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Ecology |
2Centro de Ciencias Medioambientales, C.S.I.C., Serrano 115 dpdo. 28006 Madrid, Spain; 3Department of Biology, California State University, 5500 University Parkway, San Bernardino, California 92407 USA; 4Section of Evolution and Ecology, University of California, Davis, California 95616 USA
Received for publication September 28, 2001. Accepted for publication March 1, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: crown architecture • display efficiency of the foliage • leaf absorptance • light harvesting • phyllotaxis • shade tolerance • tropical rainforest • understory light environment
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Nicotra, Chazdon, and Iriarte, 1999
). In general, less than 2% of the photosynthetically active radiation above the canopy reaches a tropical rainforest floor. This consists of very low background diffuse radiation that is randomly punctuated by generally short duration sunflecks (Pearcy, 1983
; Chazdon and Fetcher, 1984
; Canham et al., 1990
). Under these strongly limiting light conditions, plants might be expected to maximize light capture in the most efficient way, i.e., at the lowest costs in terms of construction and maintenance (Givnish, 1988
). Tropical plants have been shown to adjust their morphology and physiology to available light at different hierarchical levels including: leaf gas exchange properties (photosynthesis, respiration), leaf optical properties (absorptance, transmittance), specific leaf area (area to mass ratio of leaves), crown allometry (e.g., height to diameter ratio, supporting to non supporting tissues mass ratio, leaf area ratio), and crown architecture (branching pattern, foliage arrangement) (Hallé, Oldeman, and Tomlinson, 1978
; Kohyama and Hotta, 1990
; King, 1991
; Kitajima, 1996
; Valladares, 1999
; Poorter et al., 2000
; Valladares et al., 2000
).
A striking feature of tropical rainforest understory vegetation is the large variation in leaf morphology and crown architecture (Bongers and Popma, 1990
; Leigh, 1998
; Turner et al., 2000
). We were interested in knowing if these contrasting habits and morphologies render functionally equivalent architectures in terms of light-capture efficiency or, alternatively, if differences among understory species in efficiency exist. Branching pattern and leaf arrangement have a direct impact on leaf-display efficiency and consequently on light capture and photosynthesis (Valladares, 1999
; Valladares and Pearcy, 1999
). For plants in shaded habitats, minimum leaf overlap in the horizontal plane, which minimizes self-shading for light from above, is an expected characteristic given that it increases the mean light capture per unit leaf area (Pearcy and Yang, 1998
; Pearcy and Valladares, 1999
). For this reason, the geometry of leaf arrangement on stems (phyllotaxis) in low light is typically considered in terms of selection pressures favoring light interception (Sekimura, 1995
; Adler, Barabe, and Jean, 1997
). However, the extent to which phyllotaxis influences light capture remains poorly known because other morphological characteristics interact with and can compensate for suboptimal phyllotaxies (Niklas, 1988
). Additionally, other crown functions such as water transport and biomechanical support may constrain selection pressures for maximizing light capture (Pearcy and Valladares, 1999
). Interactions between different constraints on crown configuration could explain the large range of architectures apparent in tropical rainforest understories.
We have examined leaf and crown characteristics for 24 tree and herbaceous species of contrasting crown architectures co-occurring in a neotropical, lowland rainforest understory. The central objective of this study was to see if there were discernible patterns among taxa or growth form for light capture characteristics of the crown. Foliage display efficiency and light capture were estimated with a three-dimensional geometric modeling program (Y-plant; Pearcy and Yang, 1996
), which has been successfully used for this purpose in a number of previous studies (e.g., Pearcy and Yang, 1998
; Pearcy and Valladares, 1999
; Valladares and Pearcy, 1999
). Causal relationships among traits that determine light absorption at two hierarchical levels (leaf and whole crown) were structured and quantified using path analysis (Mitchell, 1993
; Scheiner, Mitchell, and Callahan, 2000
), which allowed for partitioning into direct and indirect or correlated effects of the traits on light absorption.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Leigh, 1998
). The mean annual precipitation is 2600 mm and mean monthly air temperature ranges from 21° to 32°C (annual mean = 27°C). Most of BCI supports a highly diverse, semi-evergreen moist tropical forest. More than 120 tree species (>2.5 cm in diameter at breast height) per hectare and more than 1370 species of vascular plants have been recorded on this 15.6 km2 island (Leigh, 1998
). The principal vegetation of the deeply shaded forest floor consists of shrubs, tree, and liana seedlings, herbaceous vines, and herbaceous ground plants. In this study, 13 monocotyledoneous and 11 dicotyledoneous species of different families, habits, growth forms, and leaf attributes were selected for comparison of light-capture efficiencies and capacities (Table 1). All plants studied were selected from shaded understory sites. Three to ten individuals of each species were harvested and separated into stems, branches, petioles, and leaves to determine stem and petiole densities (in grams per cubic centimetre), and specific leaf areas (SLA, in square centimetres per gram). Leaf area was determined immediately after collection with an LI-3000 area meter (LI-COR Instruments, Lincoln, Nebraska, USA). Stems, branches, and petioles were cut into segments with a uniform diameter along their length and the volume of these segments was determined from their diameter and length. Following this, the plant parts were placed in individual paper bags and dried in an oven at 65°C for a minimum of 72 h (10 d in the case of thick, woody material) until a constant mass was achieved.
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). The direct site factor (DSF), indirect site factor (ISF), and the global site factor (GSF) were computed by CANOPY. These factors are estimates of the fraction of direct, daily, and total radiation, respectively, expected to reach the site of the photograph compared to the radiation above the canopy (Anderson, 1964
). Weighting factor for diffuse light was 0.1 of total light. Daily photosynthetic photon flux density (PFD, in moles per square metre per day) available at each site was calculated from Y-plant simulations as discussed below for a completely clear day (1 January, 50.6 mol·m–2·d–1 reaching the overstory).
Leaf optical properties
Five to 20 leaves of each species studied were collected in the field and brought immediately to the laboratory for determination of their optical properties. Selected leaves were mature but not senescent, and macroscopic epiphylls were carefully removed before measuring the optical properties. Absorptance, reflectance, and transmittance of PFD by leaf disks were measured with an LI-1800 spectroradiometer (LI-COR Instruments).
Crown three-dimensional reconstruction and estimation of light-capture efficiency
Measurements of the crown geometric properties required for running Y-plant were made on three individuals of each species. For each plant, the angles and azimuths of the stem, of any branch, and of the petiole and surface of any leaf originating from a node were recorded with a compass-protractor. In addition, the azimuth of the midrib, the lengths of internodes, petioles and leaves, and the diameters of the petioles and internodes were recorded. Nodes were numbered proceeding from the base to the top of the plant and along each branch. Values used for the different variables were not mean values for the plant but the specific values at each node for each organ or section of the organ. By recording the mothernode (the node from which a subsequent node arises) for each node, the proper topology of the crown could be reconstructed by Y-plant. Leaf shape was established from x, y coordinates of the leaf margins, and up to 20 leaf shapes were considered for each species. Leaf size was then scaled from the measured leaf length. In order to reconstruct curved leaves such as those of Bromeliaceae (the current version of Y-plant can only handle flat leaves), leaves were divided into segments of varying elevation angle and attached one after another. In the case of climber plants (i.e., Monstera sp.), the stem of the host tree was also measured and included in Y-plant as if it were part of the plant in order to mimic the shade cast by the trunk on the target plant. The realistic graphic display of the reconstructed crowns (see Fig. 1) allowed for error checking by comparison with the appearance of the real plant in the field.
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). The PFD incident at the plant from a given sky sector was simulated from the sky PFD and the fraction of open sky visible (not blocked by the overstory canopy) in that sector. The simulated absorption of PFD by the plant was then determined with a simple ray tracing technique (Pearcy and Yang, 1996
). Summation over all sectors gave the total diffuse PFD absorbed. A similar approach was used for direct PFD except in this case direct PFD was assumed to be absorbed only when the solar disk as calculated from standard equations was within a gap along the solar track. The outputs of Y-plant used in this study were the absorbed PFD (in moles per square metre per day) resulting from the combination of the crown display, the optical properties of the leaf, and the light environment at the plant, and measures of the efficiency of the crown for light capture. These efficiency measures were the projection efficiency (foliage area projected towards a given sky direction divided by the total foliage area [Ep]), the display efficiency (the fraction of foliage that is not self-shaded and is projected towards a given sky region [Ed]), and the efficiency of light absorption (mean PFD per unit leaf area absorbed by the plant divided by PFD incident on a horizontal surface right above the plant [Ea]). In addition, we used the allometric equations to calculate the aboveground leaf area ratio (aLAR, in square metres per kilogram) and the fraction of aboveground biomass invested in support tissue (stems, branches, and petioles, S). Then, from Y-plant simulations, we calculated the aboveground effective leaf area ratio (PFD absorbed per unit plant mass divided by PFD incident per unit surface area [aLARe, in square metres per kilogram). This is equivalent to aLAR multiplied by Ea and expresses how effectively the leaf area is deployed by a plant for light capture. Note that as defined here aLAR and aLARe do not take into account belowground biomass. The mass of the sampled plants was calculated applying the measured stem and petiole densities from other harvested plants to the volumes of each segment calculated from the Y-plant measurements. Leaf mass was calculated from the leaf area as scaled from the measured leaf lengths in Y-plant. After summation over all plant parts, the total plant biomass, the percentage of plant mass invested in support (S), and aLAR were calculated.
Statistics
One-way analysis of variance (ANOVA, Tukey test; SPSS, 1996
) was used to test for differences among species in their light environment, crown architecture, and light-capture efficiency. In all cases, the data met the assumptions of normality and homoscedasticity. Significant differences among species are only considered when the power of the test was equal or larger than 0.85 for 
= 0.01.
Following the procedures of path analysis as described by Mitchell (1993)
, we analyzed the dependence of display efficiency and daily absorbed PFD by the 72 plants studied on supporting biomass, leaf angle, relative internode length (IL/LL; internode length to leaf length ratio), specific leaf area (SLA), leaf absorptance, and global site factor. Path analysis is a more general form of multiple regression that allows consideration of complicated causal schemes and that can be used when independent variables are not truly independent or are correlated. Our path diagram was kept uncomplicated by using only simple factors known to affect foliage display and light capture (Russell, Marshall, and Jarvis, 1989
; Pearcy and Valladares, 1999
; Valladares, 1999
). In path analysis, the thickness of the arrow in the diagram is proportional to the path value and represents the relative strength of a given relationship. Path values are derived from standardized partial regression coefficients so path values can be quantitatively compared. While other paths may also be feasible, our intent was not to explore the relative goodness-of-fit of different models but to quantitatively compare the relative influence on light capture of the different morphological and geometric features of the crowns. In addition to direct effects, we used path analysis to calculate the strengths of the indirect influences of a given factor on another as described by Mitchell (1993)
and Scheiner, Mitchell, and Callahan (2000)
.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). In the deeply shaded forest understory on BCI, graminoid and broad-leaf herbs, vines, lianas, shrubs, palms, mature subcanopy trees, and immature canopy tree saplings can all be found in close proximity (Croat, 1978
). Particularly striking is the broad variety of plant sizes and architectures found within the herbaceous monocots, which, by contrast, contribute relatively little to the understory flora in temperate forests. However, in spite of the contrasting crown architecture and leaf habit, the efficiency of foliage display and light absorption was found to be very similar among the 24 species studied. The exceptions were the climber species and, to a lesser extent, the Bromeliad rosette Aechmea magdalenae, which had lower efficiencies because of their steeper leaf angles. In fact, differences in PFD absorbed by individual plants were mostly determined by the PFD available at each particular site and only to a small extent by differences in crown architecture between individuals or species (Table 4, Fig. 5). In a study of six rainforest tree species Poorter and Werger (1999)
reached a parallel conclusion on the relative importance of environmental vs. specific differences: differences in crown architecture between plants growing in different environments (sun-shade) were more significant than those between species within the same environment. One of the species studied here, Alseis blackiana, was described as a pioneer tree of a remarkable shade tolerance (Dalling et al., 2001
). Shade tolerance of the seedlings of this tree was suspected to be achieved at least in part by an efficient light interception. However, our comparative results indicate that Ea of A. blackiana was not significantly larger than that of other 16 co-occurring, morphologically contrasting species (Fig. 3) and its Ed only differed from that of the climber species (Table 4).
Among the variables studied, leaf angle had the largest effect on foliage display efficiency (Fig. 5) while S, SLA, and IL/LL, which are related to allocation to leaf area, leaf spacing and support, had smaller but still significant effects. Our results indicate that plant foliage in the understory is, in general, preferentially oriented towards the brightest regions of the sky (i.e., sky sectors within the annual range of sunpaths and at 45–90° zenith angle, Fig. 4). As most light originates near the zenith in tropical forest understories this conforms to the common observation that understory plants typically have horizontally displayed leaves. The canopy gap fraction is typically greatest near the zenith because at lower elevation angles the pathlength through the canopy is greater. A trade-off to orienting most of the foliage towards a particular region of the sky is that there is a decreased efficiency of light absorption because of increased self-shading and reduced cosines of incidence for other regions of the sky. In sites with strong sidelight such as gap edges, Ackerly and Bazzaz (1995)
and Clearwater and Gould (1995)
have demonstrated a pronounced reorientation of leaves so that the lamina are facing the brightest regions.
Efficient light capture generally requires substantial biomass allocation to support leaves in a manner that minimizes self-shading and maintains efficient angular display relative to the prevailing light direction. However, thin leaves and increased allocation to leaf vs. supporting tissues are characteristic features of shade-tolerant species (King, 1991
). There must also be a continuous redeployment of resources during growth to minimize self-shading, which can become prohibitively expensive in light-limited habitats (King, 1991
; Poorter and Werger, 1999
). Also, constraining the dynamic function of crown expansion is the trade-off between the height growth required to take advantage of the strong vertical gradient of light availability even at the lowest levels in the understory and the lateral crown extension that is helpful in minimizing self-shading (Kohyama and Hotta, 1990
). In addition, other crown functions, such as hydraulics, reproduction, and minimizing damage due to falling debris in the understory, all impact the evolution of crown form. These constraints and trade-offs may account for the values of Ea exhibiting an apparent ceiling of about 0.75 (Fig. 3). As argued by Kohyama (1987)
, the architectural and allometric diversity found in forest understory plants can be related to trade-offs between these different traits and functions. This is consistent with the emergence in adaptive walk models of a greater number of potential optimal crown forms as more functions are considered (Niklas, 1994
).
Although there is a strong convergence in light-capture efficiency, the remaining small differences in Ea can have important consequences for light capture and carbon gain (Pearcy and Yang, 1998
). Comparison of Hybanthus prunifolium and Ossea quinquenervia nicely illustrates important architectural trade-offs. The aLAR of O. quinquenervia was more than threefold higher than that of H. prunifolium (Table 4). However, O. quinquenervia invested relatively little in support and consequently exhibited considerable self-shading and an Ea of 0.55, which was at the lower end of the range observed. In contrast, H. prunifolium invested far more in support to achieve a low level of self-shading and consequently exhibited a higher Ea of 0.74. Because of its low self-shading, H. prunifolium absorbed approximately 30% more of the available PFD per unit leaf area than O. quinquenervia. But despite its much lower Ea, O. quinquenervia was able to maintain a higher aboveground aLARe than H. prunifolium (data not shown, 12.5 vs. 5.0 m2/kg, respectively) because of its small investment in support tissues. These differences translate into potentially higher daily carbon gain for O. quinquenervia as compared to H. prunifolium (data not shown, 2.0 vs. 0.7 mol CO2·m–2·d–1, respectively; simulated in Y-plant using mean shade-plant photosynthetic properties from BCI, see Valladares, Allen, and Pearcy, 1997
; Valladares et al., 2000
). The arching stem of H. prunifolium may however give it an offsetting competitive advantage over O. quinquenervia since it is generally taller. Moreover, greater root costs to support water supply to the greater leaf area may offset some of the carbon gain advantage of O. quinquenervia.
Interestingly, the three climber species had the three lowest Ea values (Fig. 3). The Ea is significantly influenced by self-shading, and, in the case of the climbers, shading by the host tree. Climbing species are constrained in their growth direction and leaf display by the host orientation. This results in reduced whole-plant light capture in the understory on a leaf area basis. However, climbers typically invest relatively little in support per unit crown leaf area. Consequently, aLARe values for two of these climbing species (Monstera dilacerata and Paullinia bracteosa), although low, were not ranked at the bottom as they had been for Ea (data not shown). In the case of the third climbing species (Monstera dubia), leaves were vertically oriented and tightly appressed to the tree in the juvenile stage. This further reduced the efficiency of light absorption on a leaf area basis, which translated in a very low aLARe.
It is also interesting to note that among the 21 nonclimber species, Aechmea magdalenae had, on average, the lowest canopy light absorption efficiency (Fig. 3). It has been shown that on BCI this Bromeliad species has a significantly higher photosynthetic capacity and allocates significantly more biomass to photosynthetic tissues than comparable co-occurring understory plants (Skillman, Garcia, and Winter, 1999
). Paradoxically, despite having a high potential for plant carbon gain based upon both leaf physiology and biomass allocation, Skillman, Garcia, and Winter (1999)
found that Aechmea magdalenae has a lower aboveground relative growth rate than comparable co-occurring understory plants on BCI. Our findings that the vertically oriented leaves of this Bromeliad rosette result in Ea values significantly lower than most of the other understory species in this survey seems to resolve this paradox. Indeed, the high photosynthetic capacity and the high biomass allocation to leaf tissue observed in Aechmea magdalenae may be viewed as means of compensating for the characteristic vertical leaf orientation that is suboptimal for light capture in the shade.
In most plants, leaf primordia at the apex originate as far as possible from each other (Hofmeister's rule; Jean, 1984
; Kirchoff and Rutishauser, 1990
), which in plants with a helical phyllotaxy yields a divergence angle between consecutive leaves that is close to the "golden angle" of 137.5°. For an erect shoot, such an angle minimizes leaf overlap in the vertical projection (Bell, 1993
; Valladares, 1999
), leading to its interpretation as a mechanism for increasing leaf display efficiency (Adler, Barabe, and Jean, 1997
). Some unusual patterns, such as the monostichous phyllotaxis of Costus (see Fig. 2) with low divergence angles (20–30°), are by themselves difficult to interpret even after many years of study (Kirchoff and Rutishauser, 1990
; and references therein) because significant leaf overlap occurs. However, when coupled with a helical twining of the stem, such as is observed in Costus pulverulentus (yielding a spiromonostichous phyllotaxis; Bell, 1993
), the leaves are displaced laterally, significantly increasing Ea. The Y-plant simulations, with either a helical stem or a straight vertical stem, demonstrated that the latter gave 20% lower values of Ea, demonstrating the importance of coupling the monostichous phyllotaxy with a helical stem in this instance.
Distichy, characteristically orthodistichy, which is the typical phyllotaxy of monocotyledons (Wilder, 1992
; and references therein), causes there to be two vertical rows of leaves and therefore the potential for much mutual shading in understory environments. For the monocot species studied here, compensation for the potentially inefficient leaf display was achieved by either an arced stem (Renealmia cernua; Fig. 1), by plagiotropic shoots (Dichorisandra hexandra), long petioles (Heliconia vaginalis), or by sparse canopies (Cyclanthus bipartitus). Studies of simulated, simple shoot architectures have demonstrated that other architectural characters can compensate for potentially inefficient phyllotaxes (Niklas, 1988
; Sekimura, 1995
). Our study demonstrates that compensation for potentially inefficient phyllotaxes also can be observed among real plants in a tropical forest understory.
Leaves are the ultimate sink for light, and their optical properties can significantly affect whole plant light capture. Shade plants usually have higher chlorophyll contents per unit leaf mass basis but also thinner leaves with high specific leaf areas as compared to sun plants (e.g., Bongers and Popma, 1990
). As observed in previous studies (see Poorter et al. [2000]
; and references therein), SLA had a negative effect on leaf absorptance. However, leaf absorptance did not significantly affect the total PFD absorbed by the whole plant due to the narrow range of leaf absorptances exhibited by the different species studied here (82–92%). Consequently, available PFD at each site was the only variable leading to significant differences in light harvesting among the plants studied.
Terrestrial plants are developmentally versatile because as sedentary light capturers they must accommodate the diurnal, seasonal, and long-term changes in light environments (Niklas, 1988
). Tropical plants exhibit a remarkable phenotypic plasticity, and a large effort has gone into the investigation of their response to light gradients (Kitajima, 1996
; Agyeman, Swaine, and Thompson, 1999
; Valladares, 2000
; Valladares et al., 2000
). Most of these studies address leaf-level physiology (e.g., Evans, von Caemmerer, and Adams, 1988
; Valladares, Allen, and Pearcy, 1997
; see also Lambers, Chapin, and Pons, 1998
) but resource allocation to maintaining an efficient leaf display that minimizes leaf overlap is at least as critical if less studied. Our results emphasize the compensatory role of different leaf and crown characters in determining the efficiency of light capture and indicate that the variety of shoot morphologies capable of capturing similar fluxes of solar radiation is larger than initially thought, extending over species with very different phyllotactic patterns and contrasting crown architectures and leaf sizes.
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FOOTNOTES |
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5 Author for reprint requests (valladares{at}ccma.csic.es
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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0.2 are significant (P < 0.01). The residual terms are represented by U