Annals of Botany 89: 767-772, 2002
© 2002 Annals of Botany Company
Allocation of Resources to Reproduction in Styrax obassia in a Masting Year
1Laboratory of Wood Biology, Graduate School of Agriculture, Hokkaido University, Kita 9, Nishi 9, Kita-ku, Sapporo 060–8589, Japan, 2Tomakomai Research Station, Field Science Center for Northern Biosphere, Hokkaido University, Tomakomai 053–0035, Japan and 3Laboratory of Regional Ecosystems, Graduate School of Environmental Earth Science, Hokkaido University, Kita 10, Nishi 5, Kita-ku, Sapporo 060–0810, Japan
* For correspondence. Fax +81 144 33 2173, e-mail hiura{at}exfor.agr.hokudai.ac.jp
Received: 22 August 2001; Returned for revision: 11 January 2002; Accepted: 8 February 2002.
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ABSTRACT |
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An analysis is presented of three possible pathways of reproductive allocation, namely, allocation of resources to reproductive organs from reproductive shoots, from non-reproductive shoots and from the main trunk. These pathways were examined by comparing the amount of storage starch in reproductive shoots, non-reproductive shoots and the main trunk in Styrax obassia, a typical masting tree species, during a year of little flowering (1999) and in a mass-flowering year (2000). In addition, we measured rates of light-saturated photosynthesis in leaves of reproductive and non-reproductive shoots to examine the contribution of photosynthetic production to reproductive costs. In both the main trunk and non-reproductive shoots the pattern of seasonal variation in the amount of starch did not differ between 1999 and 2000. However, in the mass-flowering year, the amount of starch in the reproductive shoots was less than that in non-reproductive shoots during the growing season. Thus, reproductive shoots bore most of the cost of reproduction, although non-reproductive shoots and the main trunk also bore some of the cost. Mass-based rates of light-saturated photosynthesis of the leaves of reproductive shoots were significantly higher than those of non-reproductive shoots during both the flowering and the fruiting period. However, leaves of reproductive shoots had a significantly smaller area, a lower mass per area, and lower concentrations of nitrogen than leaves of non-reproductive shoots, although the number of leaves did not differ between the two types of shoots. Therefore, the amount of photosynthate per shoot was significantly lower in reproductive shoots than in non-reproductive shoots. These results suggest that the cost of reproduction depends predominantly on storage starch in reproductive shoots, although it is still unclear how much photosynthate is allocated to reproductive organs from non-reproductive shoots.
Key words: Styrax obassia Sieb. et Zucc., reproductive allocation, storage resources, starch deposition, photosynthetic production.
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INTRODUCTION |
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Some tree species need to allocate large amounts of resources to their reproductive organs to enhance their reproductive success in a year of mass flowering (Kelly, 1994). However, it is not clear whether the main resources for reproduction are derived from storage resources or from the annual production of photosynthates. A study of resource limitation by artificial defoliation revealed that such treatment had little effect on fruit set, fruit production and reproductive allocation at the branch level in Ilex aquifolium (Obeso, 1998). In addition, there was no difference in fruit set between defoliated and non-defoliated Styrax obassia (Tamura and Hiura, 1998). These studies indicate that demands for reproductive resources were not met by current photosynthetic production but were probably met by stored resources. However, in a study of the mobilization of 14C in Pinus resinosa, Dickmann and Kozlowski (1970) found that female cones were the priority sinks for photosynthates of current needles. In addition, leaves adjacent to catkins (Chapin and Moilanen, 1991) and cones (McDowell et al., 2000) were more active photosynthetically than leaves on non-reproductive shoots. These observations indicate that reproductive costs are associated with high rates of photosynthesis in leaves adjacent to reproductive tissues. Therefore, quantitative analysis is needed to clarify whether resources for reproduction are derived mainly from stored resources or from the annual production of photosynthates.
It is possible that resource limitation imposed by artificial defoliation might have no effect on fruit set because fruits might be provided with stored resources from other branches or from the main trunk (Obeso, 1998; Tamura and Hiura, 1998). It is therefore necessary to analyse the allocation of resources to reproductive organs from first-order branches, the main trunk and roots. An experiment that involved girdling shoots and first-order branches demonstrated that reproductive shoots incurred mainly delayed costs (with deleterious effects of current reproduction on future growth, reproduction and survival) and that these reproductive shoots did not share resources with other branches, even though individual reproductive shoots could not, independently, supply the resources required for fruit development (Newell, 1991). These results suggest that storage resources might be mainly used by reproductive shoots or branches. In contrast, it is possible that stored resources in roots and the main trunk might be allocated to reproductive organs. However, the pathways for allocation of resources for reproduction in the modular structure of a tree have not yet been confirmed.
In this study, we examined three possible pathways for allocation of resources to reproduction in Styrax obassia, a typical masting tree species (Kato and Hiura, 1999), namely, resource allocation to reproductive organs from reproductive shoots, from non-reproductive shoots and from the main trunk. To identify the main organ that supplies resources for reproduction, we examined periodically the amount of stored resources at several levels of the modular structure in a single tree, namely, in reproductive shoots, in non-reproductive shoots and in the main trunk. Furthermore, we analysed the effects of current photosynthetic production on the allocation of resources to reproductive organs by comparing the rates of photosynthesis in reproductive and non-reproductive shoots.
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MATERIALS AND METHODS |
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Study site
The study was conducted in 1999 and 2000 on a permanent 9 ha plot in the Tomakomai Experimental Forest of Hokkaido University (TOEF; 42°40'N, 141°36'E) in northern Japan. The permanent plot was set in a mature broad-leaved forest (Hiura et al., 1998). The mean annual temperature is 5·6 °C and the mean annual precipitation is 1161 mm. The topsoil is very shallow and the volcanic deposits of Mt Tarumae, which erupted about 330 years ago, are about 1–2 m thick.
Study species
Styrax obassia Sieb. et Zucc. (Styracaceae) is a deciduous broad-leaved sub-canopy tree that attains a height of about 15 m at maturity; it has diffuse-porous wood and is distributed in cool-temperate forests in Japan and on the Korean peninsula. At reproductive maturity, the minimum diameter at breast height (dbh) is 5·7 cm in central Japan (Abe, 1995). S. obassia has pendulous terminal racemes, 13–17 cm in length, with 10–30 flowers that are hermaphroditic. Fruits are whitish-green and egg-shaped or spherical, and each fruit grows to 2 cm in length and 1·0–1·2 cm in diameter (Miyabe and Kudo, 1986). Each fruit usually contains a single seed. Flowering occurs from late June to early July after leaf flushing. The initial fruits begin to grow rapidly 2 weeks after flowering and stop growing about 5 weeks after flowering. The most frequent visitors to flowers are Bombus spp. (Tamura and Hiura, 1998). Nearly all the current reproductive shoots die back after fruiting.
The rate of flowering per tree and the number of inflorescences have been recorded since 1995 on a 4 ha subplot in the 9 ha permanent plot in TOEF. At the population level, the coefficient of variation of inflorescences is 1·85, which is relatively high for a tree species (Kelly, 1994). The year 2000 was the second-best mass-flowering year on the 9 ha plot in TOEF, while little flowering occurred in 1999 (Fig. 1; Kato and Hiura, 1999; unpubl. res.). In 1999, no inflorescences were found on the three trees that were used in this study. In contrast, in 2000, all of the trees had many inflorescences and infructescences. The proportion of reproductive shoots was 0 % in 1999, but was 26·8 ± 10·9 % in 2000. Therefore, fluctuation in the number of inflorescences between 1999 and 2000 reflected synchronization of flowering at the population level. It is hoped that the three trees used in this study are representative of the population in our study site.
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Quantification of storage starch
Three trees of approximately equal size (13·3 ± 0·9 m tall; dbh = 14·3 ± 1·2 cm) were selected for measurements of storage starch as a storage resource. Woody tissues were sampled at approx. monthly intervals, from 19 May 1999 to 29 Sep. 2000, when all fruits had matured. Samples were taken from the main stems at a height of 1·3 m above the ground and randomly from reproductive and non-reproductive shoots of each tree. The shoots of the trees were accessed from a large scaffolding system and mono-pole ladders (Fukushima et al., 1998; Hiura, 2000). A small block containing phloem, the cambial zone and two or three annual rings was punched out with a knife and chisel. Reproductive and non-reproductive shoots were distinguished anatomically under a stereomicroscope before bud break. Storage starch in roots was not examined in this study because a preliminary study (early November 1998) had shown the amounts of storage starch in roots to be much lower than those in the main stem and shoots (Y. Miyazaki et al., unpubl. res.), and also because of the difficulty of periodically sampling tree roots without damaging the tree. All samples were immediately fixed in FAA (50 % ethanol : acetic acid : formaldehyde, 18 : 1 : 1, v/v). Trans verse sections (about 16 µm thick) were cut on a microtome (LS-113; Yamatokohki, Saitama, Japan) from FAA-fixed samples. Sections were stained with I2-KI solution for detection of stored starch (Oribe et al., 2001) and were observed under a light microscope (BHS-BH2; Olympus, Tokyo, Japan).
The amount of starch was calculated as follows: amount of starch (%) = 100 (number of xylem uniseriate ray cells that contained starch/number of xylem uniseriate ray cells).
Thirty xylem uniseriate ray cells were examined in samples from main stems, which were equivalent to three or four annual rings, and all xylem uniseriate ray cells were examined in samples from shoots. Each xylem uniseriate ray cell that contained storage starch was scored as either a 1·0 cell, a 0·5 cell or a 0·25 cell, depending on the extent of deposition of storage starch granules within the cell. A 1·0 cell was one in which storage starch occupied more than 50 % of the cell area; a 0·5 cell was one in which storage starch occupied between 25 and 50 % of the cell area; and a 0·25 cell was a cell in which storage starch occupied less than 25 % of the cell area.
Rates of leaf photosynthesis
The rate of light-saturated photosynthesis was measured in the same three trees to estimate photosynthetic production. Measurements were made on 21 Jun. 2000 (before flowering), 29 Jun. 2000 (flowering), 22 Jul. 2000 (fruiting) and 29 Sep. 2000 (after fruiting), when the weather was sunny and calm. Measurements were made between 0900 h and noon. For each tree, one leaf of each of three reproductive shoots and three non-reproductive shoots, all of which were approx. the same height above the ground (about 9 m), was used for measurements. The gas-exchange rate of each of these leaves was measured with a portable infrared gas analyser (ADC LCA 4; Shimadzu, Kyoto, Japan), using a halogen lamp (2050-H; Walz, Effeltrich, Germany) as a light source. The rate of light-saturated photosynthesis was calculated from mean values obtained from leaves when the photosynthetic photon flux density exceeded 1000 µmol m–2 s–1. The mass-based rate of light-saturated photosynthesis (Amax) was calculated from the area-based rate of photosynthesis (µmol m–2 s–1) and the leaf mass per unit area (LMA; g m–2).
The area of each of the three leaves from reproductive and non-reproductive shoots was measured with a scanner and picture-analysis software (NIH-Image, version 1·59; Rasband, NH, USA). The mass of leaves was measured after drying at 80 °C for 48 h. Leaf mass per unit area was calculated from the leaf area and the leaf dry mass. Nitrogen concentrations in leaves were measured with a C/N analyser (NC-900; Sumitomo, Osaka, Japan).
Data analysis
Differences between reproductive shoots and non-reproductive shoots in amounts of starch, mass-based rates of photosynthesis, LMA and leaf nitrogen concentrations were analysed using a paired t-test. Seasonal variation in the amount of starch in 1999 and 2000 was compared by two-way repeated-measures ANOVA in the main trunk and non-reproductive shoots. In this analysis, each year was divided into four seasons (before leaf expansion; flowering and fruiting; after fruiting; and after defoliation), and seasonal variation was calculated using all the values obtained in each the season. All analyses were performed with Stat View 5·0 (Abacus Concepts, Berkeley, CA, USA).
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RESULTS |
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Storage starch
Storage starch was found in the ray parenchyma cells and axial parenchyma cells of the xylem and in cells in the cambial zone. In reproductive and non-reproductive shoots, starch granules were also observed in pith parenchyma cells (Fig. 2). Very few starch granules were observed in the phloem. In both 1999 and 2000, the amount of starch in the main trunk and in non-reproductive shoots was lowest from early December, after the leaves had fallen, to early March (Figs 3 and 4). In the middle of March, before leaf expansion, the amount of starch in the main trunk and in non-reproductive shoots increased; however, there was a slight reduction after leaf expansion. After the leaves had developed fully, starch increased gradually until October, when the leaves became senescent. In both the main trunk and non-reproductive shoots, the pattern of seasonal variation in the amount of starch did not differ between 1999 and 2000 (Fig. 3 main trunk, F = 2·37, d.f. = 9, P = 0·143; Fig. 4 non-reproductive shoots, F = 1·44, d.f. = 9, P = 0·247), although there was a significant interaction between season and year in the main trunk (P = 0·018). In contrast, the amount of starch in reproductive shoots was lower than that in non-reproductive shoots (Fig. 2). On 22 Jul. 2000 (4 weeks after flowering), there was a statistically significant difference between reproductive and non-reproductive shoots in the amount of starch (P = 0·031, Fig. 4).
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Photosynthesis in leaves
From 21 June (before flowering) to 29 Sep. 2000 (after fruiting), we observed decreases in Amax in both reproductive shoots and non-reproductive shoots. In reproductive shoots, Amax was significantly higher than in non-reproductive shoots on 29 June (flowering; P < 0·001) and on 22 July (fruiting; P = 0·036), although there was no significant difference on 21 June (before flowering) and on 29 September (after fruiting; Fig. 5). The leaves of reproductive shoots had significantly lower LMA (P = 0·024), smaller areas, and lower nitrogen concentrations than leaves of non-reproductive shoots (Table 1; both P < 0·001). In contrast, the number of leaves did not differ between the two types of shoot (P = 0·104, Table 1).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The seasonal variation in the deposition of storage starch in S. obassia was similar to that reported in other deciduous trees (Sauter and van Cleve, 1991; Sauter, 2000). Increases in levels of soluble sugar in the autumn or in early spring coincide with hydrolysis of accumulated starch in woody plants, and soluble sugars appear to play an important role in the mechanism of freezing tolerance (Sakai and Larcher, 1987). Although we measured only the amount of storage starch, a similar mechanism to ‘starch-sugar conversion’ (Sauter and van Cleve, 1991) might occur.
In this study, both in the main trunk and in non-reproductive shoots, the pattern of seasonal variation in the amount of starch did not differ between 1999 and 2000 (Figs 3 and 4). Furthermore, the amount of starch in reproductive shoots was lower than that in non-reproductive shoots in 2000 (Fig. 4). These results indicate that the non-reproductive shoots and the main trunk allocate little storage starch to reproductive organs. Given that almost all the current reproductive shoots died back after fruiting, almost all the storage starch in reproductive shoots was exhausted.
The strong carbon sink provided by developing fruits increases rates of photosynthesis in neighbouring foliage (de Jong, 1986; Reekie and Bazzaz, 1987). Similarly, in the present study, we found that Amax of reproductive shoots was significantly higher than that of non-reproductive shoots both during flowering and during fruiting, when the sink activity of reproductive tissues was high (Fig. 5). Leaves of reproductive shoots had significantly smaller areas and lower LMA (g m–2) than leaves of non-reproductive shoots, although the number of leaves did not differ between the reproductive and non-reproductive shoots (Table 1). If we calculate the amount of photosynthate per shoot using Amax, mean leaf area and LMA, the amount of photosynthate was lower in reproductive shoots than in non-reproductive shoots mainly because of their much lower leaf area. Therefore, resources produced by the current high rate of photosynthesis in reproductive shoots might not make a substantial contribution to the resources allocated to reproduction. In addition, it is possible that smaller amounts of photosynthate per reproductive shoot were responsible for a reduction in the amounts of storage starch in reproductive shoots. Reproductive shoots might be considered as disposable units at some level, although it is still unclear how much photosynthate is allocated from non-reproductive shoots to reproductive organs.
Small leaves have been reported on reproductive shoots in birch (Chapin and Moilanen, 1991). Hiura et al. (1996) demonstrated that the seed size of Fagus crenata was negatively correlated with leaf size. The smaller size of leaves on reproductive shoots might represent a trade-off between reproductive and vegetative states (Hiura et al., 1996). Similarly, the lower LMA and leaf nitrogen concentrations in reproductive shoots might result from a trade-off between reproductive and vegetative growth, since a leaf primordium and an inflorescence primordium are present in the same bud in S. obassia.
The smaller concentrations of leaf nitrogen in reproductive shoots suggest that reproductive tissues might be sinks for nitrogen from neighbouring foliage, as noted previously in Sidalcea oregana and Pinus resinosa (Chapin, 1989; Ashman, 1994; McDowell et al., 2000).
In conclusion, our study suggests that Styrax obassia, a typical masting tree species, can use storage starch for reproduction and that the reproductive shoots exhausted almost all their storage starch. Storage resources are important for mass flowering and seeding in tree species such as S. obassia.
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ACKNOWLEDGEMENTS |
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We thank K. Shimizu, E. Nabeshima, Y. Fukushima, H. Maeno, Y. Miyake and M. Suzuki for their assistance in the field and for helpful discussions. We also thank Dr T. Koike for providing the portable infrared gas analyser, and staff of the TOEF (Hokkaido University) for arrangements at the study site. This work was supported in part by grants from the Ministry of Education, Science, Sports and Culture of Japan (nos 09NP1501, 1213204, 11440223 and 13304060 to T.H. and no. 11460076 to R.F.).
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