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JUVENILE FOLIAGE AND THE SCALING OF TREE PROPORTIONS, WITH EMPHASIS ON EUCALYPTUS.

INTRODUCTION

The occurrence of juvenile foliage in seedlings and saplings has been noted across a wide taxonomic range of trees (Kozlowski 1971) and is particularly evident in the genus Eucalyptus, where juvenile leaf characters are often used to distinguish species with similar adult foliage (Pryor 1976). Many species show changes in the shape, anatomy, and physiology of successive leaves along the stem (Ashby 1948, Cameron 1970). This change of phase may be gradual or abrupt in species termed heteroblastic (Allsopp 1967). Juvenile leaves of trees are frequently thinner and more nearly horizontal than adult leaves. Among vines which climb trees from the understory to the canopy, ontogenetic changes in leaf morphology correspond to increases in irradiance and have been interpreted as adaptations to shifts in light level and heat balance (Givnish and Vermeij 1976, Hoflacher and Bauer 1982). This view is supported by observations that, in some species, transferring plants to shade may arrest the shift to the adult phase (Allsopp 1967, Lee and Richards 1991).

However, the occurrence of distinctive juvenile foliage in young plants is not restricted to those grown in shade, particularly in the case of eucalypts, which are generally intolerant of shade and frequently regenerate following wildfires (Florence 1996). The observation of increases in leaf mass per area with increasing plant age, independent of changes in light level (Steele et al. 1989, Niinemets 1997a), suggests that additional factors besides light are involved in ontogenetic shifts in foliar properties. Among woody plants, changes of phase have been linked to the physiological age and size of the apical meristem (Allsopp 1967), which are in turn correlated with plant size. The differential scaling of surface area, mass, and mechanical stresses has been used to explain allometric patterns in animal body shape (Schmidt-Nielsen 1984), stem form (Givnish 1995), and the proportion of leaf tissues devoted to support (Givnish 1986). Differential scaling may also influence other foliar properties.

This paper develops an additional functional explanation for juvenile foliage, based on the fact that mechanical support costs increase more rapidly with plant size than does crown area. Small seedlings allocate more biomass to leaves than to stems (Sands et al. 1992), while the reverse pattern occurs for canopy trees. Because surface area increases as the square of height or width, whereas volume and mass increase as the cube of linear dimensions for objects of given shape, stem mass is expected to increase more rapidly than leaf mass. Thus, an isolated seedling can pursue the option of increasing light interception by spreading a given leaf mass over a larger area by producing thin, nonoverlapping leaves, while responding to relatively modest crown support requirements. In contrast, a canopy tree would require large increases in woody tissue were it to substantially increase its crown area.

The functional importance of the scaling of support costs is analyzed by calculating the foliar configuration maximizing growth with a simple model of production and support that balances mechanical support costs against the benefits in light interception and light use efficiency associated with a given foliar geometry. Such cost-benefit analyses have been applied to a range of plant adaptations (e.g., Parkhurst and Loucks 1972, Givnish 1986). To keep the problem tractable, I assume that leaf dry mass per unit area (LMA) and leaf area per unit crown area (LAI) can vary, but that other foliar attributes, such as leaf angle and chemical composition, are fixed. By including variation in LMA, the approach extends that of Yamamura (1997), who used an allometric model to show that increases in LAI with increasing plant mass are associated with the growth pattern maximizing light interception. The approach recognizes that the morphological development of the individual results from the genetic control of physiological processes, as modified by the internal and external environment (Poethig 1990), but assumes that this developmental sequence has been shaped by selection to increase growth and survival under certain environmental conditions. The prediction that young seedlings of favorable environments should have sparse crowns of thin leaves is shown to be robust over a range of model formulations.

THE MODEL

The calculation of optimal foliar attributes as a function of plant size and life stage is accomplished by first developing relationships for support costs and biomass production. I then consider the case of an open-grown seedling of given mass and address the question of how that mass should be configured so as to maximize biomass production, given the above relationships. A number of simplifying assumptions are made regarding crown shape and environment to isolate the influence of scaling effects on the costs and benefits of particular foliar configurations.

Relationship between crown size and support costs

Allometric studies indicate that the relationship between stem and branch biomass and plant size gradually shifts over the full size range of plants (Bertram 1989). Stem diameter commonly scales as plant height raised to a power of [less than or equal to]1 for seedlings and saplings, but increases with height raised to an increasingly higher power among canopy trees and emergents (Kohyama 1987, Farnsworth and Niklas 1995, Niklas 1995, King 1996b, Thomas 1996). As the ratio of water-conducting sapwood area to total stem cross-sectional area, and the relative impacts of wind, gravity, and falling debris all vary with plant size, corresponding shifts in allometry are not unexpected. Thus, larger trees appear to follow the design principles of elastic similarity (d [varies] [h.sup.1.5]) or stress similarity (d [varies] [h.sup.2]), while saplings fall closer to geometric similarity (d [varies] [h.sup.l]) (Farnsworth and Niklas 1995).

Trunk diameter was related to both crown proportions and height by King (1996b), who found that

[Mathematical Expression Omitted] (1)

where [d.sub.0.1] is trunk diameter at 0.1 of total tree height h, [w.sub.cr] is crown width, a is a constant, and the exponents are mean values for 14 species derived from multiple regressions fit to 1-6 m tall understory saplings in a tropical forest. (See Table 1 for symbol definitions.) If the total biomass of stem and branches (S) is proportional to [Mathematical Expression Omitted], then Eq. 1 implies that [Mathematical Expression Omitted]. A slightly different formulation is used here,

[Mathematical Expression Omitted] (2)

as this expression reduces to the simple case of geometric similarity (S [varies] [h.sup.3]) when applied to saplings with a fixed ratio of crown width to plant height. Eq. 2 is used with the cautions that it applies to saplings and not trees (for which S increases more rapidly with height) and that possible influences of variation in leaf area per unit crown area (LAI) and leaf thickness on branch thickness are not included.

Relationship between crown and foliage characteristics and production

A useful approach that separates the influence of crown geometry and leaf properties is to define production as the product of light interception and light use efficiency (LUE), defined as biomass production per unit light interception (Cannell et al. 1987). Light interception can then be calculated as a function of crown area and LAI (which influences light interception per unit crown area), whereas light use efficiency is related to the photosynthetic parameters varying with leaf mass per area (LMA).

Reported relationships between photosynthesis and LMA vary substantially, depending on how photosynthetic enzymes and leaf nitrogen vary with LMA (Evans 1989). Studies of within-species variation in leaves grown under different light levels have found that the maximum rate of photosynthesis per unit area ([A.sub.max]/area), LMA, and leaf nitrogen content per unit area (N/area), often increase in proportion to each other with increasing light level, while N/mass remains more [TABULAR DATA FOR TABLE 1 OMITTED] nearly constant (Ellsworth and Reich 1992, 1993, Niinemets 1997b). On the other hand, comparisons of leaves of different species with contrasting leaf life spans show less variation in [A.sub.max]/area with LMA, but in this case N/mass declines with increasing LMA and leaf life span (Reich and Walters 1994). Thus, [A.sub.max]/area may be proportional to LMA or N/area for leaves of a given species and chemical composition, but not for leaves of different species with differing LMA. As the emphasis here is on how size influences the costs and benefits of different foliar configurations, I assume that the chemical and enzymatic content of leaf tissue (per unit mass) remains constant, but that the arrangement of this tissue in leaves and crowns may vary with plant age. This assumption is supported by observations of constant N/mass in 6-16 mo old Eucalyptus grandis plants that increased in LMA over this timespan (Leuning et al. 1991) and concurrent increases in photosynthetic capacity and LMA over the first several months of growth in E. fastigata (Cameron 1970).

The assumption of constant chemical composition then implies a curvilinear relationship between light use efficiency and LMA, based on the results of canopy models that predict curvilinear relationships between LUE and either [A.sub.max]/area or N/area (Sinclair and Horie 1989, Sinclair and Shiraiwa 1993, Kirschbaum et al. 1994, Sands 1996). These model results are consistent with analyses of crop growth showing that LUE approaches an upper asymptote as leaf N per unit area exceeds 2 g/[m.sup.2] (Muchow 1990, Wright et al. 1993). The reason for this curvilinear relationship is that the canopy shifts from being light saturated over most of the day at low [A.sub.max] to unsaturated at high [A.sub.max]. When the canopy is light saturated, photosynthesis increases linearly with [A.sub.max], whereas the photosynthesis of an unsaturated canopy depends primarily on the quantum efficiency or slope of the light response curve and increases little with further increases in [A.sub.max].

This curvilinear relationship between LUE and LMA is specified with the nonlinear hyperbolic function:

[Theta][(LUE).sup.2] - (sLMA + [LUE.sub.max]) LUE + s(LMA)[LUE.sub.max] = 0 (3)

where s is the initial slope of the curve, [LUE.sub.max] is the maximum value of LUE approached by very thick leaves, and [Theta] is a shape parameter defining the curvature of the relationship, with [Theta] = 0 specifying a rectangular hyperbola and [Theta] = 1 specifying a linear increase in LUE until [LUE.sub.max] is attained [ILLUSTRATION FOR FIGURE 1 OMITTED]. LUE relationships specified by other canopy models can be approximated by varying [Theta] between 0 (Kirschbaum et al. 1994) and 0.83 (Sands 1996), and an intermediate value of 0.5 was chosen for subsequent calculations. A more detailed formulation would include the possibility that LUE is zero for a very thin, minimally designed leaf (Gutschick and Wiegel 1988), but this complication does not affect the overall patterns predicted by the model.

Case 1: Open-grown juvenile with no leaf loss

Consider a seedling, not shaded by neighbors, with a certain aboveground biomass that is divided between leaves and woody support tissues. The seedling is young and has not yet begun to shed leaves, so relations between leaf mass per area (LMA) and leaf life span need not be considered. The question of interest is how does the productive capacity of the seedling vary with its leaf area per unit crown area (LAI) and LMA, given the allometric constraints and production relations described thus far?

To simplify the analysis I assume that crown shape and leaf orientation are fixed, but that LAI and LMA may vary. In this case, the total biomass of aboveground support tissue, given by Eq. 2 reduces to

S = [c.sub.1][h.sup.3] (4)

where the constant [c.sub.1] depends on crown shape and the relationship between stem cross sectional biomass and crown area. If seedling leaf biomass L is expressed as a fraction f of total aboveground biomass W, i.e., L = fW, then S = (1 - f)W. Thus, seedling height can be expressed as a function of aboveground biomass and the fraction of that mass in leaves as

h = [[(1 - f)W/[c.sub.1]].sup.1/3] (5)

Seedling crown area is proportional to [h.sup.2] and is given by

[A.sub.cr] = [c.sub.2][[(1 - f)W/[c.sub.1]].sup.2/3] (6)

where the constant [c.sub.2] = ([Pi]/4)[(crown width/h).sup.2].

The leaf area index of the crown is defined as LAI = leaf area/crown area. Noting that leaf area = fW/LMA,

LAI = fW/([A.sub.cr]LMA). (7)

Daily aboveground biomass production is then specified in terms of the product of light interception and light use efficiency as

B = I[A.sub.cr](1 - [e.sup.-k[multiplied by]LAI]) LUE (8)

where I is average daily irradiance and k is the light extinction coefficient in the Beers law light interception formulation commonly used in simple production models (e.g., Sands 1995). As [A.sub.cr], LAI, and LUE are given respectively by Eqs. 6, 7, and 3, in terms of W, f and LMA, B is also a function of the latter variables.

Case 2: Mature forest tree with leaf turnover

Consider a mature forest tree with neighbors of similar height. In this case the branches and stem weigh much more than the current foliage and changes in foliar allocation have little impact on crown size over the life span of the leaves, particularly when the crown is constrained by neighboring trees. Thus, the foliar configuration maximizing production per unit crown area also maximizes whole tree production, unlike the previous case where foliar mass and crown area were linked. Eq. 8 was modified to give daily production per unit crown area as

[B.sub.A] = I(1 - [e.sup.-k[multiplied by]LAI])LUE (9)

where LUE is given by Eq. 3, and foliage mass per crown area (LMA x LAI) is determined by the balance between the production and loss of foliage.

The shedding of leaves lowers the net productivity of trees relative to young seedlings. If leaf production equals loss, then [a.sub.F][B.sub.A] = [c.sub.loss]LMA x LAI, where [a.sub.F] is the fraction of aboveground biomass production allocated to leaves and [c.sub.loss] is the fraction of leaf mass lost per day, i.e., the reciprocal of leaf life span. Rearranging the expression for leaf mass balance yields

[a.sub.F] = [c.sub.loss] LMA x LAI/[B.sub.A] (10)

and the net aboveground production available for reproduction and long-term crown extension is then

[B.sub.N] = (1 - [a.sub.F])[B.sub.A]. (11)

Model application

The model parameters were estimated for young Eucalyptus grandis. This species tends to occur on moist, fertile soils of the mild coastal region of central eastern Australia (Boland et al. 1984), and, thus, its growth is typically less limited by environmental stresses not included in the model. Model parameters, given in Table 1, were based on intensive studies of a young E. grandis plantation (Leuning et al. 1991, Cromer et al. 1993). The predictions for adult forest trees were compared to those for juveniles by using the same model parameters for light use efficiency in both cases. The loss coefficient [c.sub.loss] in Eqs. 9 and 10 was set equal to 1/365 [d.sup.-1], given that E. grandis leaves live for about one year (Cromer et al. 1993).

RESULTS

Open-grown juveniles with no leaf loss

The predicted biomass production for small vs. large plants is shown as a function of leaf mass per area (LMA) and the fraction of aboveground biomass in leaves (f) in the contour plots of Fig. 2. Production is within 10% of the maximal value over a substantial range in LMA and f but the position of the maximum shifts substantially as a function of plant size. This optimum set of LMA and f values represents a tradeoff between increasing crown area (which reduces foliage mass because of increased support requirements) and increasing foliage mass (which reduces branch mass and, hence, crown area, but increases foliage mass per unit crown area [LMA x LAI], thereby increasing light use efficiency and light interception per unit crown area). Because support mass increases with the three-halves power of crown area over the size range considered here in the current study, an increase in crown area requires a greater shift in allocation from foliage to support in large plants. Thus, the

option of increasing crown area by decreasing (LMA x LAI) becomes less advantageous with increasing plant size. The fractional allocation to support (1 - f) for the optimal strategy still increases with plant size, but at a slower rate than would be the case for constant foliage mass per crown area.

The predicted optimal LMA, f and corresponding LAI, are plotted as a function of plant mass in Fig. 3. The predicted trend of decreasing f with increasing plant mass is similar to that determined for E. grandis seedlings by Sands et al. (1992). Predicted and observed LMA's also increased to a similar extent with increasing plant mass [ILLUSTRATION FOR FIGURE 3 OMITTED]. The predicted course of growth over 16 mo is shown in Fig. 4 for a plant that increases its LAI and LMA with time so as to maintain these parameters at the optimum values maximizing each day's growth. Final plant mass is [approximately]20 x that predicted for plants that maintain the optimal LAI and LMA for an aboveground biomass of either 10 mg or 10 kg. Thus, shifting foliar attributes with plant size in accordance with allometric constraints can have substantial impacts on growth. Growth is not projected past 16 mo, as the model assumption that the plant retains all its foliage is increasingly violated thereafter.

The general prediction that the LMA and LAI that maximize growth rate increase with seedling size follows from a broad range of model formulations, although it is restricted to young plants with most of their initial foliage. A critical model relationship is the scaling of support costs. If support mass increases proportionately faster than crown area, i.e., a [greater than] 1 in the relationship [Mathematical Expression Omitted], then the optimal LMA and LAI are expected to increase with plant mass, whereas the reverse is true for the unlikely case that a [less than] 1 [ILLUSTRATION FOR FIGURE 5 OMITTED].

The assumed relationship between light use efficiency (LUE) and LMA also influences predicted patterns, as shown by changing the shape parameter 0 of Eq. 3. Over the range 0-0.8, 0 has little effect on the predicted LMA [ILLUSTRATION FOR FIGURE 6 OMITTED]. ln the extreme case where [Theta] [approaches] 1 and the curvature in the LUE curve becomes increasingly sharp [ILLUSTRATION FOR FIGURE 1 OMITTED], the predicted effect of plant size on LMA declines to zero, while the effect on LAI increases somewhat [ILLUSTRATION FOR FIGURE 6 OMITTED]. Increasing the initial slope s of the model relationship between LUE and LMA (for fixed [LUE.sub.max]) decreases the predicted optimal LMA and LAI [ILLUSTRATION FOR FIGURE 7 OMITTED]. Because changes in s have approximately the same proportional effect on predictions for large and small plants, however, the predicted trends in crown properties are little effected by the value chosen for s.

Mature forest trees with leaf turnover

The net aboveground production predicted for forest trees is maximized by a high LMA and LAI [ILLUSTRATION FOR FIGURE 8 OMITTED] compared to that expected for seedlings [ILLUSTRATION FOR FIGURE 2 OMITTED], as increasing light interception by increasing crown area is no longer an option in trees constrained by neighbors. The predicted optimal LMA of 187 g/[m.sup.2] was greater than the value of 114 g/[m.sup.2 reported for 16-mo-old E. grandis saplings (Leuning et al. 1991), but similar to the value of 190 g/[m.sup.2 noted for fallen green leaves from a mature E. grandis tree in Canberra, though the latter was outside the natural range of the species. The predicted optimum LMA increases with increased leaf longevity, as leaf replacement costs are then reduced. As was the case for seedlings, the surface describing production is quite flat near the predicted optimum. Thus, factors not included in the model and errors in assumptions could shift the optimum LMA and LAI substantially. On the other hand, the fact that the same formulation for light use efficiency and light interception for trees vs. seedlings gave rise to large differences in predicted LMA and LAI supports the hypothesis that allometric constraints influence leaf and crown properties.

DISCUSSION

The hypothesis that the scaling of mechanical support costs favors a shift from thin juvenile leaves to thicker (greater leaf mass per area [LMA]) adult leaves as plants grow in size is supported by the model's predictions that leaves with low leaf mass per area maximize growth rates in small plants, but not larger ones [ILLUSTRATION FOR FIGURE 2 OMITTED]. These predictions are in approximate agreement with reported increases in LMA with increasing plant size and age in the Eucalyptus grandis saplings to which the model was applied [ILLUSTRATION FOR FIGURE 3 OMITTED]. Restrictions on the predictions and their relation to observed patterns of development and other hypothesized explanations for phase changes are now discussed.

Applicability of the predicted patterns

The predicted increases in leaf area per crown area (LAI) and leaf mass per leaf area (LMA) with increasing plant size are limited in application by the restrictions assumed in deriving them. The analysis of tradeoffs between crown area and foliar characters assumed that leaf senescence had not yet occurred and did not consider other functions of LMA besides its contribution to photosynthetic capacity. The prediction of lower LMA in small vs. large plants is therefore restricted to young plants and is less applicable to older, suppressed seedlings of closed canopy forests.

The calculation of the foliar configuration maximizing growth as a function of plant biomass was based on the implicit assumption that past growth history does not constrain current LMA and LAI, i.e., that these variables can be shifted by the plant over time to track the optimal values. Because the optimal growth pattern involves a gradual increase in LMA and LAI as plant mass increases [ILLUSTRATION FOR FIGURE 3 OMITTED], this growth trajectory may be relatively easy to achieve by placing new leaves both above and beside old ones, and thickening leaves over time or initiating successively thicker leaves. As a seedling grows, the mean age of its leaf tissues increases. This increase in mean leaf age is associated with an increase in the age of the oldest leaves and a decrease in relative growth rate and, hence, the relative rate at which new leaf tissue is added. Thus, the optimal LMA could in principle be maintained by increasing the LMA of each individual leaf over time.

LMA generally increases after leaf expansion (Jurik 1986, Reich et al. 1991b), but this process may be limited by the fixed arrangement of cells in mature leaves. Observations of progressive increases in both number of cell layers and LMA among successive leaves (Cameron 1970), and greater LMA in adult vs. juvenile leaves on plants with both phases (Pereira et al. 1989), suggest that ontogenetic shifts associated with phase change may have a greater influence on crown LMA than developmental changes within aging leaves.

Comparison with observed patterns

A greater than two-fold increase in leaf mass per area (LMA) over the range of light levels encountered in forests is well established for shade tolerant species (Ellsworth and Reich 1992, 1993, Niimenets 1997b). The current study suggests that ontogenetic increases in LMA of similar size could occur in seedlings growing to adulthood under fixed light environments. Reported LMA values for juveniles are consistently lower than those for trees of the same species, compared under similar light and growth conditions, as shown in Table 2. As most of the values for juveniles in Table [TABULAR DATA FOR TABLE 2 OMITTED] 2 are for [greater than]1-yr-old, larger differences would be expected had younger seedlings been included in these studies. This expectation is supported by observations of increases in LMA with increasing plant mass in herb and eucalypt seedlings over the first several months of growth (Hughes 1965, Cameron 1970, Ashton and Turner 1979, Kohyama and Hotta 1986, Poorter and Pothmann 1992). LMA values of 40-70 g/[m.sup.2 have been reported for 2-4 mo old glass house grown Eucalyptus seedlings exposed to full light (Ashton and Turner 1979, Mowart and Myerscough 1983, Sands et al. 1992), less than one-third of the values for adult eucalypts (Table 2). The absence of wind and higher humidity of glass houses may have contributed to these low values for seedlings, but the trend of increasing LMA over time in both seedlings of controlled environments and older field plants indicates pronounced ontogenetic shifts in eucalypts.

The predicted differences in leaf area per crown area (LAI) between seedlings and trees are more difficult to evaluate, as LAI is customarily reported for whole canopies rather than for individual plants. Values of LAI [less than or equal to]1 are expected for seedlings in the two to six leaf stage when little leaf overlap occurs (Niklas 1988), whereas LAI values of 1.2-2.8 have been reported for 1-2 m tall open-grown saplings (Shukla and Ramakrishnan 1984, O'Connell and Kelty 1994, Bignami and Rossini 1996). The observation of substantially higher LAI values for plantation trees than open-grown saplings of Pinus strobus (Bolstad and Gower 1990, Vose and Swank 1990, O'Connell and Kelty 1994) is also consistent with the prediction of higher LAI in canopy trees [ILLUSTRATION FOR FIGURES 3 AND 8 OMITTED].

Other factors influencing LMA and juvenile leaf properties

The general agreement between observed and predicted trends in leaf mass per area (LMA) does not rule out the involvement of other factors in ontogenetic changes in leaf properties.

Alternative functional explanations for the observed trends are as follows: (1)juvenile leaves increase the shade tolerance of young plants that show this adaptation to shade even when grown in full sun, (2) LMA increases with leaf size due to an increase in the proportion of tissues allocated to supporting veins, (3) LMA increases with plant height in response to increased water deficits, and (4) LMA increases in concert with other morphological changes that deter herbivores, because size related decreases in relative growth rate increase the impacts of herbivory as trees grow.

1) The pronounced differences in the leaf morphology of young vs. old Picea sitchensis reported by Steele et al. (1989; shown in Table 2) were interpreted as an adaptation to shade in juveniles, although all measured leaves had developed in full light. Greater shade tolerance in juveniles than adults has been reported for P. sitchensis (Cary 1922), and whole plant light compensation points generally increase with plant size because of proportionately greater maintenance and structural costs in larger plants (Givnish 1988). Thin juvenile leaves would further this trend by increasing light interception per unit leaf mass in small plants. However, the rapid initial growth rates of many Eucalyptus species in full light (e.g., Leuning et al. 1991) support the hypothesis offered here that thin, spreading leaves on small plants with low support costs enhance growth rates. Thus, the production of thin juvenile leaves may lead to both greater shade tolerance and faster growth under favorable conditions.

2) The fraction of leaf biomass allocated to supporting veins and petioles increases with leaf size, as expected from considerations of mechanical support requirements (Chazdon 1986, Givnish 1986). Thus, LMA, defined as total leaf mass per area, should also increase with leaf size. However, the fraction of biomass allocated to veins appears to be rather small in most tree species, limiting the influence of this factor on LMA. Another limitation is that increases in LMA may only be correlated with increases in leaf size during the earlier stages of growth when the size of successive leaves is increasing.

3) Height-related increases in LMA have been viewed as adaptations to withstand increased water deficits in taller trees (Kull and Niinemets 1993, Niinemets 1997a). The increase in hydraulic resistance to water flow in old vs. young trees has been proposed as an important factor limiting the height growth and productivity of aging forest stands (Ryan and Yoder 1997). However, increases in hydraulic resistance have been primarily associated with aging adult trees, rather than phase changes occurring earlier in life (Mencuccini and Grace 1996), as considered here.

4) The differential effect of herbivory on fast vs. slow growing plants may select for size-related shifts in LMA and other leaf properties. A given rate of herbivory will have proportionately smaller effects on plants with high relative growth rates (RGR), because their rapid exponential growth results in rapid replacement of eaten tissue (Coley 1988). Inherently slow-growing species generally exhibit greater defenses against herbivores, including greater leaf toughness, fiber content and LMA, and lower leaf protein and N/mass (Coley 1983, Lambers and Poorter 1992, Turner 1994). Within similar light environments, RGR declines with increasing plant size because of the scaling of mechanical support requirements outlined here. Ontogenetic changes in leaf properties may thus parallel the differences noted between inherently fast- and slow-growing species, with age related increases in LMA reflecting increased exposure to herbivory, in turn caused by allometrically driven decreases in RGR. This hypothesis is supported by the ontogenetic changes in leaf anatomy observed in the more heteroblastic Eucalyptus species, which shift from soft juvenile leaves with loosely packed cells to leathery adult leaves with tightly packed cells (Johnson 1926, Penfold and Willis 1961, Cameron 1970).

Thus, plant size may influence LMA in two ways: by directly affecting the costs and benefits of spreading out photosynthetic material, as assessed here, and by influencing RGR and associated costs of herbivory. These factors are complimentary, as increases in LMA as plants grow may increase resistance to herbivores and/or mechanical damage while maintaining an optimal allometry for growth.

Further research needs

Both empirical studies and further model development are needed to distinguish the influence of size effects on support costs from other factors affecting phase changes in developing plants. Although ontogenetic patterns in leaf properties have been reported, most studies have emphasized the obvious influence of light environment on leaf development. Studies of developmental patterns in LMA, LAI, and biomass allocation would provide more rigorous tests of the scaling hypothesis presented here. Increases in leaf toughness and decreases in nutrient concentrations are associated with the alternative hypothesis that size effects on relative growth rate (RGR) and herbivore impacts select for shifts in leaf properties. Measurements of developmental patterns in leaf nutrient concentrations and structural characteristics would thus aid in evaluating the relative importance of these two size-related factors.

The model presented here considered the influence of plant geometry on current growth rates in idealized plants suffering no losses to herbivores. However, if LMA influences subsequent herbivory and leaf longevity (Reich et al. 1991a), then the production of thin, poorly defended leaves maximizing current growth may lead to decreased future growth and survival. Optimization problems where current growth patterns affect future capacities can be solved with optimal control theory (e.g., Iwasa and Cohen 1989), a standard example being the scheduling of reproductive vs. vegetative growth in annual plants (e.g., Vincent and Pulliam 1980). This approach is needed to extend the model from the young plants considered here to older juveniles where leaf life span and RGR dependent herbivory effects may be more important.

The widespread occurrence of juvenile foliage with low leaf mass per area (Table 2) suggests that the scaling constraints considered here may be common to most plants. However, interspecific differences in the juvenile phase also occur and may affect both plantation growth (King 1996a) and forest dynamics (Noble 1989). In Southeastern Australia, eucalypts of the section Maidenaria generally outgrow species of the section Obliquae during the first several years, but this trend is reversed in older stands (Duff et al. 1983, Cotterill et al. 1985). Most members of the Maidenaria bear distinctive, sessile juvenile leaves that are produced up to a height of 5 m in the case of the important plantation species, E. globulus and E. nitens, and those populations with the longest juvenile phase show the greatest early growth (Beadle et al. 1989). Interspecific comparisons of LMA, LAI, leaf angle, and light interception in plants of a range of ages are needed to evaluate these trends and would aid in the selection of traits for fast growing plantation trees.

ACKNOWLEDGMENTS

I thank Owen Atkin, Hans de Kroon, John Evans, Paul Kriedemann, and two anonymous reviewers for helpful critiques of the manuscript.

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