Dwarf bamboo is a dominant forest floor species, especially in the northern part of Japan. Sasa kurilensis, Sasa senanensis and Sasa nipponica are widely distributed in this region. Growth characteristics of these three Sasa species are also different: leaf longevity of S. kurilensis is 3–5 years. In contrast, leaf longevity of S. senanensis and S. nipponica are 2 years and <1 year, respectively. We predicted that ecophysiological characteristics of the three Sasa species would reflect their leaf longevity; however, their characteristics were still not well analysed. We examined ecophysiological parameters of the three Sasa species grown under the same environment. Net photosynthetic rate at light saturation (Psat) and nitrogen concentration (N) of S. nipponica showed high values after flushing. However, culms of S. nipponica were dropped after overwintering, and Psat of the 2-year-old leaves drastically decreased. Meanwhile, Psat of the current leaves of S. kurilensis was lower than the other two species. However, Psat of 2-year-old leaves of S. kurilensis still maintained a relatively high value. Psat of the current leaves of S. senanensis was higher than that of S. kurilensis even though N was the same. From these results, S. senanensis had a high photosynthetic nitrogen efficiency rate (Psat/N).
- photosynthetic capacity
- leaf thickness
1.1. Dwarf bamboo in Japan
Dwarf bamboo is a small size bamboo species that distributes in Eastern Asia. On the classification of bamboo in Japan, dwarf bamboo is separated from the other bamboos. For dwarf bamboo, the sheath of culm remains until its death, whereas other bamboo species are removed their sheath during the process of culm growth. Six genera and 72 species of dwarf bamboo are grown in Japan (Table 1) . Moreover, the genera of Sasa and Pleioblastus are divided into several sections by their morphological characteristics . The northern limit of distribution area of dwarf bamboo is considered at the middle part of Sakhalin where the genus Sasa distributes .
|Genera and section||Number of species||Typical species|
|Section Macrochlamys||6||Sasa kurilensis Makino et Shibata|
|Section Lasioderma||9||Sasa shimidzuana Makino|
|Section Monilicladae||4||Sasa tsuboiana Makino|
|Section Sasa||9||Sasa senanensis Rehder|
|Section Crassinodi||8||Sasa nipponica Makino et Shibata|
|Sasaella||10||Sasaella ramosa Makino|
|Sasamorpha||2||Sasamorpha purpurascens (Hechel) Makino|
|Pseudosasa||2||Pseudosasa japonica Makino|
|Subgen. Pleioblastus||4||Pleioblastus linearis Nakai|
|Section Medakea||6||Pleioblastus simonii Nakai|
|Section Nezasa||11||Pleioblastus chino Makino|
|Chimonobambusa||1||Chimonobambusa marmoreal (Mitford) Makino|
The habitats of dwarf bamboo in Japan are restricted by climate, especially winter . The climate in Japan is divided by the coasts of the Sea of Japan and Pacific Ocean , and the coast of the Sea of Japan area is considered as the snowy area. The presence of snow is an important factor to restrict the distribution of dwarf bamboo, and the main genus to distribute in the snowy area is Sasa . Among the five sections of Sasa genus, Macrochlamys and Sasa can distribute in snowy area, since they are adapted to the snowy environment . In this article, we introduce the ecological characteristics of the three species in genus Sasa that grow in the northern part of Japan. We also focus on growth characteristics of the three dominant species of genus Sasa with an ecophysiological method.
1.2. Ecological characteristics of three Sasa species in Northern Japan
In Northern Japan, the dwarf bamboo is a typical and essential component of the forest floor [6, 7]. In this region, Sasa kurilensis, Sasa senanensis, and Sasa nipponica distributed widely [1, 8]. In Hokkaido Island, which is located in the most northern part of Japan, the distribution of these three species is separated (Figure 1, ). These species are separated by the snow depth. The main distribution area of S. nipponica is the eastern part of Hokkaido, which faces the coast of the Pacific Ocean. Snow depth of this area is lower than other areas (below 75 cm of maximum snow depth) . The distribution of S. kurilensis is the mountain area with heavy snow (over 150 cm of maximum snow depth). The distribution of S. senanensis is at the middle range of maximum snow depth between S. nipponica and S. kurilensis (75−150 cm). Also, the three Sasa species have different freezing tolerance. The climate in the area of the coast of Pacific Ocean the minimum temperature is lower than −10°C, and soil freezing occurs due to low snow depth . The freezing tolerance for the bud of S. nipponica (−10 to −15°C) is higher than S. kurilensis and S. senanensis (−5 to −10°C) . As a result, bud of S. nipponica can survive soil freezing. On the other hand, the distribution area of S. kurilensis and S. senanensis is covered with deep snow during the winter [1, 4]. The culms of S. kurilensis and S. senanensis are laid on the ground by the weight of snow cover. Snow has low thermal conductivity , and low air temperature is not easily conducted to the soil; as a result, soil can escape freezing . Thus, S. kurilensis and S. senanensis can survive under the snow cover in winter. When the leaf and culm of S. kurilensis and S. senanensis are exposed above the snow depth, these organs cannot survive [12, 13].
The three Sasa species have different morphology types (Figure 2, ). The culm height of S. kulinensis reaches 3 m, and its longevity is estimated to be over 10 years. The upper part of the culm of S. kulinensis has buds on nodes and continues to bifurcate. In contrast, there are no buds at lower part of the culm of S. kulinensis. The leaves of S. kulinensis can survive for relatively longer time, and its longevity ranges from 3 to 5 years. The culm height of S. senanensis is about 2 m, and its longevity is 5 years. The culm of S. senanensis has buds on every node. The leaf longevity of S. senanensis is about 2 years. In contrast, the culm height of S. nipponica is less than 1 m, and its longevity is also about 1 year. The buds of S. nipponica exist at the underground of the culm. The leaf longevity of S. nipponica is less than 1 year.
The three Sasa species have well-developed rhizome systems and are dominant at the forest floor in general forests of this region [14, 15]. As a result, the light environment under the Sasa species is quite dark, and regeneration of other species is suppressed . Moreover, the Sasa species has high regeneration ability after disturbances. When forests suffer from forest fires, forest cannot restore; however, dwarf bamboo is able to regenerate as ground vegetation [17, 18]. The flowering period of the Sasa species is estimated to be 60–100 years ; however, information of flowering is still limited. Based on previous information, flowering of Sasa species occurs synchronously and often expands over 1000 ha in area [4, 19]. After flowering, numerous seeds are produced, and all culms of the Sasa species dies [4, 19], as does a monocarpic plant.
2. Ecophysiological characteristics of three Sasa species
In the previous chapter, we summarized the ecological characteristics of the three dominant Sasa sp. in Northern Japan: S. kurilensis, S. senanensis, and S. nipponica. We showed specific traits of leaves and culm longevity of the three species. To survive and grow under different growth conditions, the Sasa species have adapted to each habitat through morphological and physiological adaptation. For example, leaf and stem longevities of S. nipponica are 1 year, and so its leaf has to obtain large amount of photosynthetic productivity during the one growing period. In contrast, leaves and culms of S. kurilensis can survive for a long period. Therefore, it also may be possible for S. kurilensis to obtain photosynthetic productivity for a long period. In general, plant growth form can be evaluated through ecophysiological characteristics [20, 21]. Photosynthetic characteristics of three Sasa species have been measured by previous research [22, 23, 24]. However, characteristics cannot be compared because the measurement was done under different conditions.
There are contrasting growth characteristics, namely fast and slow . Fast-growing species have short-lived leaves with a high photosynthetic capacity, whereas slow-growing species have long lived leaves with a low photosynthetic capacity that can maintain its function over long periods. The differences of photosynthetic capacity between fast- and slow-growing species are related to foliar nitrogen concentration, which is usually higher in fast-growing than in slow-growing species . In contrast, photosynthetic nitrogen use efficiency is an indicator for allocation of nitrogen to photosynthetic apparatus; slow-growing species shows a high value . The nitrogen use characteristic is predicted to be different according to life form. For example, the photosynthetic rate and concentration of nitrogen may be high for S. nipponica, since it has a short leaf longevity. We predicted, in contrary, that leaves of S. kurilensis may have a low photosynthetic rate and low nitrogen concentration. The long longevity of S. kurilensis may be compensated with low photosynthetic productivity as found in several kinds of evergreen spruce .
The aim of this chapter is to show ecophysiological characteristics of the three Sasa species in relation to their different life forms, such as leaf longevity, culm height, etc. We measured the seasonal change of photosynthetic rates, concentrations of nitrogen and chlorophyll, and leaf thickness of different aged leaves of the three Sasa species planted in a common garden.
2.2. Materials and methods
This research was conducted in an arboretum of the Hokkaido Research Center, Forestry and Forest products Research Institute (43°00′N, 141°23′E, 141 m a.s.l.) located in Sapporo City, Hokkaido, Japan. The annual mean, maximum, and minimum temperatures at the metrological station of this centre were 7.3, 35.7, and −22.8°C, respectively, from 1975 to 2003 . The range of annual precipitation was from 581 to 1490 mm year−1 during 1975–2003 . The maximum snow depth in winter was 130 cm . In this arboretum, the subterranean stem of S. kurilensis, S. senanensis, and S. nipponica was planted in 1982. The size of planting area was 5 × 10 m for each Sasa species. Plantations of Sasa species were exposed to full sunlight the whole day because there were no surrounding trees around the plantation.
We measured the photosynthetic rate at light saturation (Psat, μmol m−2 s−1) from May to October 2004. The measurements were carried out at 10:00–15:00 each month. Second leaves counted from the top of culm of each Sasa species were used for the measurement of Psat. We selected four leaves of current and 2-year-old ones located at sunny positions. Measurements were made by using a portable gas analyzer (LI-6400, LI-COR Biosciences, Lincoln, NE, USA) under steady-state conditions (25°C, 36.0 Pa of CO2, and 1800 μmol m−2 s−1 photosynthetic photon flux using LED), which were previously determined .
After measuring photosynthetic rate, we sampled the leaves and analysed the chlorophyll concentration. The fresh mass of leaves were first measured, then crushed by liquid nitrogen, and finally extracted by dimethyl sulfoxide. Measurement of chlorophyll was done by a spectrophotometer (V560, JASCO Co., Tokyo, Japan), and its concentration was calculated by an equation . The remaining leaf samples were dried at 80°C, for 4 days. After drying, we measured specific leaf area (SLA = leaf area per dry mass, cm2 g−1, ). Leaf samples were ground to a fine powder using a sample mill (WB-1; Osaka Chemical Co., Osaka, Japan). The mass-based concentration of nitrogen (Nmass, mmol g−1) was analysed using a NC analyser (NC-800, Sumika Chemical Analysis Service, Osaka). We also calculated the photosynthetic nitrogen use efficiency (PNUE, nmol mmol−1 s−1, ) as an indicator of photosynthetic apparatus allocation. PNUE was calculated by the following Eq. (1). We also calculated area-based concentration of nitrogen (Narea, mmol m−2) from the value of SLA Eq. (2).
The value of Psat, SLA, concentrations of chlorophyll and nitrogen, and PNUE was examined using Tukey tests. The mean values were compared among S. kurilensis, S. senanensis, and S. nipponica.
Concerning the value of Psat for the current leaves, S. nipponica showed high values (14 μmol m−2 s−1) from June when its leaves flushed (Figure 3). In July, Psat of S. nipponica increased to 18 μmol m−2 s−1, and its value was significantly higher than other Sasa species (P < 0.01). However, Psat of S. nipponica started to decrease from September. Psat of S. senanensis in June was significantly lower than S. nipponica (P < 0.001); however, Psat increased to 16 μmol m−2 s−1 from July to September. In contrast, flushing of leaves of S. kurilensis was in July, and Psat was significantly lower in July and August than other Sasa species (P < 0.001). In September, Psat of S. kurilensis increased to 15 μmol m−2 s−1.
In 2-year-old leaves, all Sasa species showed high values of Psat in May when all species had not yet flushed new leaves. However, Psat of 2-year-old leaves was decreased from June. Especially, the culms of S. nipponica fell to the ground in June, and Psat was drastically decreased. Psat of S. senanensis and S. kurilensis was also decreased from July. However, Psat of S. kurilensis was maintained at 8 μmol m−2 s−1 until September, and these values were significantly higher in July, August, and September than that of S. senanensis (P < 0.05).
The value of SLA was also different among the three Sasa species. For the current leaves, SLA in July and September showed significantly high values for S. nipponica than that for S. senanensis and S. kurilensis (Figure 4, P < 0.05). In contrast, SLA for current leaves of S. kurilensis was the lowest values from July to September. The values of SLA for current leaves decreased by time for all Sasa species. Compared to current and 2-year-old leaves, SLA showed low values for 2-year-old leaves for all Sasa species. From July, there was no significant difference in SLA of 2-year-old leaves among the three Sasa species.
Concentration of mass-based nitrogen (Nmass) in current leaves showed the highest values in June for S. nipponica and S. senanensis; however, their values decreased by time (Figure 5). In the case of S. kurilensis, the decrease of Nmass in current leaves was not clear. Nmass for current leaves was significantly higher for S. nipponica from June to September than those for S. senanensis and S. kurilensis (P < 0.05). In October, Nmass of S. nipponica showed similar value with S. kurilensis. As for the trend of 2-year-old leaves, all Sasa species decreased Nmass with time. Nmass in June of 2-year-old leaves of S. nipponica was significantly lower than the Nmass of S. senanensis and S. kurilensis (P < 0.05).
Compared with Nmass, area-based nitrogen (Narea) showed that its decrease by time was not obvious for current leaves. The peak of Narea showed in June of 2-year-old leaves for S. kurilensisand S. senanensis, whereas its peak was in June of current leaves for S. nipponica. Narea for current leaves of S. nipponica showed significantly higher than that of S. senanensis from June to August (P < 0.01). In contrast, Narea for current leaves of S. nipponica did not show significant difference with S. kurilensis from July to September. In October, Narea for current leaves showed significantly higher for S. kurilensis than those of other Sasa species (P < 0.001). Also, Narea for 2-year-old leaves showed significantly higher for S. kurilensis than that for S. nipponica (P < 0.01). Narea for 2-year-old of S. senanensis showed middle range between S. kurilensis and S. nipponica, and its trend was similar with S. kurilensis.
Total chlorophyll (Chl a+b) concentration showed the low value after flushing and increased in August for S. kurilensis and S. nipponica and in June for S. senanensis (Figure 6). Compared with Sasa species, chlorophyll concentration was significantly high value for current leaves of S. kurilensis in September and October (Figure 6, P < 0.05). In August, chlorophyll concentration of current leaves was significantly higher at S. nipponica compared to S. kurilensis and S. senanensis (P < 0.05).
Chlorophyll concentration for 2-year-old leaves of S. kurilensis and S. senanensis was maintained these values compared with current leaves, whereas its value of S. nipponica was decreased gradually. S. kurilensis had a significantly higher chlorophyll concentration in all months than that of S. nipponica and S. senanensis (P < 0.05). Concentration of chlorophyll for 2-year-old leaves showed remarkable decrease from September.
PNUE of current leaves showed significantly high values for S. senanensis from July compared with the other Sasa species (Figure 7, P < 0.05). In contrast, PNUE of current leaves of S. nipponica decreased from September. PNUE of current leaves of S. kurilensis increased from September. PNUE of current leaves was decreased for all Sasa species in October.
For 2-year-old leaves, PNUE showed high in May; however, this value was decreased in June. From June to August, the value of PNUE was maintained these values for three Sasa species. In September, PNUE of S. kurilensis and S. senanensis was increased, whereas its value was decreased for S. nipponica. Compared with three Sasa species, PNUE for 2-year-old leaves of S. kurilensis was significantly higher from July to October than those for other Sasa species (P < 0.05).
Based on the results, the ecophysiological characteristics of the three Sasa species were different. The leaf of S. nipponica showed high Psat from flushing (Figure 3). The leaf of S. nipponica also had high N (Figure 5), and this made it possible to maintain a high Psat concentration. Furthermore, the leaf of S. nipponica was thin with a high value of SLA (Figure 4). In general, thin leaves have a low value of CO2 diffusive conductance ; as a result, thin leaves show high Psat. So, the relatively thin leaf of S. nipponica has a big advantage to obtain a high photosynthetic rate through diffusion of CO2 in its leaves. In contrast, 2-year-old culm of S. nipponica was fallen in June, and its leaves were laid at a low layer of the plantation. Psat of 2-year-old leaves decreased (Figure 3), and the photosynthetic productivity of its leaf may have been small. However, we confirmed that the leaves of S. nipponica could survive over 1 year, even if the culm has fallen.
These characteristics that show high photosynthetic capacity and high concentration of nitrogen for younger leaf and short leaf longevity are corresponded with fast-growing species . In general, fast-growing species shows that photosynthetic rate is decreased drastically by increase of leaf age [21, 30]. This trend is clear for evergreen oak compared with conifer species . Moreover, there are a fast-growing species among same genus of Picea, and Picea abies and Picea glauca are considered as fast-growing species . These species showed high photosynthetic rate for younger leaves; however, their high values were not maintained. Also, fast-growing species have a high rate of leaf turnover . Woody species have a leaf turnover mechanism, and when old leaves are lost, leaf nitrogen is retranslocated to younger leaves . S. nipponica showed continuous decrease of Nmass (Figure 6), and its trait is probably related with retranslocation of nitrogen. S. nipponica may be retranslocated nitrogen from old to young leaves, thus maintaining high photosynthetic capacity.
For the other Sasa species, the maximum value of Psat for current leaves of S. kurilensis was lower than other species; however, its value for 2-year-old leaves was maintained for 5 months (Figure 3). These traits are corresponded with slow-growing species . The concrete slow-growing species are Taxus baccata, Picea mariana, and Picea rubens [21, 30]. The leaf longevities of these species were over 5 years, and photosynthetic rates showed high value for 6-year-old leaves [21, 30]. Also, maximum leaf longevity of S. kurilensis is 5 years , and its ecophysiological characteristics are similar with other slow-growing species. Also, slow-growing species have a characteristic to maintain high value of PNUE for aged leaves [21, 30], and S. kurilensis showed high PNUE for 2-year-old leaves (Figure 7). This trait is related with the maintenance of photosynthetic rate for long period.
On other traits, slow-growing species has thick leaves [21, 25]. Leaves of S. kurilensis showed a low value of SLA (Figure 4), which was characterised by thick leaves. In general, species with a small SLA allocates nitrogen to the leaf cell wall and increases toughness of the cell . This trait contributes to the extent of leaf longevity . Thus, allocation of nitrogen in leaves for S. kurilensis is probably larger for cell wall than for protein of photosynthetic apparatus. As a result, S. kurilensis may make leaves with a long longevity but with a low photosynthetic rate.
Psat of S. senanensis for current leaves showed high values in August and September (Figure 3). In contrast, current leaves of S. senanensis were thick (Figure 4), and Narea and Nmass were low compared with S. nipponica (Figure 5). Thus, ecophysiological characteristics of S. senanensis are not similar with S. nipponica. In contrast, leaves of S. senanensis were thin (Figure 4) and short longevity (about 2 years, ) compared with S. kurilensis. Thus, ecophysiological characteristics of S. senanensis are also not similar with S. kurilensis. Consequently, ecophysiological characteristics of S. senanensis are intermediate between fast- and slow-growing species. On the remarkable characteristics of S. senanensis, PNUE showed the highest value for current leaves (Figure 7). S. senanensis may allocate more nitrogen to protein of photosynthesis apparatus compared with other Sasa species. Similar ecophysiological characteristics were reported for Pinus pinea and Picea jezoensis var. hondoensis [21, 30].
In addition, the trait of chlorophyll concentration also concerns with ecophysiological characteristics. The concentration of chlorophyll showed high values for S. kurilensis, especially 2-year-old leaves (Figure 6). In general, chlorophylls have light harvesting complex proteins (LHCP) at thylakoids in the chloroplast . As an increase of chlorophyll contributes to an increase in photon absorption, chlorophyll concentration shows a positive relationship with photosynthetic rate within the same species . In the case of 2-year-old leaves of S. kurilensis, Psat showed a high value despite not having a high nitrogen concentration (Figures 3 and 5) and small SLA (Figure 4). There is a possibility that 2-year-old leaves of S. kurilensis allocate nitrogen to chlorophyll (Chl/N) and reinforce the absorption and transferring capacity of photon. Consequently, S. kurilensis may use absorbed photo efficiently for increasing photosystem by decreasing CO2 diffusion in its leaf. Leaf longevity of S. kurilensis is 3–5 years . Therefore, aged leaves of S. kurilensis are considered to be shaded by new leaves that flushed later on; therefore, mutual shading occurs. High concentration of chlorophyll in 2-year-old leaves of S. kulinensis may have had the advantage under shady conditions.
Sasa species regenerates at the same place with clonal development, and these traits cannot be simply classified into fast- and slow-growing species as other species. We regard the Sasa species as follows: S. nipponica is classified as a fast-growing species, whereas S. kulinensis are slow-growing species. Indeed, ecophysiological characteristics of Sasa sp. are the same as slow- and fast-growing species as found in other plant species. S. senanensis cannot be classified as two growing types and showed intermediate characteristics between fast- and slow-growing species.
Related to the habitat of the three Sasa species, edaphic habitat of S. nipponica is considered to be the deep humus layer and A-horizon . The characteristics of a fast-growing species is to have an advantage in a fertile habitat, and the growth trait of S. nipponica shows a rapid turnover of leaves and culms , which is considered to be suitable for the habitat. We conclude that ecophysiological characteristics of S. nipponica are adapted to fertile habitats. The distribution area of S. nipponica is classified as low altitudes, facing to the coast of Pacific Ocean where the summers are relatively cloudy with high humidity and the high photosynthetic performance of S. nipponica is kept . Moreover, although the snowy period there is short, the soil freezes with cold climate . Sasa cannot keep evergreen leaves during winter; hence, the Sasa species must produce new leaves from spring after the death of leaves of previous year. Its high photosynthetic rate may be compensating short leaf longevity.
In contrast, the distribution of S. kurilensis is hillsides and slope of valley sides where soil depth is shallow . In general, these locations restrict plant growth. The leaves and culms of S. kurilensis can survive for several years , and these traits may exist to compensate for low photosynthetic productivity. S. kurilensis showed high concentration of chlorophyll and PNUE for 2-year-old leaves (Figures 6 and 7). This characteristic is suitable for conditions where resources are limited. Thus, we conclude that ecophysiological characteristics of S. kurilensis reflect the adaptability to infertile habitats. S. kurilensis distributes at high mountain areas in Hokkaido Island (Figure 1). The area of S. kurilensis probably corresponds with deep snow and harsh environmental conditions.
The habitat of S. senanensis is similar to the soil condition of S. nipponica . Leaf longevity of S. senanensis is about 2 years , and this characteristic is probably suitable for relatively good environmental conditions, such as high soil fertility. Compared with S. nipponica, Nmass and Narea in current leaves were lower for S. senanensis (Figure 5). Thus, the nutrient requirement of S. senanensis is also lower than that of S. nipponica, and S. senanensis can adapt to infertile habitats or resources limited conditions. Moreover, the longevity of culm of S. senanensis is about 5 years, which is different from its leaves. Its culm has buds at every node (Figure 2), and the leaves can flush during the latter period of the culm life-span. Based on these results, we conclude that the growth characteristics of S. senanensis may be high flexibility, and it is also able to adapt to different nutrient and environmental conditions. In fact, the distribution area for S. senanensis in Hokkaido Island is the largest (Figure 1). The flexibility of S. senanensis may be enabling this species to grow in a broad distribution range.
We thank Dr. M. Kitao, Dr. H. Tobita, Dr. H. Utsugi (FFPRI) and Prof. Y. Maruyama (currently Nihon University) for their invaluable comments on this study. Thanks are also given to researchers at the Hokkaido Research Center, FFPRI for their encouragement. We are grateful to the technical staff of Hokkaido Research Center, FFPRI for maintenance of the arboretum. We thank Ms. Saki Fujita (Hokkaido University) for English improvement and Ms. M. Ohbuchi for assistance in the experiments.