| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
2 Department of Biological Sciences, Florida International University, Miami, Florida 33199 USA Fairchild Tropical Garden, Miami, Florida 33156 USA; 3 Department of Statistics, Florida International University, Miami, Florida 33199 USA; and 4 Forest Research Institute of Malaysia, Kuala Lumpur 52109, Malaysia
Received for publication January 5, 1999. Accepted for publication July 20, 1999.
ABSTRACT
We studied the development of leaf characters in two Southeast Asian dipterocarp forest trees under different photosynthetic photon flux densities (PFD) and spectral qualities (red to far-red, R:FR). The two species, Hopea helferi and H. odorata, are taxonomically closely related but differ in their ecological requirements; H. helferi is more drought tolerant and H. odorata more shade tolerant. Seedlings were grown in replicated shadehouse treatments of differing PFD and R:FR. We measured or calculated (1) leaf and tissue thicknesses; (2) mesophyll parenchyma, air space, and lignified tissue volumes; (3) mesophyll air volumes (Vmes/Asurf) and surfaces (Ames/Asurf); (4) palisade cell length and width; (5) chlorophyll/cm and a/b; (6) leaf absorption; and (7) attenuance/absorbance at 652 and 550 nm. These characters varied in response to light conditions in both taxa. Characters were predominantly affected by PFD, and R:FR slightly influenced many characters. Leaf characters of H. odorata were more plastic in response to treatment conditions. Characters were correlated with each other in a complex fashion. Variation in leaf anatomy is most likely a consequence of increasing leaf thickness in both taxa, which may increase mechanical strength and defense against herbivory in more exposed environments. Variation in leaf optical properties was most likely affected by pigment photo-bleaching in treatments of more intense PFD and was not correlated with Amax. The greater plasticity of leaf responses in H. odorata helps explain the acclimation over the range of light conditions encountered by this shade-tolerant taxon. The dense layer of scales on the leaf undersurface and other anatomical characters in H. helferi reduced gas exchange and growth in this drought-tolerant tree.
Key Words: Dipterocarpaceae • Hopea • leaf structure • rain forest • red:far-red ratio • seedling • shade
Producing new and structurally altered leaves is the primary means for plants to respond to changes in the radiation environment. Variation in leaf structure may affect plant function in at least three ways. First, leaf anatomy, particularly stomatal density and the extent and shape of mesophyll air spaces, affects resistance to gas exchange and may limit photosynthetic assimilation. Second, pigment content and distribution, influenced by anatomy, determine the efficiency of light capture by leaves and influence photosynthesis. Finally, leaf toughness may reduce a plant's susceptibility to herbivory, increase its longevity, and enhance the plant's carbon balance. Renewed interest in the contributions of leaf structure to photosynthesis and growth (Terashima, 1989
; Smith et al., 1997
) may help to solve the old mystery of the differences in growth rates among plants (Lambers and Poorter, 1992
).
Here we examine the effects of light environments, differing both in photosynthetic photon flux density (400–700 nm, PFD) and in spectral quality (as documented by the red to far-red ratio of quanta, or R:FR; Smith, 1994
) on leaf structure and function in seedlings of two rain forest trees native to Southeast Asia. We focus particularly on the responses of leaf anatomy and pigment content. The seedling growth, photosynthesis, and architecture have been described previously (Lee et al., 1997
).
Leaf structure and function
Leaf anatomy may directly influence CO2 uptake by its effects on diffusive resistances (Nobel, 1991
). Earlier research in crop plants hoped to find such anatomical traits that could be manipulated to increase crop production (El-Sharkawy and Hesketh, 1965
; Wilson and Cooper, 1967
). These resistances begin at the boundary layer, influenced by leaf size and shape. Stomatal size and density play a crucial role (Wong, Cowan, and Farquhar, 1979
). Although the role of mesophyll air space is less understood, its influence may also be substantial (Nobel, 1977
; Parkhurst, 1994
). The degree of mesophyll air space can be assessed as a percentage or an actual volume per unit area. The surface of the air space/cell contacts can be estimated as a ratio to the leaf surface (Ames/Asurf) using stereological techniques (Parkhurst, 1982
). Three anatomical variables altering Ames/Asurf include (1) leaf thickness; (2) differentiation of palisade and spongy mesophyll; and (3) the degree of mesophyll air space (Nobel, 1991
). Additional resistances, less amenable to analysis, include the mesophyll cell walls, cytosol, and chloroplasts.
Leaf anatomy affects the efficiency of light absorption in two ways. Light is absorbed by pigments, principally chlorophylls a and b, in the chloroplasts. Other pigments, including the carotenoid accessory pigments and flavonoids (as anthocyanins) also modify absorption. Leaf anatomy is important in the way in which it influences the distribution of chloroplasts in leaves (Lee et al., 1990
; Vogelmann, 1994
). Since chlorophyll is produced in plastids and not dispersed throughout the leaf, quanta may pass through them without being absorbed. This probability reduces the absorption by chlorophyll at the wavelengths it most effectively absorbs (such as at 650 nm) due to sieving or flattening effects (Duysens, 1956
; Das et al., 1967
). Additionally, cellular structures within the leaf (as cell walls and air spaces) scatter radiation in a complex fashion and make the internal light environment more uniform. This scattering increases the effective path length of radiation and increases the probability of absorption by chlorophyll at weakly absorbed wavelengths, as at 550 nm (Butler, 1964
; Kirk and Goodchild, 1972
).
The contribution of leaf structure to sieving and path-lengthening effects can be assessed by comparing the ratio of absorbance of chlorophyll in vivo to that in vitro, the attenuance to absorbance ratio (Ruhle and Wild, 1979
; Terashima and Saeki, 1983
; Lee et al., 1990
). Such a ratio should indicate sieving effects at strong absorbance wavelengths (<1.00 at 652 nm) and path-lengthening effects at weakly absorbed wavelengths (>1.00 at 550 or 700 nm). These ratios will depend upon the chlorophyll concentration and the distribution of chloroplasts. Differentiation of mesophyll tissue into palisade and spongy cell types should increase the sieving effects, along with the shape of the palisade cells. Long and narrow cells increase this effect (Lee et al., 1990
). Because of the difference between the refractive indices of air and cell components (1.40–1.45), the extent and distribution of air spaces strongly influence path-lengthening effects. Still other anatomical features, as pubescence and surface waxes, influence absorption (Ehleringer, Björkman and Mooney, 1976
; McClendon, 1984
). Pubescence or scales on the abaxial surface may actually increase absorption (Eller and Willi, 1981
).
Shade responses
Shadelight under forest canopy varies in quantity and spectral quality, and both factors may affect leaf development, structure, and function. Reduced PFD affects leaf development in the classical ways (size and thickness) described in numerous studies (Chabot and Chabot, 1977
; Dengler, 1980
; Björkman, 1981
; Jurick, Chabot, and Chabot, 1982
). Since such research has combined shade conditions (reduced PFD) with the spectral quality of full sunlight (high R:FR), it is bound to underestimate the extent of anatomical responses to shadelight (Schmitt and Wulff, 1993
). Reduced R:FR, affecting phytochrome equilibria in plant tissues (Smith, 1994
), may influence leaf anatomy, although there are few such studies in response to R:FR. The challenge in this research has been to separate the effects of quantity and quality in assessing such effects. Ashton and Berlyn (1992, 1994)
simultaneously altered PFD and RFR in shade experiments and demonstrated significant changes in leaf anatomy with physiological significance. Chazdon and Kaufman (1993)
encountered such parallel changes in their choice of natural light environments, as did Araus and Hogan (1994)
.
The approach described here combines the variation in PFD and R:FR in a factorial experimental design with simultaneous leaf measurements of (1) photosynthesis and transpiration; (2) quantitative anatomy allowing estimates of Ames/Asurf; (3) pigment composition and leaf absorption permitting estimates of attenuance/absorbance; and (4) stomatal density and other anatomical differences.
Plants studied
We examined seedling leaves of two species of Hopea, H. helferi (Dyer) Brandis and H. odorata Roxb., of the family Dipterocarpaceae. These are closely related taxa, both placed within subsection Hopea by Ashton (1982)
, and extremely similar based on restriction fragment length polymorphism analysis of chloroplast genes (Tsumura et al., 1996
). They have the same geographical distributions, Indo-China south to the northern Malayan Peninsula, but different site preferences (Lee et al., 1997
). Hopea helferi grows on exposed slopes in evergreen and semideciduous forests, and H. odorata grows in more protected river margins.
The purpose of this research was to answer three interrelated questions. First, how do variations in light intensity (PFD) and spectral quality (R:FR) affect the development of leaf anatomical characters? Second, how might these anatomical differences explain the differences in photosynthesis and growth among treatments within each species and between the two taxa? Third, how do the developmental responses in leaf anatomy help explain the differences in the physiology and the ecological distributions of Hopea helferi and H. odorata?
MATERIALS AND METHODS
Seeds for germination and growth trials were obtained from tree populations of H. helferi and H. odorata in the arboretum at the Forest Research Institute of Malaysia (FRIM), near Kuala Lumpur. Seedlings were grown in a series of replicated shade environments: (1) 40% solar PFD and 1.25 R:FR, HRR; (2) 12% PFD and 1.25 R:FR, MRR; (3) 12% PFD and 0.25 R:FR, MFR; (4) 3% PFD and 1.25 R:FR, LRR; and (5) 3% PFD and 0.25 R:FR, LFR. We also grew seedlings in direct sunlight at an adjacent site (SRR). The potted seedlings were placed randomly on a 9 x 9 grid within the shadehouses, 0.4 m apart. These methods and conditions were described in detail by Lee et al. (1996, 1997)
.
We selected tissue from the most recently matured leaf on each plant for all analyses, the same leaf and area used for gas exchange measurements (Lee et al., 1997
). We chose areas midway between the blade margin and midrib, keeping them on moist paper toweling in low light and processing them in the laboratory within 2 h.
We measured diffuse reflectance, diffuse transmittance, and then calculated absorption, with the integrating sphere attachment to a Li-1800 spectroradiometer (LI-COR Inc., Lincoln, Nebraska; Lee and Graham, 1987
). We used a solar spectrum at FRIM as the reference for calculations.
We measured chlorophyll a and b concentrations from 1 cm diameter samples obtained with a cork borer, with the n,n-dimethyl formamide technique of Moran (1982)
. Attenuance/absorbance ratios (att/abs) were calculated using log-transformed absorption values at 550, 652, and 800 nm (Lee et al., 1990
). The extinction coefficient of 
= 34.5 L/mg at 652 nm, equal for chlorophylls a and b, was obtained from Arnon (1949)
, and calculated from an 80% acetone leaf extract as a ratio at 550 nm, of 4.82 L/mg, using a Shimadzu spectrophotometer (Shimadzu Instruments, Tokyo, Japan).
For the anatomical analysis 1-mm2 samples were fixed in 0.50 Karnovsky's fixative (Karnovsky, 1965
) for 24 h at 25°C and transferred to 70% aqueous ethanol. Specimens were then dehydrated in an ethanol series and embedded in Spurr resin (Ladd, Burlington, Vermont, USA). Sections were cut at 1.5 µm with a Reichert-Jung Supercut 2050 Microtome (Reichert-Jung, Heidelberg, Germany) with diamond histo-knife, stained with 1% aqueous toluidine blue, and mounted on glass slides. An image analysis system (Agvision, Decagon Instruments, Pullman, Washington, USA) attached to a standard light microscope facilitated quantitative anatomical measurements. Magnification at 400x produced a field with sections 200 µm across. We measured (1) leaf section area; (2) mesophyll area; (3) lengths and widths of the three largest palisade cells; (4) total mesophyll air space and perimeter; and (5) distance of upper epidermis across the section. We then calculated the mean leaf and mesophyll thicknesses. Palisade cell volumes were estimated by assuming a cylindrical shape for these cells, with hemispherical ends. Epidermal cell volumes were estimated from their thickness and the numbers of cells observed per field. We used stereological techniques to estimate areas of mesophyll-airspace contacts in relation to adaxial leaf surface (Ames/Asurf) and mesophyll air space volume in cubic millimeters per cubic centimeter of leaf surface (Parkhurst, 1982
, and personal communication; Buisson and Lee, 1993
). Given the deviation of cell shapes from uniformity, we used a shape factor of 1.20 for calculations (Thain, 1983
).
We randomly located replicates of each treatment on the roofs of two adjacent buildings, and we analyzed results as a stratified random block design using the General Linear Models Procedure of ANOVA (SAS, 1985
). We used individual pots, randomly located within shadehouses, as the statistical unit. Initial data were checked for normality and rank transformed when necessary. We used the Fisher's least significant difference test, with a significance threshold of P < 0.05, for post hoc comparisons. Relative influences of PFD and R:FR on the development of different traits were estimated from the two-way ANOVA of rank-transformed data from the factorial design of the low- and medium-irradiance treatments (LRR, LFR, MRR, and MFR). These influences were visualized by calculating their coefficients of determination (Sokal and Rohlf, 1981
), dividing sums of squares from the two-way ANOVA by the total sums of squares. We also calculated Pearson product correlations among many characters, again using rank-transformed data.
RESULTS
Treatments significantly affected leaf morphology, anatomy (Fig. 1), pigment composition, and optical properties. The primary effects were attributable to intensity (PFD), although spectral quality (R:FR) influenced some characters (Table 1).
|
|
) and palisade length (Table 2). Although leaves of H. odorata were only slightly thicker than H. helferi, the contributions of tissue layers varied; palisade cells were longer in the former and the spongy mesophyll layer was thicker in the latter. The distribution of cell types within the mesophyll layer did not differ much among light treatments within each species (Fig. 3), but H. helferi produced significantly more lignified tissue than H. odorata. Volumes of palisade and upper epidermal cells were increased by higher PFD, and were significantly greater in H. odorata (Table 3). Palisade cell shape, particularly maximum width, was influenced by light conditions. Low R:FR moderately decreased palisade cell width in both species. Leaf thickness also increased with the amount of mesophyll air volume per leaf area (Vmes/Asurf; Tables 2, 3). These spaces were also strongly associated with increased mesophyll-air space contact surface (Ames/Asurf) in both species, although the treatment effects at low and medium PFD were not large.
|
|
|
).
|
Interactions between PFD and R:FR were generally of little importance in explaining variation in leaf characters; coefficients of determination for the interactions were small and not significant (Table 1). The most likely contribution to interaction effects would be the effect of spectrally altered light reflected from adjacent plants in the LRR and MRR treatments (Ballaré et al., 1993
; Lee et al., 1997
). Reflected light is not a significant developmental factor under these experimental conditions, particularly since reduced R:FR generally did not affect the development of leaf characters.
DISCUSSION
In general, these shade treatments influenced leaf anatomical characters much less than they did variations in growth, allocation, and seedling architecture (Lee et al., 1997
). Also, variations of characters within species were smaller than those between the two taxa. These results are helpful in answering questions raised in the introduction.
PFD vs. R:FR
Spectral quality had negligible importance in the development of leaf anatomical characters. Reduced R:FR did not affect the contribution of tissue layers to total leaf thickness (Fig. 2), nor tissue composition in the mesophyll (Fig. 3). These results are inconsistent with the small literature reporting significant R:FR effects on palisade cell shape, contributing to thinner leaves, as in tropical vines (Lee, 1988
) and papaya (Buisson and Lee, 1993
). However, the life history characteristics of the latter plants predict greater plasticity of light responses because of the heterogeneity of habitats encountered by the vines and the early-successional niche of papaya (Paz and Vázquez-Yanes, 1998
). Most of the coefficients of determination for the R:FR effects of both species were very small, although characters from H. odorata varied more than H. helferi (Table 1).
|
Other correlations may be due to parallel, but functionally unrelated, effects of the light treatments. Total plant growth rate for both species (Lee et al., 1997
) was strongly correlated with many leaf characters (Table 3). These correlations are primarily the consequence of (1) the increase in leaf thickness and (2) the reduction in chlorophyll concentration with intensity of light treatments.
The classical pattern of response and adaptation to higher light intensity is a thicker leaf with longer palisade cells (Björkman, 1981
). Strauss-Debenedetti and Berlyn (1994)
measured such changes among taxa of different successional status in the Moraceae. There was no clear relationship between successional status and photosynthetic plasticity, and leaf anatomy did not vary with physiological traits in a clear manner. Chazdon and Kaufman (1993)
found a correlation between mesophyll thickness and photosynthesis in a gap species of Piper. Ashton and Berlyn (1992)
observed a complex pattern of anatomical and physiological relationships in four closely related Shorea species (Dipterocarpaceae) in Sri Lanka. Leaf structure, function, and ecology were generally correlated in individual taxa.
Photosynthesis (Amax; Lee et al., 1997
) was poorly correlated with leaf characters in both Hopea species. The strongest correlation was with conductance, which was measured at the same instance in each leaf. The lack of significant correlation of photosynthesis with Ames/Asurf and mesophyll air volume in both species suggests that variations in these characters do not significantly alter CO2 uptake in these species. Ames/Asurf was correlated with Amax in Plectranthus parviflorus, and in several other high-light species (Nobel, Zaragoza and Smith, 1975
; Nobel, 1977
; Longstreth, Hartsock, and Nobel, 1980
). However, Araus et al. (1986)
did not observe such differences in more shade-tolerant species, and mesophyll conductance and leaf thickness were negatively correlated in several taxa (Syvertson et al., 1995
). Theoretical calculations by Parkhurst (1994)
suggest that mesophyll limitations on gas diffusion for leaves may be only a few percent, much less important than stomatal conductance (Wong, Cowan, and Farquhar, 1979
; von Cammerer and Farquhar, 1981
; Sharkey, 1985
). However, the results of Niinemets, Kull, and Tenhunen (1998)
on a suite of temperate woody species suggested that anatomical/morphological leaf traits were more important than biochemical ones in explaining differences in photosynthetic yield. Clearly, we need more research in this area (Smith et al., 1997
).
Optical properties were also not correlated with photosynthesis. The variables affecting att/abs652 include chloroplast distribution, mesophyll cell size and shape, and pigment concentration. Positive correlations with leaf thickness and associated characters indicate that the more elaborate mesophyll structure in thicker leaves reduces sieving effects. However, anatomical influences are weak compared to the strong negative correlation with chlorophyll concentrations in both species. Att/abs550 was significantly correlated with leaf thickness and internal anatomical characters, suggesting their contribution to path-lengthening effects. However, the strong negative correlation with chlorophyll content is similar to the ratio at 652 nm. Given the weak correlation of these characters with maximum photosynthesis (Table 2), it is more likely that the correlations are the consequences of variation of other traits, particularly leaf thickness and chlorophyll concentration, than directly due to light treatments.
Gas exchange was weakly correlated with growth and developmental characters. Stomatal conductance (Lee et al., 1997
) was weakly correlated with stomatal density in H. helferi, and stomatal density with photosynthesis for H. odorata, partly due to the large variances in the conductance data. Maximum photosynthesis was positively correlated with seedling growth rates (mass/day), but only significantly so for H. odorata, with its greater responses. Leaf characters were more significantly correlated among leaf characters for H. odorata than for H. helferi, consistent with the greater response of the former leaf characters to the shade treatments (Tables 1, 2). Photosynthesis was negatively correlated with growth efficiency (mass per mole, MMO) because of the reduced growth efficiency at the highest light treatments (Lee et al., 1997
). Photosynthesis was correlated with growth per day in H. odorata, but not significantly so in H. helferi. Photosynthesis measurements, no matter how carefully measured, are instantaneous, and may not correlate as well as other characters, as the more lengthy measurements of growth.
Species differences
Leaf morphology and anatomy between the two species differ in several important ways that help explain their functional ecology. First, H. odorata produced larger palisade cells in all treatments. Cell size and intercellular spaces contributed to the greater Ames/Asurf of this species. Smaller leaf cells (both palisade and upper epidermal cells documented for H. helferi) have been associated with drought tolerance in many plants (Larcher, 1995
).
Second, leaf stomatal density was greater in H. odorata, except at the lowest light treatments. Stomatal aperture lengths were also greater in H. odorata [15.5 ± 0.5 nm (N = 10) for all treatments compared to 12.4 ± 0.4 nm (N = 10) for H. helferi], with no differences between treatments. This contributed to the greater stomatal conductances measured in H. odorata in all but the MRR treatment (Lee et al., 1997
), and should promote higher rates of carbon assimilation. Evidence for the ecological advantages of these anatomical differences would be their correlations with water use efficiency (WUE). Unfortunately, the larger variances of transpiration measurements made those of the ratios even larger, and none of the treatments were significantly different. The WUE of H. odorata (3.84 ± 1.03 x 10-3) was not significantly less than that of H. helferi (5.10 ± 1.03 x 10-3) seedlings grown at 40% of sunlight. This variance also decreased the likelihood of any significant correlations.
Third, treatments of H. helferi had similar or greater PFD absorption capacity despite slightly reduced chlorophyll concentrations. Although lower in H. odorata, chlorophyll a/b ratios varied little within species except at very high light levels, indicating no significant changes in photosystem stoichiometry due to the shade treatments (Chow, Melis, and Anderson, 1990
). Sieving effects (mirrored by greater attenuance/absorbance652 nm) were larger in H. odorata, and path-lengthening effects were smaller (smaller attenuance/absorbance550 nm). A single factor that may contribute to these optical characters is the leaf undersurface scales in H. helferi, which would backscatter light back into the mesophyll (Eller and Willi, 1981
). Such backscatter would increase total absorptance, reduce sieving effects, and increase path-lengthening effects.
Fourth, leaves of H. helferi produced more lignified cells (sclerenchyma and vasculature) in the mesophyll—generally vertically all across this tissue layer. Finally, leaves of H. helferi produce undersurface scales (Fig. 1; Ashton, 1982
). Such scales should reduce stomatal conductance, Amax, and presumably limit growth rates as well. Both the lignification and scales help explain the greater mass per area of the leaves of H. helferi.
The greater plasticity of response of most leaf characters may provide H. odorata with a greater capacity of growth responses in different environments. These anatomical differences have clear implications for function and help explain the greater drought tolerance of H. helferi. They may also contribute to greater leaf toughness and durability, which may reduce rates of herbivory in these plants. Both produce terpenoid compounds that may be more important deterrents than these structures. All of these differences are remarkable for their physiological consequences in two species so closely related (Tsumura et al., 1996
), suggesting that such characters, controlled by light conditions, evolved quite rapidly.
Conclusions
Seedling leaves of Hopea helferi and H. odorata developed differences in anatomy, optical properties, and physiology in the shade conditions of this research. Photon flux density was by far the most important variable in influencing leaf characters in both taxa, although spectral quality affected palisade cell widths in both taxa. Within each species, variation in characters of leaf anatomy and optics was not well correlated with physiological performance, suggesting that they are primarily the consequence of other characters affected by the light treatments. Increasing leaf thickness, affected by higher light exposure in both taxa, influenced internal mesophyll architecture. Yet, leaf thickness and toughness may be more important in increasing mechanical strength, reducing herbivory, and increasing drought tolerance. Reductions in chlorophyll concentrations per unit area influenced optical properties, but are most likely the consequence of photo-bleaching in the higher light treatments (HRR and SRR). Plant architecture and allocation (both influencing leaf display) appear more important in explaining growth rates within the two taxa than leaf anatomy and optics.
Seedling leaves of Hopea helferi and H. odorata differed in several important ways, and those of the latter were more plastic in response to the range of light conditions. This species grows primarily in dense forest along streams and appears more shade tolerant (Lee et al., 1997
). Secondly, leaves of H. helferi produced a dense layer of undersurface scales in all treatments. Since other anatomical differences (including leaf thickness and stomatal density) were small between the two species, this layer of scales most likely contributes to the reduced stomatal conductance and reduced maximum photosynthesis rates. Despite the lack of correlation between maximum photosynthesis (Amax; Lee et al., 1997
) and seedling growth rates within each species, the significantly reduced Amax and dry mass increments in H. helferi are most likely due to the presence of these scales. This species grows primarily on well-drained soils on slopes in evergreen forest. The significant advantage for this species is probably the greater economy of water use in an environment where seedlings are frequently subject to drought.
FOOTNOTES
1 The authors thank Dato Salleh Mohamed Noor, former Director-General of FRIM for encouragement and support, technical support from Siti Asha Abu Bakar, Zaiton Salleh, K. C. Ang, Zaini Bahari, Noraida Idaris, Hamsinah Hashim, Juntak So, Rosli Alias, Akoh Jin, Birgith Phillips, Eric Pop, Fran Mahr, and Maria Morera, and Joel Trexler and Tom Turner for advice. The German GTZ mission at FRIM provided lodging for the U.S. authors. Research was supported by NSF grant DEB-9020137 and a donation of materials from the 3M Corporation. The final preparation of this article was assisted by a Bullard Fellowship at the Harvard Forest, awarded to D. Lee. This is contribution 16 from the Tropical Biology Program at Florida International University. 
5 Author for correspondence (Ph: 305 348-3111; FAX: 305 348-1986; e-mail: leed{at}fiu.edu
).
LITERATURE CITED
Araus, J. L., R. Alagre, L. Tapia, R. Calafell, and M. D. Serret. 1986 Relationships between photosynthetic capacity and leaf structure in several shade plants. American Journal of Botany 73: 1760–1770. [CrossRef][ISI]
———, and K. Hogan. 1994 Leaf structure and patterns of photoinhibition in two neotropical palms in clearings and forest understory during the dry season. American Journal of Botany 81: 726–38. [CrossRef][ISI]
Arnon, D. L. 1949 Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24: 1–15.
Ashton, P. F. S. 1982 Dipterocarpaceae. In C. G. G. J. van Steenis [ed.], Flora Malesiana, series I 9: 237–582.
———, and G. P. Berlyn. 1992 Leaf adaptations of some Shorea species to sun and shade. New Phytologist 121: 587–96. [CrossRef][ISI]
———, and ———. 1994 A comparison of leaf physiology and anatomy of Quercus (section Erythrobalanus-Fagaceae) species in different light environments. American Journal of Botany 81: 589–97. [CrossRef][ISI]
Ballaré, C. L., A. L. Scopel, R. A. Sanchez, and S. R. Radosevich. 1993 Photomorphogenic processes in the Agricultural environment. Photochemistry and Photobiology 56: 777–788. [CrossRef]
Björkman, O. 1981 Responses to different quantum flux densities. In O. L. Lange, P. S. Nobel, C. B. Osmond, and H. Zeigler [eds.], Encyclopedia of plant physiology new series, vol. 12A, 57–107. Springer Verlag, Heidelberg.
Buisson, D., and D. W. Lee. 1993 The developmental responses of papaya leaves to simulated canopy shade. American Journal of Botany 80: 947–952. [CrossRef][ISI]
Butler, W. L. 1964 Absorption spectroscopy in vivo: theory and application. Annual Review of Plant Physiology 14: 451–470.
Chabot, B. F., and J. F. Chabot. 1977 Effects of light and temperature on leaf anatomy and photosynthesis in Fragaria vesca. Oecologia 26: 363–377.
Chazdon, R. L., and S. Kaufman. 1993 Plasticity of leaf Anatomy of two rain forest shrubs in relation to photosynthetic light acclimation. Functional Ecology 7: 385–394. [CrossRef][ISI]
Chow, W. S., A. Melis, and J. M. Anderson. 1990 Adjustments of photosystem stoichiometry in chloroplasts improve the quantum efficiency of photosynthesis. Proceedings of the National Academy of Sciences, USA 87: 7502–7506.
Das, M., E. Rabinowitch, L. Szalay, and G. Papageorgiou. 1967 The "sieve effect" in Chlorella suspensions. Journal of Physical Chemistry 71: 3543–3549. [CrossRef][ISI]
Dengler, N. G. 1980 Comparative histological basis of sun and shade leaf dimorphism in Helianthus annuus. Canadian Journal of Botany 58: 717–730.
Duysens, L. N. M. 1956 The flattening of the absorption spectrum of suspensions, as compared to that of solutions. Biochimica Biophysica Acta 19: 1–12.
Ehleringer, J., O. Björkman, and H. A. Mooney. 1976 Leaf pubescence: effects on absorptance and photosynthesis in a desert shrub. Science 192: 376–377.
Eller, B. M., and P. Willi. 1981 The significance of leaf pubescence for the absorption of global radiation by Tusilago farfara L. Oecologia 49: 366–370. [CrossRef][ISI]
El-sharkawy, M., and J. Hesketh. 1965 Photosynthesis among species in relation to characteristics of leaf anatomy and CO2 diffusion resistance. Crop Science 5: 517–521.
Jurick, T. W., J. W. Chabot, and B. F. Chabot. 1982 Effects of light and nutrients on leaf size, CO2 exchange, and anatomy in wild strawberry (Fragaria virginiana). Plant Physiology 70: 1044–1048.
Karnovsky, M. J. 1965 A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. Journal of Cell Biology 27: 137A.
Kirk, J. T. O., and D. J. Goodchild. 1972 Relationship of photosynthetic effectiveness of different kinds of light to chlorophyll content and chloroplast structure in greening wheat and in ivy leaves. Australian Journal of Biological Science 25: 215–241.
Lambers, H., and H. Poorter. 1992 Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Advances in Ecological Research 23: 187–261. [ISI]
Larcher, W. 1995 Physiological plant anatomy, 3rd. ed. Springer-Verlag, Berlin.
Lee, D. W. 1988 Simulating forest shade to study the develop-mental ecology of tropical plants: juvenile growth in three vines in India. Journal of Tropical Ecology 4: 281–292.
———, K. Baskaran, M. Mansor, H. Mohamad, and S. K. Yap. 1996 Light intensity and spectral quality effects on Asian tropical rainforest tree seedling growth and morphology. Ecology 77: 568–580. [CrossRef][ISI]
———, ———, ———, ———, and ———. 1997 Effects of light intensity and spectral quality on seedling development of two Southeast Asian Hopea species. Oecologia 110: 1–9.
———, R. Bone, S. Tarsis, and D. Storch. 1990 Correlates of leaf optical properties in tropical forest extreme shade and sun plants. American Journal of Botany 77: 370–380. [CrossRef][ISI]
———, and R. Graham. 1987 Leaf optical properties in extreme shade plants. American Journal of Botany 73: 1100–1108. [CrossRef][ISI]
Longstreth, D. J., T. L. Hartsock, and P. S. Nobel. 1980 Mesophyll cell properties for some C3 and C4 species with high photosynthetic rates. Physiologia Plantarum 48: 494–98. [CrossRef]
McClendon, J. H. 1984 The micro-optics of leaves I. Patterns of reflection from the epidermis. American Journal of Botany 71: 1391–97. [CrossRef][ISI]
Moran, R. 1982 Formulae for determinatIon of chlorophyllous pigments extracted with n,n-dimethyl formamide. Plant Physiology 69: 1376–81.
Niinemets, Ü., O. Kull, and J. D. Tenhunen. 1998 An analysis of light effects on foliar morphology, physiology and light interception in temperate deciduous woody species of contrasting shade tolerance. Tree Physiology 18: 681–696.
Nobel, P. S. 1977 Internal leaf area and cellular CO2 resistance: photosynthetic implications of variations with growth conditions and plant species. Physiologia Plantarum 40: 137–144. [CrossRef]
———. 1991 Physicochemical and environmental plant physiology. Academic Press, San Diego, California, USA.
———, L. J. Zaragoza, and W. K. Smith. 1975 Relation between mesophyll surface area, photosynthetic rate, and illumination level during development for leaves of Plectranthus parviflorus Henckel. Plant Physiology 55: 1067–1070.
Parkhurst, D. F. 1982 Stereological methods for measuring internal leaf structure variables. American Journal of Botany 69: 31–39.
———. 1994 Diffusion of CO2 and other gases inside leaves. New Phytologist 126: 449–479. [CrossRef][ISI]
Paz, L., and C. Vasquez-Yanes. 1998 Comparative seed ecophysiology of wild and cultivated Carica papaya trees from a tropical rain forest region in Mexico. Tree Physiology 18: 277–280. [ISI][Medline]
Ruhle, W., and A. Wild. 1979 The intensification of absorbance changes in leaves by light-dispersion: differences between high-light and low-light leaves. Planta 146: 551–557. [CrossRef][ISI]
SAS. 1985 User's guide: statistics, version 5. SAS Institute, Cary, North Carolina, USA.
Sharkey, T. D. 1985 Photosynthesis in intact leaves of C3 plants: Physics, physiology and rate limitations. Botanical Review 51: 53–105.
Schmitt, J., and R. D. Wulff. 1993 Light spectral quality, phytochrome and plant competition. Trends in Ecology and Evolution 8: 47–51. [CrossRef]
Smith, H. 1994 The perception of light quality. In R. E. Kendrick and G. H. M. Kronenberg [eds.], Photomorphogenesis in plants, 187–217. Martinus Nijhoff, Dordrecht, The Netherlands.
Smith, W. K., T. C. Vogelmann, E. H. Delucia, D. T. Bell, and K. A. Shepherd. 1997 Leaf form and photosynthesis. BioScience 47: 785–793. [CrossRef][ISI]
Sokal, R. R., and F. J. Rohlf. 1981 Biometry, 2nd ed. W. H. Freeman, New York, New York, USA.
Strauss-Debenedetti, S., and G. P. Berlyn. 1994 Leaf anatomical responses to light in five tropical Moraceae of different successional status. American Journal of Botany 81: 1582–1591. [CrossRef][ISI]
Syvertson, J. P., J. Lloyd, C. Mccouchie, P. E. Kriedemann, and G. D. Farquhar. 1995 On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant, Cell and Environment 18: 149–157.
———, and T. Saeki. 1983 Light environment within a leaf I. Optical properties of paradermal sections of Camellia leaves with special reference to differences in the optical properties of palisade and spongy tissues. Plant Cell Physiology 24: 1493–1501.
Terashima, I. 1989 Productive structure of a leaf. In W. R. Briggs [ed.], Photosynthesis, 207–226. Alan R. Liss, New York, New York, USA.
Thain, J. F. 1983 Curvature correction factors in the measurement of cell surface areas in plant tissues. Journal of Experimental Botany 34: 87–94.
Tsumura, Y., T. Kawahara, R. Wickneswari, and K. Yoshimura. 1996 Molecular phylogeny of Dipterocarpaceae in Southeast Asia using RFLP of PCR-amplified chloroplast genes. Theoretical and Applied Genetics 93: 22–29. [CrossRef][ISI]
Vogelmann, T. C. 1994 Light within the plant. In R. E. Kendrick and G. H. M. Kronenberg [eds.], Photomorphogenesis in plants, 2nd ed., 307–337. Martinus Nijhoff, Dordrecht, The Netherlands.
Von Cammerer, S., and G. D. Farquhar. 1981 Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153: 376–387. [CrossRef][ISI]
Wilson, D., and J. P. Cooper. 1967 Assimilation in Lolium in relation to leaf mesophyll. Nature 214: 989–992. [CrossRef]
Wong, S. C., I. R. Cowan, and G. D. Farquhar. 1979 Stomatal conductance correlates with photosynthetic capacity. Nature 282: 424–426. [CrossRef][ISI]
This article has been cited by other articles:
|
|
 |
|
  Y. Onoda, F. Schieving, and N. P.R. Anten Effects of Light and Nutrient Availability on Leaf Mechanical Properties of Plantago major: A Conceptual Approach Ann. Bot., April 1, 2008; 101(5): 727 - 736. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. A. Leicht and J. A. Silander Jr. Differential responses of invasive Celastrus orbiculatus (Celastraceae) and native C. scandens to changes in light quality Am. J. Botany, July 1, 2006; 93(7): 972 - 977. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. J. COOKSON and C. GRANIER A Dynamic Analysis of the Shade-induced Plasticity in Arabidopsis thaliana Rosette Leaf Development Reveals New Components of the Shade-adaptative Response Ann. Bot., March 1, 2006; 97(3): 443 - 452. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Poorter, S. Pepin, T. Rijkers, Y. de Jong, J. R. Evans, and C. Korner Construction costs, chemical composition and payback time of high- and low-irradiance leaves J. Exp. Bot., January 1, 2006; 57(2): 355 - 371. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. L. Baltzer and S. C. Thomas Leaf optical responses to light and soil nutrient availability in temperate deciduous trees Am. J. Botany, February 1, 2005; 92(2): 214 - 223. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
0.05, **P 
