1590
Branching, biomass distribution, and light capture efficiency in a pioneer tree, Rhus trichocarpa, in a secondary forest Noriyuki Osada
Abstract: Crown architecture and biomass distribution patterns were investigated in relation to branching and tree size in a pioneer species, Rhus trichocarpa Miq. (Anacardiaceae), in a Japanese secondary forest. Crown architecture changed with tree size and with branching. Crown depth and area were greater in taller trees. In addition, branched trees had crowns of greater depth, and crown area increased more rapidly with increasing height in branched trees as compared with unbranched trees. In contrast, biomass distribution to nonphotosynthetic and photosynthetic organs changed only with tree size and was similar in unbranched and branched trees of similar size. Light capture efficiency was related to neither height nor branching status for trees with heights of 1–2.5 m. Coexistence of unbranched and branched trees at the height around the onset of branching is possible because these trees realize similar biomass distribution patterns and light capture efficiencies. Individual leaf area and leaf area index increased with tree size in unbranched trees but decreased with tree size in branched trees. These results suggest that several leaf clusters of limited size are sparsely arranged in a large threedimensional space in tall trees. Key words: allometry, crown architecture, individual leaf area, leaf area index, onset of branching, tree height. Re´sume´ : L’auteur a e´tudie´ l’architecture du houppier et les patrons de distribution de la biomasse en relation avec la ramification et la dimension des arbres, chez une espe`ce pionnie`re, le Rhus trichocarpa Miq. (Anacardiaceae), dans une foreˆt secondaire du Japon. L’architecture du houppier se modifie selon la grosseur de l’arbre et la ramification. La profondeur du houppier et sa superficie sont plus importantes chez les grands arbres. De plus, les arbres ramifie´s ont des houppiers plus profonds, et la surface des houppiers augmente plus rapidement avec l’accroissement en hauteur chez les arbres ramifie´s, comparativement aux arbres non-ramifie´s. Au contraire, la distribution de la biomasse aux organes photosynthe´tiques et non- photosynthe´tiques change seulement selon la dimension de l’arbre, et est semblable chez les arbres ramifie´s ou non-ramifie´s de meˆme dimension. L’efficacite´ de la re´ception de la lumie`re est relie´e ni a` la hauteur ni a` l’e´tat de la ramification, chez les arbres de 1–1,25 m de haut. La co-existence d’arbres ramifie´s et non-ramifie´s, environ a` la hauteur ou` de´butent les branches, pourrait eˆtre possible parce que ces arbres ge´ne`rent un patron de distribution similaire de la biomasse et d’efficacite´ de la re´ception de la lumie`re. La surface des feuilles individuelles et l’index de surface foliaire augmentent avec la grosseur de l’arbre, chez les arbres non-ramifie´s, mais diminue avec la grosseur chez les arbres ramifie´s. Ces re´sultats sugge`rent que plusieurs faisceaux foliaires, de dimension limite´e, sont parcimonieusement distribue´s selon un large espace tri-dimensionnel chez les grands arbres. Mots cle´s : allome´trie, architecture du houppier, surface foliaire individuelle, index de surface foliaire, de´but de ramification, hauteur des arbres. [Traduit par la Re´daction]
Introduction Woody plants are characterized by sequential development of aboveground structures according to a geometric configuration (Room et al. 1994). With increasing tree size, complex crown architecture is formed through ramification (Halle´ et al. 1978; Ku¨ppers 1989; Farnsworth and Niklas Received 27 June 2005. Published on the NRC Research Press Web site at http://canjbot.nrc.ca on 14 February 2006. N. Osada.1,2 Laboratory of Forest Ecology, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan, and Graduate School of Life Sciences, Tohoku University, Aoba, Sendai 980-8578, Japan. 1Corresponding
author (e-mail:
[email protected]). address: Graduate School of Life Sciences, Tohoku University, Aoba, Sendai 980-8578, Japan.
2Present
Can. J. Bot. 83: 1590–1598 (2005)
1995). As self-shading limits the number of leaves that can be supported by a single branch, branching is considered an important strategy to increase foliar area and enhance light interception at the tree crown level (Honda and Fisher 1978; Alvarez-Buylla and Martinez-Ramos 1992; Sterck and Bongers 2001), as well as to grow and exploit space in competition with surrounding plants (Jones and Harper 1987; Ku¨ppers 1989). Consequently, trees have crown architectures that are typical for each species as a result of genetically determined growth rules and different responses to environmental factors (Halle´ et al. 1978; Bell 1991). Because of such growth patterns, a woody plant must produce new nonphotosynthetic supporting organs to produce new leaves, and the turnover rate is much faster in the latter (Halle´ et al. 1978; Givnish 1988). The biomass of nonphotosynthetic organs therefore increases more rapidly than that of photosynthetic organs, resulting in a decrease in the leaf
doi: 10.1139/b05-133
#
2005 NRC Canada
Osada
mass fraction (LMF; total leaf mass per total aboveground mass) and leaf area ratio (LAR; total leaf area per total aboveground biomass) with increasing tree height (Shukla and Ramakrishnan 1984; Givnish 1988). Since an increase in branch number may be necessary to increase the foliar area and mass of the crown, branching may also affect biomass distribution patterns. Alternatively, changes in leaf size with increasing height may compensate for the limited number of leaves maintained by a single branch. Various species are known to change leaf size with ontogeny (Alvarez-Buylla and Martinez-Ramos 1992; Thomas and Ickes 1995; Yamada et al. 2000, 2005; Reich et al. 2004). Tree species generally have a specific height at the onset of branching (King 1998), and various studies have related leaf size to the onset of branching: leaf size gradually becomes larger with increasing tree height during a monopodial phase, and decreases once branching occurs (Alvarez-Buylla and Martinez-Ramos 1992; Yamada et al. 2000, 2005). Alvarez-Buylla and Martinez-Ramos (1992) showed that the slope of the relationship of total leaf area to tree height was similar between unbranched and branched trees of Cecropia obtusifolia, irrespective of differences in individual leaf size. However, these studies did not focus on biomass distribution because of the difficulty in measuring the biomass of tall trees. It is thus of interest to investigate whether biomass distribution patterns change with tree height and branching in a similar manner. In general, both unbranched and branched trees of similar heights coexist at the height around the onset of branching. This further brings about the question of whether these coexisting trees realize similar biomass distribution patterns and light capture efficiency irrespective of the branching status. Based on these views, crown architecture and biomass distribution patterns were investigated in relation to tree size and branching status in a pioneer species, Rhus trichocarpa Miq. (Anacardiaceae), in a warm–temperate forest in Japan. Rhus trichocarpa is a small tree species that grows up to ca. 6–8 m in height. Pioneer trees generally regenerate in high light environments and grow without experiencing shaded conditions (King 1994; Ackerly 1996), suggesting the importance of crown architecture and biomass distribution patterns in rapid height growth and efficient display of leaf area by branching throughout the life span of this species. I hypothesized that, although biomass distribution pattern changes with tree size, biomass distribution and light capture efficiency are similar between unbranched and branched trees of similar heights at the onset of branching.
Materials and methods Study site and species The study was conducted at the Kamigamo Experimental Forest Station, Kyoto University (35804’N, 135846’E), near the northern limits of the warm–temperate zone. Both evergreen and deciduous tree species coexist in this forest, which consists mainly of secondary forest dominated by Quercus serrata Thunb. ex Murray, Quercus glauca Thunb. (Fagaceae), Ilex pedunculosa Miq. (Aquifoliaceae), Pinus densiflora Siebold et Zucc. (Pinaceae), and Chamaecyparis obtusa (Siebold et Zucc.) Endl. (Cupressaceae). Most of the canopy is 10–12 m in height (N. Osada and K. Kawamura,
1591
unpublished data). The main component species and their flowering phenologies at this study site were described by Osada et al. (2003). Rhus trichocarpa is a small deciduous tree that grows up to ca. 6–8 m in height. This species produces large compound leaves with few orthotropic branches of large crosssectional area, allowing for the whole branch and crown architecture to be analyzed easily (Fig. 1). The leaves are arranged in a flat plane at the apex of each current-year shoot, and self-shading among leaves is minimal within a currentyear shoot. Terminal buds often die, and branches are then produced sympodially (Fig. 1). Even the monopodial trees of nearly 1 m in height produce inflorescences laterally without branching. This species is abundant in temperate secondary forests of Japan (e.g., Kamitani et al. 1998; Osada 2005). Crown architecture and biomass distribution patterns A 30 m 50 m plot was established in the study area. This plot was part of the young secondary forest described by Kawamura and Takeda (2002). All R. trichocarpa >0.5 m tall inside this plot were marked, and tree height, diameter of the main trunk at 10% of the height, and the width and depth of each crown were measured. Widths were measured at the widest part of the crown and perpendicular to it. The projected area of the crown was calculated as an ellipse based on these two measurements. Crown depth was calculated as the depth from the lowest point on the lowest leaf to the highest point on the highest leaf. At the same time, the numbers of branches and leaves were counted. Furthermore, the lengths of the rachis and petiole of all leaves were measured for all trees 0.5–3 m tall and subsampled in trees >3 m tall. To measure these traits for trees >3 m tall, ladders were attached to neighboring canopy trees. In August 2000, tree height and trunk diameter were measured in a similar way for 23 trees of various heights (0.6– 8.2 m) outside the plot, and these trees were harvested to measure the total stem biomass after drying at 70 8C. Based on these samples, allometric equations were constructed to estimate the total stem biomass from diameter and height: ½1
mT ¼ 0:377ðdT2 hT Þ0:956
r2 ¼ 0:996
where mT, dT, and hT are the total stem dry mass (g), diameter (cm), and tree height (cm), respectively. Because allometric relationships were similar between unbranched and branched trees of similar height, the same equation was used irrespective of differences in branching status. Furthermore, 30 leaves were randomly collected, the lengths of the rachis and petiole were measured, and leaf area was calculated by using the image analysis software NIH image (National Institute of Health, Maryland, USA) for digitized data of photocopies of the leaves. Mass of the leaf petiole plus rachis was then measured after drying: ½2
aL ¼ 0:3068ðlR2 Þ0:989
½3
mPR ¼ 0:00004ðlPR Þ2:53
r2 ¼ 0:944 r2 ¼ 0:908
where aL, lR, mPR, and lPR are individual leaf area (cm2), length of the rachis (cm), dry mass of the petiole plus rachis (g), and length of the petiole plus rachis (cm), respectively. #
2005 NRC Canada
1592
Fig. 2. Crown architecture of Rhus trichocarpa. Tree height versus trunk diameter at 10% height (A), crown depth in relation to tree height (B), and crown area in relation to tree height (C). Filled and open circles indicate unbranched and branched trees, respectively. o 800 A o o o ooo oooooooo o o •ooo o o •o •o•••o•oo••ooooo•ooo o •••o••ooo•ooo••ooo•oo o o • • o • • •• • •o•••o•••••o•o•• •o • 100 • • •• o••••••o••o••• •• • o • • •••••• o
Tree height (cm)
Fig. 1. Rhus trichocarpa of different heights. The upper panel shows a tree with a height of 0.5 m. The middle panel shows the branching patterns of a tree that is 3.5 m high. The arrows indicate the death of terminal buds. The lower panel shows the branches of tall trees (about 6 m high) expanding in the direction of high light.
Can. J. Bot. Vol. 83, 2005
• • •••••••• •
40 0.2
Crown depth (cm)
1000
10
B o o o ooo o o o oo o ooooooo o o o o o o o ooo ooo oo oo o o o • o oo• • •oo o o • •• • • o o• •o• •o•• • •• •• •••o••o•oo•••o • •••••••••o••ooo• o ••• • • ••• •••• •••••o••••••• •• • •• o•• • • • • • •
100
10
• •• • •••• • • • •••••• •• • •• 1 40 100 30 10
Crown area (m 2)
1 Diameter (cm)
o
800
C o
o
o
o
o o o o oo o o ooo ooo ooo o o o o • o o•oo•oo••o•••o•o•oo••o•o •o • • o •o••oo •o o• • • • • •• •••••oo•••••••••o••••••oo•••ooo••o• •• ••o• o• • o •••• ••••••••o••o•o ••• • •
1 0.1
• •• • ••
0.01 40
To convert leaf area to leaf mass, two to three leaflets were collected from trees inside the plots. The area and dry mass of each leaflet were measured, and the mean specific leaf area (SLA) was calculated for each individual tree.
100 Tree height (cm)
800
Light environment Seventy-eight trees 1.0–2.5 m tall were randomly selected inside the plot, and hemispherical photographs were taken above the apex of these trees in the fall of 2000 with a CoolPix 910 digital camera with an FC-E8 fisheye converter (Nikon, Tokyo, Japan). At this time, canopy leaves were still stable and had not senesced. An indirect site factor (ISF) was calculated with Hemiview ver. 2.1 (Delta-T Devices, Cambridge, UK). The ISF represents the proportion of dif#
2005 NRC Canada
Osada
1593 Table 1. The results of standard major axis regression analyses between the traits of crown architecture (log X and log Y). X
Y
All data included Diameter Height Crown depth Crown area Height
Crown depth Crown area
Group
n
R2
Slopea
95% CIb
Intercept
Pc
Unbranched Branched Unbranched Branched Unbranched Branched Unbranched Branched Unbranched Branched
114 63 114 63 114 63 114 63 114 63
0.80 0.92 0.16 0.70 0.55 0.84 0.20 0.66 0.61 0.77
1.17*** 0.87*** 1.75*** 1.54*** 1.86*** 1.68*** 1.50*** 1.77*** 1.60*** 1.94***
1.07–1.27 0.81–0.93 1.48–2.08 1.33–1.77 1.64–2.11 1.52–1.86 1.27–1.78 1.53–2.06 1.42–1.79 1.72–2.19
2.24 2.20 1.09 1.36 –0.49 –0.54 –2.28 –2.54 –4.07 –4.81
0.001
86 45
0.54 0.64
1.65*** 2.27***
1.42–1.91 1.89–2.73
–4.20 –5.52
Trees with heights of 0.7–3.0 m Height Crown area Unbranched Branched
0.25 0.19 0.13 0.027
0.010
a
***, statistical significance at P < 0.001. Confidence interval. c P values of the test for the common slope between groups. b
Fig. 3. Relative frequency distribution of light level (indirect site factor (ISF)) for unbranched and branched Rhus trichocarpa trees with heights of 1.0–2.5 m.
0.6 0.5 0.4 0.3 0.2 0.1 0
0
10
20
30
40
50
0
10
20 30 ISF (%)
40
50
0.6 0.5 0.4 0.3 0.2 0.1 0
fuse (indirect) solar radiation reaching a given position relative to an open site. Analyses of allometry and architecture Allometric relationships were examined for tree height, crown depth, and crown area in relation to trunk diameter, and crown depth and area in relation to tree height. In addition, the biomass of photosynthetic organs (i.e., leaflets; hereafter referred to as ‘‘leaf mass’’), total leaf area, mean individual leaf area, and standing leaf number were related to tree height and the biomass of nonphotosynthetic organs (stem, petiole, and leaf rachis; hereafter referred to as ‘‘stem mass’’). All variables were log-transformed. Standard major axis (SMA) slopes were calculated, because the purpose was to summarize the relationship between pairs of variables, rather than generating equations for predicting Y from X. The SMA slopes of unbranched and branched trees were compared using the program (S)MATR (version 1, D.S. Falster,, D.I. Warton, and I.J. Wright http://www.bio. mq.edu.au/ecology/ SMATR). To compare observed relationships between groups, I tested for statistical differences in the slope and intercept of group SMA relationships. Tests for homogeneity of slopes and calculation of common slopes used a likelihood ratio method (Warton and Weber 2002). The ability to calculate common slopes allows one to test for elevation (intercept) differences between groups, as in standard analyses of covariance (ANCOVA). Where nonheterogeneity of slopes was demonstrated, I tested for elevation shifts in SMAs between groups by transforming slopes such that the common slope was 0 (Y’ = Y – bX, where b is the common slope) and then testing for differences in group mean Y’ with t tests (Wright et al. 2002). Light capture efficiency Light capture efficiency was calculated for the 1.0–2.5 m tall trees in which light environment could be measured. Effective leaf area was first calculated as the product of total leaf area (cm2) and light environment (indirect site factor; #
2005 NRC Canada
1594
Can. J. Bot. Vol. 83, 2005
Fig. 4. Leaf traits and biomass distribution with respect to tree size in Rhus trichocarpa. Total leaf number, mean individual leaf area, total leaf area, and total leaf mass in relation to tree height (A, B, C, D) and to stem mass (E, F, G, H). Filled and open circles indicate unbranched and branched trees, respectively. 1000 1000
A
100
Leaf No.
E
o oo o o o o o o o o ooo o o o o oo o o o ooo o o o oooo ooooo o o o•oo•o o•••o•oo o•••o• •o• • • • o ••••••••o••o••••o••••••••••o••••••••oo••• •• •• • •
10
• • • •• •
•
100 10
1
Mean leaf area (cm 2 )
1000
100
800
1 1000
B •••• • • o• •• ••••o• o•o • o••••••••oo•o•oooooo • • • • • •••••••••••o•••••ooo•oo•ooo•o• ooooo o o • ••••o•o•o• ••••• oo••o•o oo o •• •••••••••ooo••• • • o • ••
100
o ooooo o
10
100
1000
10000
F • •••o••• • o • • • • • • • ••••••oo••o•o•oooooo o o o ooooo • • • •••••o•o• •oooo oo oo o •••••o••o•••o••o••o•••o•oo••ooooo•o• oo o ••• • •• o ••• ••o••••o•• • •
100
10
o
10 40
50000
100
800
C oo o o o • oo •oooo o o • • • oo•oo•ooo••o•o••ooo•oo••o •o • o o • • • • • •• o••o• • •••o•••••••••••o•o••o••••o•••••oo••oo••• • • • • • • • •• •o••o•o• ••••• •
10000 1000
• • •••• • • • ••
100 50 40 200 100 Total leaf mass (g)
•• •• • • •
1 40
Total leaf area (cm 2 )
o oo o o o o ooo o o o o oo oooooooooo o o ooo o ooooooo o o oo o o oo••oo•• •• • •o • o• •••••o•••o o •• • ••• •••••• ••••o•••o••o••••••o•••••••
800
• oo o • o •ooo•oo••o••o•oo•o•oo o••o o • •• •o••••ooo••oooo•o o•o•• • • • • • o o • • • •• ••••o••••••o••••o•o•• o•o•• ••••••••o••o••• •• • • • o• • • ••••• •• •
0.2 40
10000
100 Tree height (cm)
1
0.2
Crown architecture The slope of the SMA regression line between tree height and trunk diameter was steeper in unbranched trees than in
1000
ooo• oo • o•o••ooo••oo••o••oo•oooo o • • •••••••oo•o•••o•ooo•oo•• o ••o•• o•• • • •••••••o•••o•••o•• ••o o o • • • ••••••oo•••o •• • • • • • • •• • • •
1
Results
100
o o
10
ratio) of the trees. Accordingly, the effective leaf area was greater for the trees of higher light, even for the trees that had similar total leaf area. Light capture efficiency was then calculated by dividing the effective leaf area by the stem mass (support mass) of trees.
10
H
o o o o
800
1000
10000
• •• ••••••• • • • • •
200 100
ooo
100
o o o o o o o ooooo••ooooo o o o oo • • oo••o•oo•oo•ooo • ••••••oo••o•oo••o•o• • •••••••o••o•o•o••o•o• •••••o•o••o••o•o•••• ••
1000
100
10
G
100 50
oo
1
50000
o o oo o o o
•
D
10
1
1
10
oo
10000 o
o oo o
100 1000 Stem mass (g)
10000
branched trees (Fig. 2). The slope was >1 in unbranched trees but 1 in the log-log relationship, because leaf number was strongly correlated with branch number in a tree (r = 0.99, P < 0.001). In contrast, the slopes were less steep in branched than in unbranched trees for the relationships of mean individual leaf area to tree height and stem mass (Table 2; Fig. 4). Slope was significantly steeper than 1 in unbranched trees, and the maximum individual leaf area was observed in unbranched trees (Fig. 4). As a result of these relationships, the slope of total leaf area against tree height was similar in unbranched and branched trees (Table 2; Fig. 4), and the intercept of this relationship also did not differ (F = 0.77, P = 0.38). The slope of total leaf area against stem mass was slightly but signifi#
2005 NRC Canada
1596
Can. J. Bot. Vol. 83, 2005
Fig. 5. Leaf area index (LAI) in relation to tree height (A) and stem mass (B) in Rhus trichocarpa. Filled and open circles indicate unbranched and branched trees, respectively.
1.2
o o o ooo o •• • •ooooooo••o o • • • • •o••••o•••o•••ooo•• o • o•• • • •••••oo•• o••o• oo •••••• ••o •o o • • •••••••••••••••o••• o•••o••• o • o o • • • o•o• •o••• • •• •• •• •o• o o
1 LAI (cm 2 /cm2 )
1.2
A
0.8 0.6 0.4
••
0.2
•
B oo o o o oo•o• • • o o• ooo•ooo o • •• • • •o•••••o•••ooo•• o o o • o• ••••••o••••o •••o o oo o o o • • • o • •••• o o o ••••• ••o••o • •o •••••o•••••o• •••••o•• • • oo o •• •••o o o
1 0.8 o
o
o
0.6
o oo o
0.4
•
•• •
0.2
0
•
•
0 40
100 Tree height (cm)
800
1
10
100 1000 Stem mass (g)
10000
Table 3. The results of standard major axis regression analyses between the traits of biomass allocation (log X and log Y). X Height
Y Effective leaf area Light capture efficiency
Group Unbranched Branched Unbranched Branched
n 49 29 49 29
R2 0.562 0.461 0.001 0.008
Slopea 3.81*** 3.86*** ns ns
95% CIb 3.14–4.63 2.90–5.14
Intercept –5.845 –5.958
Pc 0.939
a
***, statistical significance at P < 0.001; ns, not significant at P > 0.10. Confidence interval. c P values of the test for common slope between groups. b
cantly steeper in unbranched than in branched trees (Table 2), although this difference disappeared when trees of similar stem mass (5–200 g) were compared (Table 2). Taller trees had a proportionately larger total leaf area (slope >1), but trees of greater stem mass had a proportionately smaller total leaf area (slope
