Plant height reflects strategy for securing carbon profit via light capture (Grime et al. 1988; Weiher et al. 1999; Westoby et al. 2002). As taller plants shade shorter plants, competition favours additional expenditure on stems, opening an evolutionary arms race for light (Givnish 1982; Iwasa et al. 1985; Falster & Westoby 2003). However, not all plants are equally tall: in tropical vegetation; for instance, species potential (or maximum) height ranges from 1 to over 50 m (Foster & Janson 1985). Consequently, much of the emphasis in recent work has been on understanding the trade-offs associated with increased height that allow shorter species to persist in vegetation (e.g. Thomas 1996; Thomas & Bazzaz 1999; Turner 2001; Kohyama et al. 2003; Poorter et al. 2003).
Overall, there is growing consensus that species spread out along (at least) two axes summarizing light capture strategy (Fig. 1, Loehle 2000; Pacala & Deutschman 1995; Westoby 1998; Thomas & Bazzaz 1999; Sterck et al. 2001; Turner 2001; Poorter et al. 2003). The first corresponds to a vertical light gradient, comparing species at a point in time. Taller species capture a disproportionate share of available light (Hirose & Werger 1995; Kohyama 1993) but are restricted either in leaf area ratio or by poor sapling survival and performance in low light conditions (Iwasa et al. 1985; Givnish 1988; Aiba & Kohyama 1997; Thomas & Bazzaz 1999; Kohyama et al. 2003), opening an opportunity for shorter species to succeed.
The second axis known to be important for coexistence among height strategies extends through successional time (Fig. 1, Huston & Smith 1987; Shugart 1984; Pacala & Rees 1998). Following disturbance (removal of above-ground biomass), early successional species gain access to light pre-emptively via rapid height growth and superior colonization of vacant space. The requirements for rapid height growth bring with them increased risks of herbivory (Coley 1988), pathogen infection (Augspurger & Kelly 1984), mortality (Loehle 1988; Dalling et al. 1998; Davies 2001) and decreased shade-tolerance (King 1994; Kitajima 1994; Davies 1998). Due to decreased longevity and poor performance in low-light environments, early successional species are prevented from monopolizing time spent at the top of the canopy.
Species coexistence along the vertical axis is facilitated via trade-offs in realized productivity between high- vs. low-light environments. Along the successional axis, coexistence arises via trade-offs between the pace of height gain vs. longevity and shade tolerance (Huston & Smith 1987; Pacala et al. 1996; Pacala & Rees 1998). In each case, the trade-off may be manifested strategically via variation in several other key traits. For the light gradient at a point in time, relevant traits are expected to be coordinated with potential height (Thomas 1996). Species replacement during succession, however, also corresponds to an overall increase in potential height (Fig. 1, Gómez-Popma & Vászquez-Yanes 1981; Navas et al. 2003) leading to an alternative prediction for trait correlations with height. In principle, the nature of these correlations (their slopes and intercepts on bivariate plots) could differ depending on which gradient was being considered, reflecting the different strategic trade-offs associated with each axis.
The primary aim of the current study was to compare trait relationships with potential height among sets of species selected to span successional and vertical light gradients (Fig. 1). Several authors have reported correlations with one or another trait among species spanning one of the gradients (e.g. Thomas & Bazzaz 1999; Kohyama et al. 2003), but to our knowledge the two gradients have not yet been explicitly compared. Our working hypothesis was that trait relationships (if present) would differ between sets of species spanning each gradient, with tighter (higher r2) relationships observed among species spanning one of the gradients than across the entire species complement.
Several leaf, wood, architectural and reproductive traits were chosen for study (summarized below). These traits are informative about height strategy because of their influence on height growth, on longevity or on growth at low light. Our list is by no means exhaustive; it was limited by resources and by the design imperative to quantify traits across significant numbers of species in the field. Summaries of each trait and expected relationships with potential height are provided in Table 1.
|Trait||Description||Hypothesized correlation with potential height|
|(a) Successional gradient||(b) Vertical light gradient|
|LMA||Leaf mass area−1 (mg mm−2)||+ ve: height growth rate||(1) + ve: maximize light interception |
(2) − ve: resource conservation
|Nmass, area||Nitrogen leaf mass−1 or area−1 (mg N mg−1 or mm−2)||− ve: height growth rate||+ ve: light level|
|WD||Wood density (mg mm−3)||+ ve: height growth rate; longevity||– ve: hydraulic conductance; vertical growth|
|Stem extension rate (mm mm−1 day−1), comprised of:||– ve: height growth rate||– ve: structural reinforcement|
|SMPL: stem mass length−1 (mg mm−1)||+ ve: vertical growth|
|LMPL: leaf mass length−1 (mg mm−1)|
|LMF: leaf mass fraction (mg mg−1)|
|LAR: leaf area ratio (mm2 mg−1)|
|LNF: leaf nitrogen fraction (mg N/mg stem)|
|BMF||Branch mass fraction (mg branch/mg shoot)||+ ve: height growth rate||– ve: light interception|
|SM||Seed mass (mg)||+ ve: colonization/shade tolerance||+ ve: height allometry|
|TwXSA||Terminal twig cross-sectional area (mm2)|
|AN||Dry mass gain per leaf nitrogen (mg mg N−1)|
Leaf mass per area (LMA; mg dry mass mm−2)
LMA is one of several intercorrelated leaf traits, representing a fast–slow continuum in leaf economics across species (Wright et al. 2004). Low LMA is associated with short leaf life span, high leaf nitrogen, high photosynthetic capacity, short nutrient residence times and high relative growth rates (reviews by Westoby et al. 2002; Reich et al. 2003). Low LMA species are capable of rapid height growth (Coley 1988; Reich et al. 1992), but as a result may encounter increased mortality. A positive correlation with height is therefore expected in the successional set. Low LMA also improves use of low light, through its effect on leaf area ratio of the plant and hence on light capture per unit biomass (Givnish 1988). Recent reviews (Walters & Reich 1999; Reich et al. 2003), however, suggest the opposite: that LMA is higher among shade-tolerant species, contributing to a resource-conservation strategy favoured when carbon budgets are marginal (King 1994; Kitajima 1994). Thus there are two possible predictions on the relationship between LMA and height along the light gradient.
Wood density (mg mm−3)
The amount of dry matter invested per volume of stem varies considerably across species (e.g. from 0.26 to 1.29 for 243 tropical tree species, Ter Steege & Hammond 2001). Low density facilitates rapid volumetric growth (Enquist et al. 1999; Suzuki 1999) and is associated with high hydraulic conductance (Hacke et al. 2001), but results in decreased structural stability (Niklas 1994), increased risk of pathogen infection (Augspurger & Kelly 1984), cavitation risk (Hacke et al. 2001) and decreased shade tolerance (Lawton 1984; Loehle 1988; Osunkoya 1996). Density is commonly adopted as an indicator of successional status (Lawton 1984; Ter Steege & Hammond 2001), so we hypothesize a positive correlation with height in the successional group. Existing data indicate the opposite pattern for the light gradient (Thomas 1996; Kohyama et al. 2003) due to the need for increased vertical growth and hydraulic conductance among taller species.
The biomass cost per length of stem seems fundamental to a species’ height strategy. Yet despite significant variation among species (Poorter & Werger 1999), this trait has received little attention to date. Three measures of the process of stem extension bear consideration. First is the amount of dry mass required to achieve a unit of stem extension. Second is the rate at which leaf mass (or area) can be deployed in conjunction with a unit of stem growth. Third is the manner in which one and two combine to influence the rate of stem extension. Early successional species are hypothesized to economise on stem biomass (Schippers & Olff 2000), thereby facilitating rapid growth. Similarly, plants higher in the canopy may need stronger reinforcement to withstand increased exposure to wind (Osada et al. 2002), suggesting a negative relationship between extension rate and height in both sets (Table 1).
For comparison between species, extension cost is most usefully quantified for a common length of stem. In the current study, extension costs are quantified at two scales for mature plants: at the branch tip and for the terminal metre of stem. Measurements at the branch tip are essential for describing the effect of LMA, wood density and twig cross-sectional area on stem extension, without additional influence from branching and stem thickening. Branching increases the biomass cost per unit extension, decreasing height growth rate (Kohyama 1987; Kohyama & Hotta 1990). Thus we hypothesize a positive correlation between branching and potential height along the successional gradient. Lateral spread can also reduce self-shading, thus improving carbon gain under low light and increasing shade tolerance (Horn 1971; Kohyama & Hotta 1990; Pacala et al. 1996), suggesting a negative relationship with height along the light gradient.
Seed mass (mg)
Species mean seed mass summarizes much variation in dispersal and establishment success (reviews by Leishman et al. 2000; Westoby et al. 2002). Early successional species tend to have small seeds (Foster & Janson 1985; Osunkoya 1996), thereby emphasizing seed output and colonizing ability. Late successional species have larger seeds, emphasizing survival in low light (Foster & Janson 1985; Leishman et al. 2000). Recent work has also demonstrated a tight positive correlation with height across large numbers of species (Moles et al. 2004). Short early successional species are therefore hypothesized to have smaller seeds than equivalent-height late successional species (Foster & Janson 1985), but with a positive relationship between seed mass and height predicted for each set.