Shoot Development and Leaf Senescence A Leaf Phenology

Phenological plant research on both herbaceous and woody plants has focused on the description of seasonal events using pheno-diagrams which are useful (Lieth, 1971); however, this method may provide limited inference about the functional and dynamic aspects of plant life affected by environmental and endogenous conditions. More quantitative description is needed to show the dynamics of tree growth. Description of functional events of tree shoots has provided us with an understanding of their mode of growth.

The pattern of shoot development is usually related to the successional traits of deciduous broad-leaved trees (Marks, 1974; Maruyama, 1978). For example, based on morphological observation of the structure of a shoot, the early-successional tree species were found to elongate their shoots through a year, while late-successional trees species may keep leaves for a long time in Malaysian tropical rain forests (Koriba, 1958; Ninomiya et al, 2000).

Similar leaf dynamics of successional tree species are found in the Indian mountain region with seasonal climatic conditions (Boojh and Ramakrishnan, 1982).

A similar relationship between the shoot elongation and diameter growth is also found for deciduous broad-leaved trees in the Appalachian mountain forests (Bicknell, 1982). Among these observations, the pattern of shoot elongation seems to directly relate to the forest dynamics. Early-successional species produce shoots over a long period, while late-successional species flush shoots all at the same time in order to occupy growth space. Demographic analysis of the individual leaves of a plant is a useful tool for addressing functional aspects of leaf phenology (Harper, 1987; Kikuzawa, 1983, 1984).

Deciduous broad-leaved trees with pioneer traits usually have the longer period of shoot elongation in order to secure growth space. The duration of shoot elongation of established late-successional species is usually short (Maruyama, 1978). However, some conifers, such as pine species (Pinus densiflora) with growth traits of the early-successional species flush their shoots at the beginning of the growing season (Nagata, 1983). By contrast, late-successional type species, such as Sugi cedar (Cryptomeria japonica) and Hinoki cypress (Chamecyparis obtusa) elongate shoots for a long time (Koike, 1982). Therefore, the pattern of shoot elongation is not always reflected from successional growth characteristics in tree species.

Leaf longevity and successional traits of deciduous broad-leaved tree species are closely correlated with the decreasing rate of net photosynthesis after it reaches the maximum value (Koike, 1988). Most early-successional trees or light-demanding species show a rapidly decreasing rate, while late-successional trees or shade-tolerant species have a slower decreasing rate (Koike, 1988; Reich etal., 1995).

B. Leaf Shedding

Shedding of leaves is considered to occur to avoid environmental stresses, such as shading, cold and desiccation (Axelrod, 1966; Kozlowski and Pallardy, 1997; Addicott, 1982). In some tree species (e.g., cinnamon tree, Cinnamomum camphora), the old leaves turn orange in spring just before new leaf unfolding; thus, the life-span of cinnamon tree leaves is almost one year (Sato, 1989). Before leaf shedding in the beginning of early summer, one-year-old leaves change their color and nutrients are recycled from aged leaves to new leaves or branches. Similar phenomena are found for the evergreen shrub Daphniphyllum macropodum (the Japanese common name is "replacing leaves"). In heavy snow areas, it sheds older colored leaves after new leaves have unfolded (Hayashi, 1985). Snow cover usually acts as protection for plants against low temperature and winter desiccation, which may prolong leaf longevity. However, the physiological activities of photosynthetic production of those aged leaves decrease because of shading by shoots with new leaves. This shedding of aged leaves is believed to minimize the cost of photosynthesis due to respiration loss by new leaves under shady conditions and minimizing the leaf area to reducing evapotranspiration.

In a temperate forest, leaf senescence and shedding in small trees sometimes shows unique patterns relative to the canopy cover. For example, seedlings of Prunus ssiori unfold all leaves before canopy closure in deciduous broad-leaved forests of northern Japan. This cherry species efficiently uses incident light flux during the leafless period of the overstory in spring. In contrast to this species, Carpinus cordata seedlings flush all leaves at almost the same time as the canopy closure of tall trees but usually keep green leaves after leaf shedding of the overstory and have dead leaves in the next spring (Kitaoka et al., 2000).

An interesting example of shade avoidance is found for Daphne kamtschatica, a summer deciduous shrub in the forest of northern Japan (Kikuzawa, 1984; Lei and Koike, 1998). In this shrub, leaf senescence starts with leaf yellowing after canopy closure of overstory trees in late spring, and all leaves are shed by mid-summer. This summer deciduous-ness seems to be complete shade avoidance. The photosynthetic rate of D. kamtschatica tended to be saturated at less than 400 ^mol m-2 s-1 (Lei and Koike, 1998). However, photosynthetic photon flux density (PPFD) at the forest floor after canopy closure is 80 and 200 ^molm-2 s-1 depending on the density of canopy layers (Lei et al., 1998). Although the shading cloth only reduced the PPFD and did not alter the spectrum, the leaves cannot carry out net photosynthesis under these conditions. This treatment with an artificial shading cloth accelerated senescence of the leaves. This shrub starts to unfold leaves at the beginning of autumn when most of the trees of the overstory begin to shed leaves.

Deciduousness may serve to avoid water deficits in the tropics (Axelrod, 1966). In the dry season of tropical areas, most trees shed leaves to avoid the desiccation period (Addicott, 1982). This may also be true for the shedding of needles of pine species in various seasons. For example, pine species originating from the high latitudes change needle color to yellow in autumn and shed needles before the winter season to minimize exposure to winter cold and desiccation. By contrast, pines in tropical regions sometimes shed their needles throughout the year. The intermediate case is found in middle latitude pines that change color and shed needles twice per year, namely during spring and autumn (Oohata, 1986).

Larch is well known as a deciduous conifer (Gower and Richards, 1990). However, lower branches of alpine larch (Larix lyallii) keep needles over winter when the moisture content in the soil is adequate (Richards, 1984). Similar overwintering capacity is also found in needles of larch seedlings (L. gmelinii and L. decidua) growing in heavy snow regions (Miyoshi, 1934; Koike, 2002). Before needle shedding, aged needles (usually one-year-old needles) change color from green to yellow and mobilize their nitrogen to new needles. This summer yellowing of overwintering needles of larch seedlings seems to be induced by desiccation in the soil rhizosphere. Leaf abscission starts in most tree species of different leaf habit (e.g., deciduous, evergreen, and marcescent) at a time of insufficient soil moisture (Escudero and del Arco, 1987). Marcescent tree species, such as oak (Quercus dentata) and carpinus (Carpinus cordata), usually hold their dead leaves until new leaves are unfolding and are apparent exceptions; however, it is believed that the transpiration stream is sealed off in these dead leaves and they protect leaf primordia from desiccation by the strong dry winds during winter and salt spray near seashores. In fact, Q. dentata is a major component of forest stands close to seashores.

Under mild stress conditions, leaf longevity usually increases. For instance, leaf longevity is greater in plants growing on infertile soils (Escudero and Arco, 1987; Koike and Sanada, 1989; Reich et al., 1992, 1995; Kayama et al., 2002). In fact, Sobrado (1991) found a ratio of leaf construction cost to maximum assimilation (costMmax where Amax is the maximum photosynthetic rate at light saturation) as a function of leaf life-span. In general, the decline in photosynthetic rate once it reaches its maximum value is rapid for most light-demanding species, while that in shade-tolerant species is slow (Koike, 1988,1991; Reich etal., 1995). Moreover, based on the rate of decline in photosynthesis with increase in time, the longevity of individual leaves was estimated as a function of the cost and benefit of construction of a leaf (Kikuzawa, 1991; Chapter 25). Therefore, leaf shedding should be found when the surplus production of older leaves would be less than the maintenance cost of older leaves and new leaf production.

However, leaflongevity is sometimes diminished by various kinds of stresses. Leaf habit (i.e., evergreeness or deciduousness) is dependent on the specific survival strategy in a forest stand or tundra where the availability of resources is different (Chapin et al, 1990; Chapin and Kedrowski, 1983).

C. Leaf Nitrogen Content and Light Environment

Leaf nitrogen reflects photosynthetic activities (e.g., Evans, 1989; Ono et al, 2001). The foliar nitrogen content in leaves of various deciduous broad-leaved trees native to North America decreases with age (Cote and Dawson, 1986). As the salt-extractable protein of leaves in eastern cottonwood (Populus deltoides) and white basswood (Tilia heterophylla) decreases, the free amino acids increase. Usually, plants keep more of their nutrients in their body when they grow under infertile soil conditions. In fact, the remobilization rate of leaf nitrogen was lower for black alder and cottonwood grown in fertile conditions compared with those in infertile conditions (Cote et al., 1989).

Apple (Malus domestica) also shows no special autumn coloration, but its green period is elongated by nitrogen supplied at the beginning of autumn (Millard and Thomson, 1989). In the active phase, allocation of leaf nitrogen to ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) is usually around 20% for wild plants (Evans, 1989; Evans and Seeman, 1989) or 15-30% for several crop plants (Makino et al., 1992). In autumn, degradation of Rubisco in leaves accounted for between 32 and 48% of the nitrogen subsequently remobilized and stored for leaf growth in the following spring. Most leaf protein is degraded and amino acids are exported from the leaf for storage over the winter as protein in bark (e.g., Chapin et al., 1990; Ono et al., 2001). This mobilization process of nitrogen is recognized as internal cycling of nitrogen (Chapter 14) and is more prominent in infertile conditions (Killingbeck, 1996).

Leaf nitrogen concentration is positively correlated with the maximum photosynthetic rate in many plant species (e.g., Evans, 1989). Generally, plants arrange their active leaves with high nitrogen content at the surface of the canopy, exposed to maximal sunlight. Field (1983) simulated that distribution of leaf nitrogen content that maximizes photosynthetic carbon gain over the canopy of an entire plant. The optimal nitrogen content increases with increasing daily photosynthetically active photon irradiance. Studies on Solidago sp. (Hirose and Werger, 1987) supported these results. Furthermore, the distribution of leaf nitrogen in a plant depends on the light environment for the leaf (Hikosaka et al., 1994). If an aged leaf of the herbaceous vine Ipomoea tricolor receives adequate light flux under fertile conditions, the nitrogen content of the leaf is almost the same as that of active young leaves.

Similar nitrogen distribution patterns have been reported for a canopy of Scotch pine (Pinus sylvestris) grown in eastern Siberia where the tree density was very low (Koike et al., 1999). The sparse pine stand on permafrost provides enough light flux in the deeper part of a pine crown, which means that most of the needles of a crown can receive enough light flux for photosynthesis. In fact, the nitrogen content of 8-year-old needles was almost the same as that of 2-year-old needles. Content of calcium in needles is found to increase with increasing needle age.

However, in autumn, the nitrogen concentration of individual leaves showed a specific pattern in the canopy of deciduous, broad-leaved trees (Koike et al., 1992). The leaf nitrogen content of early-successional trees with inderminant type (e.g., birch and alder) decreased from leaves located at the base of a shoot or stem, while that of late-successional trees with determinant type (e.g., maple, basswood and beech) decreased from the surface of a crown or the canopy top (Fig. 16-2). That is, the nitrogen content in the basal leaves of determinant type species of leaf flush is less than that in the apical leaves. The former pattern is commonly found for most crop plants and many conifers. By contrast, the latter pattern is only observed for late-successional tree species with a deciduous leaf habit, especially for leaf flush type species.

In the crown of an alder (Alnus hirsuta) sapling, aged leaves positioned near the stem start to shed from mid-July without any yellowing (Kikuzawa, 1978; Koike et al., 2001). The rest of the leaves usually remain green until frost comes, at which time they are shed green. This earlier leaf shedding is recognized as a structural specialization in shoots of alder species (Kikuzawa, 1983), but this unique trait is partly stimulated by self-shading from younger leaves. Moreover, the above-mentioned pattern of nitrogen distribution in a canopy of early

Figure 16-2. Seasonal changes in net photosynthetic rates of individual leaves with different leaf emergence patterns. Numbers in figures mean the leaf order from shoot base.

and late successional tree species and progress of autumn coloration are usually found for a whole canopy of trees exposed to full sunlight. However, trees in a forest sometimes do not clearly show this pattern of autumn coloration in their crowns, because their lower canopy receives little strong sunlight. In fact, full autumn coloration requires strong sunlight to promote anthocyanin synthesis (Feild et al, 2001). The development of autumn coloration in tree crowns seems to be adapted to maximize photosynthetic production of the canopy of the tree.

In the next section, we will consider the relationship between the progress pattern of autumn coloration and leaf structure in deciduous broad-leaved trees.

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