Asymptotic height as a predictor of photosynthetic characteristics in Malaysian rain forest trees

Ecology, July, 1999 by S.C. Thomas, F.A. Bazzaz

INTRODUCTION

The most broadly accepted axiom in plant ecophysiology is perhaps that of a relationship between photosynthetic physiology and ambient light levels. Sun plants tend to have higher light-saturated photosynthetic rates ([A.sub.max]) than do shade plants; conversely, at low light levels, shade plants often display higher photosynthetic rates than do sun plants (e.g., Bjorkman and Holmgren 1963, Berry 1975, Boardman 1977, Bjorkman 1981, Givnish 1988). A broad range of physiological and morphological characteristics, from leaf thickness to thylakoid biochemistry, are associated with these differences (e.g., Givnish 1988, Thompson et al. 1992a, b, Strauss-Debenedetti and Berlyn 1994). The sun-shade dichotomy is thus a powerful basis for predicting many aspects of physiological variation within and among plant species.

From an ecological perspective, sun vs. shade "trade-offs" have mostly been interpreted in terms of successional status, with early-successional species tending to exhibit sun-plant characteristics, and late-successional species shade-plant characteristics (e.g., Bazzaz 1979, Bazzaz and Pickett 1980, Fetcher et al. 1994, Reich et al. 1994, Strauss-Debenedetti and Bazzaz 1996). However, in addition to "horizontal" patterns of variation in light environments, such as those created by gaps, closed-canopy forests also have strong and predictable vertical gradients in light availability (e.g., Yoda 1974), as well as vertical gradients in temperature, humidity, air movement, and C[O.sub.2] concentrations (e.g., Aoki et al. 1978, Trumbore et al. 1990, Bazzaz and Williams 1991). A number of studies have previously examined variation within individual species along understory-canopy gradients (Fuchs et al. 1977, Schulze et al. 1977a, b, Pearcy 1987, Doley et al. 1988, Ellsworth and Reich 1993), and there have been a few systematic attempts to describe analogous interspecific patterns of variation in photosynthetic characteristics from the understory through the canopy (e.g., Jurik et al. 1988, Koniger et al. 1995). However, we are aware of no previous work that specifically addresses evolved photosynthetic responses to understory-canopy gradients.

One method of describing interspecific variation along an understory-canopy gradient is to utilize measures of asymptotic height ([H.sub.max]) to quantify variation in tree species size as a continuous variable (Thomas 1996a). Height growth generally levels off or ceases entirely in very old trees, and [H.sub.max] can be defined as the average maximum height reached by a cohort of such old trees (of a given species in a given environment). Because diameter growth is generally nonasymptotic, [H.sub.max] can be estimated through analyses of height-diameter relationships, provided that a sufficient number of trees at or near the height plateau are sampled (Thomas 1996a). Recent comparative studies using this approach have found significant relationships between [H.sub.max] and various aspects of growth, morphology, and reproductive characteristics in Malaysian rain forest trees (Thomas and Ickes 1995, Thomas 1996a, b, c). In particular, larger statured late-successional species exhibit higher growth rates as either adults or saplings (Thomas 1996a), but also lower survivorship (Thomas 1993), than do small-statured species. This suggests the existence of an underlying tradeoff between growth efficiency under low light in understory species, and high growth potential under high light in canopy tree species. Although correlations between photosynthetic rates and growth parameters are not always high (Ramos and Grace 1990, Kitajima 1994), such a trade-off is also likely to be reflected in patterns of photosynthetic physiology.

Hypothesis

It is clear that tree species differing in adult stature would, as mature individuals, differ in physiological characteristics as a direct result of acclimation to the light gradient found through the forest canopy. However, we suggest that species of differing stature should also show systematic differences in physiological characteristics as seedlings or saplings under uniformly low light conditions in the forest understory. This hypothesis follows from three premises, namely: (1) that photosynthetic characteristics are not determined entirely by acclimation to ambient light conditions, but rather are also constrained to some degree by genetic factors; (2) that the developmental processes determining adult-phase physiology also determine, to some extent, the morphology and physiology of sapling leaves; and (3) that trees attaining larger sizes at maturity do in fact experience higher ambient light levels on average, and have thus been subject to a selective regime favoring the evolution of high light photosynthetic characteristics.

The present study directly tests the hypothesis that saplings of taller statured tropical tree species tend to show "sun-plant" photosynthetic characteristics relative to smaller statured species, even in the absence of differences in ambient light conditions. We do not explicitly test the three premises listed above; however, previous studies support each of these assertions. With regard to the first premise, common garden and controlled environment studies clearly indicate considerable genetically based physiological differences among tropical forest species (e.g., Strauss-Debenedetti and Bazzaz 1991, Kitajima 1994). Moreover, a large body of literature exists suggesting that the capacity for photosynthetic acclimation is often, though not always, quite limited in late-successional tropical plant species (Langenheim et al. 1984, Oberbauer and Strain 1984, 1986, Kwesiga et al. 1986, Fetcher et al. 1987, Ramos and Grace 1990, Chazdon et al. 1996, Strauss-Debenedetti and Bazzaz 1996). With regard to the second premise, relatively little is known concerning the developmental genetics of leaf traits in tropical trees. However, clear morphological similarities exist between leaves of seedlings and those of adult trees, even in species that undergo marked "phase-change" (e.g., Ng 1991). Comparative studies have also found strong correlations between, for example, sapling and adult leaf size among species (e.g., r = 0.90 for average sapling vs. adult leaf area: Thomas and Ickes 1995). Finally, with regard to the third premise, the vertical gradient in light availability at the site of the present study has been quantitatively examined (Yoda 1974). Although light levels experienced by adult trees of individual species have not been directly characterized, it has been shown that larger statured species generally begin reproducing at larger sizes (in either absolute or relative terms) than do smaller statured species (Thomas 1996b). Moreover, a wealth of observational evidence also indicates that most small-statured species in this system reproduce under closed-canopy conditions, while many large-statured species reproduce only under high light conditions in the canopy (e.g., Yap 1982, Appanah 1990, Thomas 1996b, c).