaves (Fig. 4b,d). The difference in RPFD among leaf orders was usually significant in Polygonum (two-way ANOVA, P < 0 05) and Alnus (two-way ANOVA, P < 0 01) except at the initial stage of shoot elongation. For Alnus, in June the sixth and seventh leaves received more than 90% of full sunlight, while in August the 11th and upper leaves received full sunlight, and in September the 13th and upper leaves received full sunlight. Lower leaves usually received less sunlight. In short, there were gradients in PFD across leaf positions. The gradient shifted toward higher positions with time as the lower leaves were shed. PHOTOSYNTHETIC RATES Potential photosynthetic rates (P max ) of each leaf showed a similar vertical trend to that of RPFD. In Polygonatum and Fagus, P max was not substantially different among leaves of different positions (Fig. 5a,c), but the rate decreased with time probably due to leaf ageing. No significant differences in the two species were found among leaf orders by two-way ANOVA, except in August when distal leaves senesced early. Fig. 4. Mean (± SE) of relative photon flux density (RPFD) on leaves of different leaf order at different points in the 1993 season in two herbaceous species, and in the 2000 season in two woody species. Differences in RPFD among shoots and leaf orders were tested by two-way ANOVA. (a) Polygonatum odoratum var. maximowiczii: 2 June (F = 1 717; 0 2 < P < 0 5); 29 June (F = 1 65; 0 2 < P < 0 5); 7 August (F = 1 207; 0 5 < P). (b) Polygonum sachalinensis: 2 June (F = 7 60; P < 0 01); 29 June (F = 4 37; P < 0 01); 24 July (F = 2 21; 0 01 < P < 0 05). (c) Fagus crenata: 5 May (F = 0 365; 0 5 < P); 4 June (F = 0 296; 0 5 < P); 30 July (F = 1 06; 0 5 < P). (d) Alnus sieboldiana: 21 May (F = 40 9; P < 0 01); 18 June (F = 43 21; P < 0 01); 30 July (F = 7 49; P < 0 01); 10 September (F = 5 42; P < 0 01).

7 35 Leaf emergence patterns and photosynthesis Fig. 5. Mean (± SE) of potential photosynthetic rate (P max ) of different leaf orders at different times in the 1993 season in two herbaceous species, and in the 2000 season in two woody species. Differences in photosynthetic rate among shoots and leaf orders were tested by two-way ANOVA. (a) Polygonatum odoratum var. maximowiczii: June 12 (F = 1 58; 0 05 < P); June 29 (F = 0 42; 0 5 < P); August 7 (F = 3 66; 0 01 < P < 0 05). (b) Polygonum sachalinensis: 12 June (F = 14 1; P < 0 01); 29 June (F = 10 97; P < 0 01); 24 July (F = 7 36; P < 0 01). (c) Fagus crenata: 24 June (F = 1 02; 0 5 < P); 2 July (F = 0 799; 0 5 < P); 6 August (F = 5 46; P < 0 01). (d) Alnus sieboldiana: 19 June (F = 16 9; P < 0 01); 5 August (F = 6 47; P < 0 01); 15 October (F = 6 02; P < 0 01). In Polygonum and Alnus, P max was usually greater in leaves at higher positions (Fig. 5b,d). Differences among leaf orders were significant (P < 0 01) except early in the season (May and early June in Alnus). Leaves of higher P max shifted towards a higher position with time. Light photosynthesis relationships of Alnus and Fagus were well described by the nonrectangular hyperbola (Fig. 6). The maximum photosynthetic rate at saturating light was approximately three times higher in Alnus than in Fagus. In lower light conditions, photosynthetic rate was higher in Fagus than Alnus. Dark respiration was greater in Alnus than in Fagus. Initial potential photosynthetic rates (P max ) of Polygonum and Alnus were as high as 15 µmol m 2 s 1 (Fig. 5b,d), but decreased quickly with time to less than half the initial rates within 30 or 40 days. Initial P max of Polygonatum and Fagus was less <10 µmol m 2 s 1 (Fig. 5a,c). However their rates declined slowly with time, becoming less than half the initial rates in 60 (Polygonatum) and 100 (Fagus) days. As all leaves appeared simultaneously within a short period in Fagus and Polygonatum, leaves in their canopies Fig. 6. Light photosynthesis relationships of Alnus sieboldiana ( ) and Fagus crenata ( ). The curves were approximated by the non-rectangular hyperbola: φi+ A φi+ A) 2 θφai} 05 {( 4 P(I) = R 2θ where P(I) is instantaneous photosynthetic rate as a function of photon flux density (I), and A, R, φ and θ are parameters. For Alnus (r 2 = 0 999), A = 20 1, φ = 0 05, θ = 0 861, R = 1 70; for Fagus (r 2 = 0 998); A = 6 62, φ = , θ = 0 865, R = 0 89.

8 36 K. Kikuzawa Fig. 7. Estimated photosynthetic rate (P est ) under measured PFD of leaves of each order (numbers attached on curves) in canopies of (a) Alnus sieboldiana; (b) Fagus crenata. P est was estimated using the light photosynthetic rate curve shown in Fig. 6 and measured PFD at each time point. behaved similarly. For example, in Fagus estimated photosynthetic rates under measured PFD (P est ) of all leaves increased slightly from April to July, reached a peak in July, then decreased linearly with time until September, and all the leaves were shed in October (Fig. 7b). In the successive species Alnus, leaves appeared at different times and decreased their photosynthetic rates (P est ) individually, because of ageing and the decrease in PFD (Fig. 7a). At any time in the season, a canopy consisted of leaves of different ages and photosynthetic performances (Fig. 7a). Discussion AVOIDANCE OF SELF-SHADING IN SPACE AND TIME Leaves on a vertically growing shoot suffered from mutual shading, creating gradients of RPFD from the distal to the basal part of a shoot, as seen in Polygonum and Aluns (Fig. 4b,d). A method of avoiding self-shading in the upright shoot is to differentiate the timing of appearance of each leaf. Kikuzawa et al. (1996) first pointed out that successive leafing is a method of avoiding self-shading in time. By placing newly emerged leaves in a position with better light conditions, the plant will achieve higher levels of photosynthesis than by placing all leaves at the same position throughout a season. By extending shoots vertically, taller plants can access more light and thereby obtain competitive advantages over neighbours (Givnish 1988). In contrast to successive-leafing species, simultaneousleafing species must adopt some means of avoiding selfshading in space. Plant architecture is considered to be an adaptive design to receive light effectively by avoiding self-shading (Takenaka 1994; Ackerly & Bazzaz 1995b; Hikosaka & Hirose 1997; King et al. 1997; Yamada et al. 2000). Inclined shoots, adopted by the two simultaneous-leafing species in this study, provide another method of avoiding self-shading in space. There was little difference in RPFD among leaf orders at any time in the growing season (Fig. 4a,c). Thus light conditions on a single leaf were essentially the same throughout a season. In forest understoreys some trees invest resources to extend vertical growth, while others extend lateral growth (Kohyama 1987; King 1990). These are considered different strategies to avoid self-shading and receive sunlight effectively. Even within the same species, plastic changes in architecture under different light conditions are observed (Valladares & Pearcy 1998; King 2001). In some sunlit environments, however, vertical shoots with steeply inclined leaves in

9 37 Leaf emergence patterns and photosynthesis a spiral phyllotaxy with short internodes may be an adaptation to minimize photoinhibition (Valladares & Pearcy 1998). LEAF LONGEVITY AND PHOTOSYNTHESIS In the two successive species Alnus and Polygonum, there were gradients in P max as well as PFD from the top to the bottom, while few gradients were observed in the two simultaneous species Fagus and Polygonatum. Ackerly & Bazzaz (1995a) found gradients of photosynthetic capacity coupled with the gradients in PFD of successive-leafing, tropical pioneer species. Mooney et al. (1981) compared gradients of maximum photosynthetic rates of several annual plant species, together with gradients in leaf nitrogen contents and leaf mass per area. The gradients should be considered in relation to nitrogen translocation and leaf longevity (Ackerly 1999; Westoby, Warton & Reich 2000). The translocation of nitrogen from leaves at darker places in the canopy to those at upper, brighter positions will maximize canopy photosynthesis (Ackerly & Bazzaz 1995a; Mooney et al. 1981; Field 1983; Field & Mooney 1983; Hirose & Werger 1987). The P est of Alnus declined quickly (Fig. 7a), possibly due to degrading PFD with time (Hikosaka, Terashima & Katoh 1994), in addition to the effects of N translocation and ageing. Leaf longevity of this species was short. P est of the simultaneous species was relatively lower than that of successive species and was not affected by the changes in light conditions, but declined slowly with the effects of leaf ageing (Fig. 7b). Hence leaf longevity was relatively long. There is a trade-off between high photosynthetic rate and maintenance of rates for a long period. Thus there are negative correlations between leaf longevity and maximum photosynthetic rate (Chabot & Hicks 1982; Kikuzawa 1989; Kikuzawa 1991; Reich et al. 1991, 1992), and between leaf longevity and specific leaf area (Westoby et al. 2000). COMPARISON OF CANOPY-LEVEL PERFORMANCE Although many more leaves were produced in a growing season by successive species than by simultaneous species, the number of leaves actually attached to the shoot was not substantially different between the species of each form (Fig. 1). The difference between the two types of plant is therefore not in the number of leaves actually attached to the shoot, but in the way the leaves are produced and displayed. In the simultaneous species the initial number of leaves is maintained through the growing period, thus leaves become older with time, and the trend in photosynthetic rate of the entire leaf population is the same as that of a single leaf (Fig. 7b). In contrast, in the successive species leaves are replaced within the growing period, thus the age structure of a leaf population is nearly the same throughout the season (Fig. 2); the leaf population is always composed of young leaves. Thus photosynthetic gain by leaf populations does not decrease with time, but remains high as leaves are replaced, although P est of a single leaf decreases with time. The advantage in successive species is the maintenance of a higher photosynthetic rate throughout the season by always recruiting new leaves. However, successive species must produce many more leaves overall, compared to simultaneous species. Production of more leaves will incur a nitrogen cost as nitrogen is translocated from senescing leaves. Concomitantly, these species must pay for the supporting tissues of these leaves. The high cost of production of more leaves and of supporting tissues in successive species will be offset by their advantages in high photosynthetic rate and height growth. They can attain height growth by vertical elongation of the terminal shoot. Such a method of active height growth can be attained in an environment with high light availability. If, for example, light is limited, the potential high photosynthetic rate of successive species cannot be realized fully, and the advantage of this method will be reduced. In addition to successive leafing, other traits such as higher P max and short leaf longevity are characteristics of species in resource-rich sites (Kikuzawa 1995). Height growth in simultaneous species is limited only to the initial flush at the start of the growing season. Moreover, the shoot of simultaneous species is usually inclined, which reduces height growth further. Horizontally extending shoots could be a means of effectively receiving diminishing sunlight in darker conditions. Other traits, such as longer leaf longevity and low light-utilizing photosynthetic traits (Fig. 6), are characteristic of species in resource-limited sites such as the forest understorey. Acknowledgements I thank Hiromi Kikuzawa for her encouragement and support in the fieldwork. Field assistance by Hiroyuki Shirakawa is also acknowledged. David Ackerly, Martin Lechowicz, Maki Suzuki, Yoshiyuki Miyazawa and Kiyoshi Umeki offered useful comments. I also thank anonymous referees for their comments. This work was supported by the Japanese Ministry of Education and Science # and # References Ackerly, D.D. (1999) Self-shading, carbon gain and leaf dynamics: a test of alternative optimality models. Oecologia 119, Ackerly, D.D. & Bazzaz, F.A. (1995a) Leaf dynamics, selfshading and carbon gain in seedlings of a tropical pioneer tree. Oecologia 101, Ackerly, D.D. & Bazzaz, F.A. 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