J For Res (2005) 10:51–55 DOI 10.1007/s10310-004-0095-x
© The Japanese Forest Society and Springer-Verlag Tokyo 2005
SHORT COMMUNICATION
Akira Mori · Hiroshi Takeda
Changes in shoot properties in relation to vertical positions within the crown of mature canopy trees of Abies mariesii and Abies veitchii
Received: September 16, 2003 / Accepted: March 29, 2004
Abstract We investigated current shoot properties in two contrasting vertical positions (leader crown; LC, and lower branch; LB) within the crowns of mature trees of two subalpine conifer species, Abies mariesii and A. veitchii. For both LCs and LBs, shoot length decreased with increasing branching order. However, shoot properties were different between LCs and LBs. Shoots in LCs had more needle biomass per unit of shoot length. Shoots in sunny conditions pack needles closer along the shoot and intercept incoming light more completely. This causes the shoots in the LCs to have more needles. In contrast, less needle packing per unit shoot length in LBs results in the avoidance of mutual shading among needles in order to intercept limited light more effectively. Because branch systems in lower layers tend to be more shaded, the quantity of irradiance received by the shoots in LBs is smaller. Thus, reduced needle amounts on the shoots in LBs reflect the needle arrangement acclimating to the lower light availability. This study suggests the importance of changes in the properties of individual shoot as a component of a branch system and accordingly a whole-crown system in mature canopy trees of A. mariesii and A. veitchii. Key words Biomass allocation · Branch system · Crown maintenance · Current shoot · Needle arrangement
Introduction Tree crowns, which provide the framework for leaf display, are composed of repetitive productions of shoots (Kellomäki and Strandman 1995; Takenaka 2000). Patterns
A. Mori (*) · H. Takeda Laboratory of Forest Ecology, Division of Environmental Science and Technology, Graduate School of Agriculture, Kyoto University, Oiwake-cho, Kitashirakawa, Sakyo-ku, Kyoto 606-8502, Japan Tel. 81-75-753-6080; Fax 81-75-753-6080 e-mail:
[email protected]
of crown formation and maintenance are therefore determined by the property of each of the constituting shoots. Shoot properties such as leaf arrangement within the shoots and biomass allocation patterns are known to be affected by environmental factors such as light regimes (Sprugel et al. 1996; Stenberg 1996; Stenberg et al. 1998; Takenaka 2000; Mori and Takeda 2004b). Within the complex structure of a crown, light availability for each shoot is spatially heterogeneous (Kellomäki and Strandman 1995). The leader part of the crown that is not shaded by its neighbors receives high irradiance, whereas light availability in lower parts of the crown tends likewise to be lower, due to self- and neighbor-shading. Therefore, the spatial position in which each shoot is localized is the crucial determinant of light availability for shoots (Kellomäki and Strandman 1995). Light regime significantly affects the properties of individual shoot (Sprugel at al. 1996; Mori and Takeda 2004b). Accordingly, shoot properties should differ greatly according to the spatial position within the tree crown. As a summation of the shoots that show different properties, tree crown would be structured and maintained. Crowns of conifer species generally consist of wellhierarchized branching systems (e.g., Kellomäki and Strandman 1995; Bégin and Filion 1999). Therefore, rather than at the level of the branching structures being strongly regulated by inherent growth rules, acclimation to the environmental conditions at each shoot level may be crucial for crown formation and maintenance in conifer species. This might be especially noticeable in the crowns of mature adult conifer trees, since they have complex, developed crown structures. In the subalpine region in central Japan, old-growth forests are characterized by evergreen conifer species (Franklin et al. 1979). Abies mariesii Masters and Abies veitchii Lindley are typical climax, codominant species in many of these mature forests (Franklin et al. 1979; Kohyama 1984). In the absence of catastrophic disturbances, their great dominance would continue to be maintained (Mori and Takeda 2004a). According to Kanzaki (1984), individual trees of A. mariesii and A. veitchii can
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survive for 200–300 years. However, little is known about how they can survive and persist in the canopy layer for decades and centuries. Here, by investigating the shoots constituting the crown of canopy trees, we can provide significant data relating to the persistence mechanisms of A. mariesii and A. veitchii individual trees in the canopy layer. In this study, we specifically focus on the properties of shoots located at two contrasting vertical positions within the crown of mature canopy trees of A. mariesii and A. veitchii.
LC Order 1 (Main trunk)
LB
Order 3 (Axis on Order 2)
Order 5 (Axis on Order 4)
Materials and methods
Order 2 (Main axis of lateral branch: Axis on Order 1)
Order 4 (Axis on Order 3)
Fig. 1. Diagram of data sampling from leader crown (LC) and lower branch (LB)
Study site The study site is located within a subalpine forest (altitude 2050 m, 35°56N, 137°28E) on Mt. Ontake (peak 3067 m) in central Japan. Mean annual precipitation is approximately 2500 mm and mean annual temperature is about 3–4°C. Snow covers the ground from mid-November or early December to late May or early June. The maximum snow depths from 1995 through 1999 in the study plot ranged from 175 to 230 cm. This forest mainly consists of four coniferous species; Abies mariesii Masters, Abies veitchii Lindley, Picea jezoensis var. hondoensis (Sieb. et Zucc.) Carrière, and Tsuga diversifolia (Maxim.) Masters, and one hardwood species, Betula ermanii Cham. (Mori and Takeda 2003a, 2004a). In the study plot, A. mariesii and A. veitchii comprised 82.4% of the relative density (Mori and Takeda 2003b). In the canopy layer (defined as height 18 m), the plot contained 79 stems/ha for A. mariesii and 69 stems/ha for A. veitchii. Attainable heights of these two Abies species exceed 27 m in this forest (Mori and Takeda 2003b). Data collection In May 1999, we selected canopy trees (individual trees that have reached canopy layer and overtopped neighbors at the upper part of crown) of A. mariesii and A. veitchii in the plot. For one canopy tree of each species, we harvested a leading section of the main trunk (about 150 cm in length, hereafter termed the leader crown (LC); Osada et al. 2002), and one leading section of a lower lateral branch that was sound and located at about 10 m below the leader crown (also about 150 cm in length, hereafter termed the lower branch (LB)) (Fig. 1). At harvest, no shoots had any signs of bud-break, which normally occurs in late June at this site. Two-dimensional diagrams were drawn to describe the branching structure of LCs and LBs. After this, we measured stem length, stem biomass, and needle biomass of all the youngest shoots (hereafter, current shoots; Mori and Takeda 2004b) within the LCs and LBs. All tissues were dried for 96 h at 40°C before weighing. In addition, branching order number of each current shoot was determined from the branching structure diagrams. In this study, the branching order was determined according to the method used in earlier studies (Bégin and Filion 1999; Sabatier and
Barthélémy 1999; Suzuki 2002), in which the main trunk was defined as the first-order axis; the main axis of lateral branches issuing directly from the main trunk was defined as the second-order axis; the axis directly attaching on the second-order axis was defined as the third-order axis; and so on (Fig. 1). Data analysis Total biomass of current shoots (bT) and needle weight ratio (NWR) were determined as: bT bS bN NWR bN bT
where bS and bN are the stem biomass and needle biomass on each shoot, respectively. Intraspecific differences in NWR were tested with the Mann-Whitney U test. To analyze the shoot structures in LCs and LBs, we used the following regression, which represents an allometric relationship: ln y a b ln x where x and y are any two components of shoot traits, and a and b are specific parameters determined from the reduced major axis (RMA) regression (Niklas 1994). Since both y and x variables have variation which derives from the measurement errors, RMA regression is more appropriate than the regression which minimizes sum of squares in the y-dimension only (Niklas 1994). Furthermore, we analyzed the differences in slope and/or intercept obtained from each RMA regression between LC and LB. First, we tested the homogeneity of slopes from the regressions in shoots of LC and LB. Then, if no significance was found, the interaction term can be excluded from the following analyses (Sokal and Rohlf 1995). This was tested using (S)MATR program version 1.0 (D.S Falster, D.I. Warton, and I.J. Wright, http://www.bio.mq.edu.au/ecology/SMATR). Differences in shoot length in relation to the branching order were tested with the Kruskal-Wallis test. In this study, all statistical analyses except for the RMA regressions were performed with SPSS software version 10.0.5 (SPSS, Chicago, IL, USA).
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Results Shoot length in relation to branching order Mean shoot length of current shoots on each branching order is shown in Fig. 2. In both A. mariesii and A. veitchii, shoot length was significantly different among the branching orders in both leader crown (LC) and lower branch (LB); shoot length decreased with increasing branching order. Stem and needle biomass in relation to shoot length In both A. mariesii and A. veitchii, stem and needle biomass of the current shoots increased with increasing shoot length (Fig. 3). For both species, RMA regression slopes of the allometric relationship between stem biomass ( y) vs. shoot
length (x) was significantly larger in the shoots of LCs than of LBs (Table 1). Additionally, regression intercepts of this relationship was larger in the shoots in LCs (Table 1). These results suggest that, within the observed results, stem biomass per unit shoot length tended to be greater in the current shoots of leader crowns than the shoots of lower branches (Fig. 3). For allometric relationships of needle biomass (y) vs. shoot length (x), RMA regression slopes were not significantly different but intercepts were significantly larger in the shoots of LCs than of LBs (Table 1), indicating that, within the crown of A. mariesii and A. veitchii canopy trees, current shoots in leader crowns had greater amount of needle biomass per unit shoot length than the shoots in lower branches (Fig. 3). For both A. mariesii and A. veitchii, the needle weight ratio (NWR) was significantly larger in the current shoots in
A. mariesii 14
ln Stem biomass (g)
A. mariesii
A. veitchii LC
LC
12
P < 0.0001
P < 0.05
0 -2 -4 -6
8
ln Needle biomass (g)
Shoot length (cm)
10
6 4 2 0 6
LB
LB
P < 0.05
P < 0.05
4
LC: R 2 = 0.88**** LB: R 2 = 0.57****
LC: R 2 = 0.87**** LB: R 2 = 0.81****
LC: R 2 = 0.61**** LB: R 2 = 0.56****
LC: R 2 = 0.69**** LB: R 2 = 0.73****
-8 2 0 -2 -4 -6 -8
2
-1
0
A. veitchii
2
2
3
4
5
2
3
4
0
1
2
3
-1
0
1
2
3
ln Shoot length (cm)
5
Branching order Fig. 2. Length of current-year shoots of A. mariesii and A. veitchii in relation to branching order in leader crown (LC) and lower branch (LB). Mean S.E. Differences were tested with the Kruskal-Wallis test
Fig. 3. Relationships between stem and needle biomass (y) vs. shoot length (x) in leader crown (LC) and lower branch (LB) of A. mariesii and A. veitchii. Open symbols LC, cross symbols LB. Solid lines indicate the RMA regression lines for LC, and dotted lines indicate the RMA regression lines for LB. Results of the RMA regressions are shown in Table 1. Significance levels: **** P 0.0001
Table 1. Summary of results of analysis which tested the differences in allometric relationships of current shoots based on the RMA regressions of the two layers (leader crown; LC and lower branch; LB) Species
Dimension Dependent variable (y)
Abies mariesii
Abies veitchii
Independent variable (x)
Stem biomass
Shoot length
Needle biomass
Shoot length
Stem biomass
Shoot length
Needle biomass
Shoot length
*** P 0.001; **** P 0.0001
Statistical value for difference between LC and LB Slope (b)
Intercept (a)
23.18***
–
3.01 14.07*** 2.33
238.19**** – 113.21****
Layer
LC LB LC LB LC LB LC LB
Results of RMA regression R2
N
Slope (b)
Intercept (a)
0.88**** 0.57**** 0.61**** 0.56**** 0.87**** 0.81**** 0.69**** 0.73****
110 76 110 76 116 101 116 101
2.37 1.56 1.65 1.38 2.26 1.83 1.95 1.73
4.85 5.59 2.86 3.54 5.48 6.21 3.52 4.06
54
A. mariesii 1
A. veitchii
P < 0.0001
P < 0.0001
NWR
0.8 0.6 0.4 0.2 0
LC
LB
LC
LB
Fig. 4. Needle weight ratio (NWR) in leader crown (LC) and lower branch (LB) of A. mariesii and A. veitchii. Mean S.E. Differences were tested with the Mann-Whitney U test
LBs than LCs (Fig. 4), indicating that relative amounts of photosynthetic organ (needle) in the total shoot biomasses were larger in lower branches.
Discussion Consistent with previous studies (Sabatier and Barthélémy 1999; Suzuki 2002), shoot length decreased with increasing branching order (Fig. 2). Longer shoots on the terminal part of the branch system are effective in exploiting space for the whole-branch system (Bégin and Filion 1999; Suzuki 2002), and shorter shoots can fill marginal spaces. Such correlative growth inhibition within the branch system is effective in filling space. Although shoot length tended to be longer in the leader crown, space filling by this shoot extension pattern was maintained at the branch systems in both vertical positions within the crown (Fig. 2). As expected, such a persistent pattern of shoot growth, which is hardly affected by the positions within the crown, might be due to the wellhierarchized, monopodial branching structures in the conifer crown. The fact that such shoot extension pattern was commonly observed for both Abies species further suggests the intensity of constraints on branching structures in the crowns of these conifer species. Properties of current shoots differed greatly between the two positions within the crown (Table 1). Shoots in the leader crowns had more needle biomass per unit of shoot length (Table 1, Fig. 3), suggesting close needle packing within the shoots (Mori and Takeda 2004b). Although this study did not measure actual light regimes, the leader crown of a canopy tree is expected to receive sufficient irradiance. In sunny conditions, the close packing of needles along the shoot is effective in intercepting incoming light more completely (Sprugel et al. 1996). Thus, the greater needle amounts on the shoots of the leader crowns may be a consequence of dense needle arrangement in response to sufficient light availability. Moreover, it is known that this needle arrangement requires a greater cost for mechanical support (Sprugel et al. 1996). The greater stem biomass per unit shoot length in the leader crowns (Table 1, Fig. 3) could reflect such a requirement.
In contrast, because branch systems in the lower layer tend to be located in more shaded conditions (Suzuki 2002), irradiance received by the shoots is generally less in the lower branches than in the leader crowns. In this study, current shoots in the lower branches had smaller needle biomass per unit of shoot length (Table 1, Fig. 3), suggesting less dense packing of needles within the shoots (Mori and Takeda 2004b). Such needle arrangement increases the ratio of shoot silhouette area to total needle surface area (STAR), resulting in the avoidance of mutual shading among needles in order to intercept the limited light more effectively (Sprugel et al. 1996; Stenberg 1996; Stenberg et al. 1998). Therefore, the reduced amounts of needles on the shoots of the lower branches may reflect the needle arrangement acclimating to the lower light availability. Also, this needle arrangement on the shoots can reduce the substantial requirement for mechanical support (Mori and Takeda 2004b), resulting in the smaller stem biomass per unit shoot length in the lower branches (Table 1, Fig. 3). Furthermore, low irradiance in the lower crown restricts shoot extension and vigor (Suzuki 2002). In this study, the lower branches produced shorter shoots than the leader crowns (Fig. 2). In general, because the mechanical requirement for support is less in shorter shoots, the photosynthetic organ comprises a greater proportion of total shoot biomass in shorter shoots than longer shoots (Niinemets and Kull 1995; Mori and Takeda 2004b). Shoots in the lower branches therefore had a greater proportion of photosynthetic organs within the total shoot biomass than the shoots in the leader crowns (Fig. 4). This may enhance the probability of the shoots in the lower branches maintaining a positive photosynthesis/respiration balance, which is most important consideration for shade shoots (Sprugel et al. 1996). As developing branch structures and whole-crown systems, branches tend to be shaded by their own and neighboring crowns. In spite of such expected differences in environmental conditions between the leader crowns and the lower branches, shoot extension patterns were constant irrespective of the positions within the crown of canopy trees. However, the properties at the each shoot level, such as needle arrangement and biomass allocation pattern, were changed according to the prevailing environmental conditions within the crown. It is worth noting that the fact that such tendency was generally observed for both A. mariesii and A. veitchii greatly implies the significance of changes in the shoot properties within the conifer crown. Because this study did not measure actual environmental conditions, which are expected to affect the development and maintenance of branch systems, such as light availability and branch age, further study is needed to clarify the detailed mechanisms of branch/crown maintenance affecting the persistence of A. mariesii and A. veitchii canopy individuals. However, this study proposes the importance of changes in the properties of each shoot as a component of a branch system and accordingly a whole-crown system in mature canopy trees of A. mariesii and A. veitchii that dominate in the subalpine forests in central Japan.
55 Acknowledgments We thank T. Ando, K. Kurumado, N. Miyamoto, and the members of the Takayama Research Station, Institute for Basin Ecosystem Studies, Gifu University for their support in the field research; K. Umeki and three anonymous reviewers for their critical reading of the manuscript; and all members of the Laboratory of Forest Ecology, Kyoto University, for their useful discussion. This study was partly supported by JSPS Research Fellowships for Young Scientists for A.M.
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