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Ecology |
Department of Biology, University of Miami, Coral Gables, Florida 33124-0421 USA
Received for publication January 12, 2004. Accepted for publication August 26, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Convolvulaceae • gas exchange methodology • Ipomoea pes-caprae • subtropical beaches • vine
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Functionally symmetric leaves are amphistomatous and have palisade parenchyma beneath both the adaxial and abaxial epidermises. Symmetry is commonly reported for plants with vertically inclined leaves that grow in high-light environments and in xeromorphic species (Fahn, 1990
).
We would expect that the effects of high and low reflected light flux on the abaxial leaf surface would be similar to whole-leaf responses to sun and shade. These responses, described by Boardman (1977)
and Bjorkman (1981)
, are attributed to modifications in physiology, anatomy, and optical properties. In general, photosynthetic parameters of leaves in the sun differ from those of shaded leaves (Boardman, 1977
). Shaded leaves typically have lower dark respiration rates (Marler et al., 1994
), light compensation points, and photosynthetic maxima (Avalos and Mulkey, 1999
) than do sun-exposed leaves. Anatomically, shade leaves are thinner than sun leaves because of reduced palisade parenchyma layers, and they have a lower stomatal density (Sims and Pearcy, 1992
). Optical properties of leaves may also be influenced by the light regime (Mooney et al., 1977
; Ehleringer and Bjorkman, 1978
). Plants in high light environments often reduce light absorption (Ehleringer, 1981
; Lee and Graham, 1986
) and by doing so lower leaf temperature, transpiration, and metabolic rate, all of which may be advantageous under stress conditions (Ehleringer, 1981
).
Adaxial and abaxial surfaces of functionally symmetric leaves would have to respond virtually independently to their local light regimes to detect an effect of reflected light heterogeneity. DeLucia et al. (1991)
investigated photosynthetic rates and palisade thickness of species with functionally symmetric leaves held at different inclination angles, thus altering light flux intercepted by the leaf surface and confirmed that abaxial and adaxial surfaces of functionally symmetric leaves can respond virtually independently to their local light. The vertical-leaf species Eryngium yuccifolium intercepted the same amount of light on the adaxial and abaxial leaf surfaces and, therefore, the rates of photosynthesis and palisade thickness were equal for each surface. Conversely, the horizontal-leaf species Solidago canadensis intercepted more light on the adaxial than abaxial surface and the adaxial surface showed higher rates of photosynthesis and greater palisade thickness than the abaxial. In general, responses to direct light heterogeneity of abaxial and adaxial surfaces are similar to those of sun and shade leaves.
The objective of this study was to determine whether heterogeneous reflected light conditions, which occur in a natural sand dune habitat, affect the leaf-level processes of vegetation. Using a model species with functionally symmetric leaves, the general approach was to compare gas exchange, anatomy, and optical properties of adaxial and abaxial surfaces within individual leaves and among leaves borne in high and low reflected light environments in situ. To accomplish this, we introduce a new methodology to simultaneously illuminate and measure leaf gas exchange on one leaf surface at a time in situ. We test the following hypotheses (1) abaxial leaf surfaces show plasticity in response to a heterogeneous reflected light environment, and (2) heterogeneous reflected light influences asymmetry in gas exchange, anatomy, and optical properties between abaxial and adaxial surfaces of individual leaves.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Woodbury et al., 1977
; Johnson and Barbour, 1990
). The leaves of I. pes-caprae are alternately arranged, amphistomatous, and have adaxial and abaxial palisade parenchyma that is separated by a central layer of spongy mesophyll tissue. Although diurnal heliotropic leaves have been reported within the genus Ipomoea (Darwin, 1881
) and seasonal heliotropism of flowers has been reported in I. pes-caprae (Patino et al., 2002
), there is no evidence to suggest the leaves of I. pes-caprae are heliotropic. Ipomoea pes-caprae is an ideal candidate for this study because it grows horizontally over various types of groundcover substrates, and thereby it does not self-shade from reflected light as would a vertical leaf arrangement. This research was conducted on the sand dunes at Bill Baggs State Park in Key Biscayne, Florida (25°68' N, 80°15' E). The dunes extend from the tidal edge to approximately 50 m inland where a hardwood hammock community begins. The climate is humid subtropical with an average annual rainfall of 1325 mm and a well-defined dry season (November through May). Data were collected during the dry season between November 1999 and March 2000.
Twenty individuals of I. pes-caprae, 10 growing over patches of sand and 10 over vegetation, were identified from which a subset of five individuals from each patch type were randomly selected for this experiment. The groundcover, either sand or vegetation, extended at least 30 cm in all directions around selected leaves. Direct and reflected light flux was measured in each patch with a quantum radiometer photometer (LI-COR 185B; LI-COR, Lincoln, Nebraska, USA) that integrated wavelengths in PAR during sunny and dry conditions on 3 March, 2000 between 1300 and 1400. The light sensor pointed toward the ground to measure the intensity of reflectance, and the sensor was turned skyward to measure direct sunlight. Measurements were taken 10 cm above patches, approximately the same height as the leaves of I. pes-caprae. The air saturation deficit (D) was calculated from values of ambient air temperature (Ta) and relative humidity (Rh) within the patches that were recorded during measurement of light response curves (Jan–Mar 2000) by a portable photosynthesis system (LI-COR 6400).
Nutrients and leaf angles
Nutrient content, azimuth orientation, and inclination and drip angles of leaves may alter photosynthetic rate, therefore these factors were measured to address the possibility they may confound the effects of reflected light on photosynthesis. Nitrogen and carbon concentrations of leaves used for light response curves were measured with a Carlo-Erba NC 2100 analyzer after leaf tissues were dried at 60°C for 5 d (N = 4 plants x 3 leaves x 2 patch types = 24). Nitrogen can be preferentially distributed to younger leaves, a process that results in lower rates of photosynthesis in older leaves (Hikosaka et al., 1994
; Kitajima et al., 1997
). Therefore, internode position was restricted to the first six leaves that were fully expanded to eliminate effects of leaf age on photosynthesis that may have confounded those of reflected light. Nutrient content of leaves within the same patch type was compared between internode positions (linear regression), and, between leaves from sand and vegetation patches (one-way ANOVA).
Leaf angles were measured in situ (N = 5 plants x 3 leaves x 2 patch types = 30) and compared between leaves in different patch types (one-way ANOVA). Azimuth was measured as the compass direction into which a line along the midrib points (from petiole to leaf apex). Elevation angle, the angle from which the midrib deviates from the horizontal, and drip angle, the inclination of the steepest angle of the two halves of the folded leaf, were measured with an inclinometer (Dasco Pro, Rockford, Illinois, USA). Circular mean inclination angle and parametric circular standard error of the mean were calculated using methods described by Fisher (1993)
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Anatomy and optical properties
Leaf tissue thickness of the epidermal layers, palisade parenchyma, spongy mesophyll, and stomatal density were measured on the same leaves measured for gas exchange within 6 h after collection from the field (N = 3 plants x 5 leaves x 2 patches = 30). Three transverse sections of each leaf were cut from the tissue between the midrib and leaf margins. Tissue thickness of each section was measured with a light microscope equipped with an ocular micrometer at 350x magnification. The mean values of the tissue thickness from each leaf were calculated. Means were compared between two main effects of leaf surface and reflected light environment (two-way ANOVA and t test for mesophyll layers). Stomata were dyed with a waterproof black marker before they were counted at 350x magnification. Stomate density was compared between abaxial and adaxial surfaces in each reflected light treatment (two-way ANOVA).
Five leaves from each patch type (N = 5 plants x 1 leaf x 2 patches = 10) were collected from the field in March 2000, and kept in plastic bags with moist paper towels to prevent water loss until their optical properties were analyzed in the laboratory several hours later. Reflectance and transmittance of adaxial and abaxial surfaces were measured over the spectral range of 400–700 nm using a spectroradiometer and integrating sphere (Li1800/22, LI-COR). Absorptance was calculated with the following equation
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Isolation of gas exchange on one leaf surface
Gas exchange of one leaf surface is often measured using a leaf-disk oxygen electrode. The method is intended to measure oxygen evolution under conditions of CO2 saturation and requires that leaf disks are first excised from a plant, then brought to the laboratory for analysis (Delieu and Walker, 1981
; DeLucia et al., 1991
). In this study we developed a method to illuminate and measure gas exchange of one leaf surface in situ and under varying CO2 conditions with an infrared gas analyzer (IRGA) (LICOR 6400 portable photosynthesis system). First, the lower half of the IRGA chamber was covered with two layers of polyethylene. Next, the leaf was placed on top of the polyethylene layer, and the chamber was closed. This procedure ensured that gas exchange was measured in only the upper half of the chamber, where the LED light sources is located. Therefore, it was possible to measure gas exchange on the same half of the leaf that was illuminated.
The method was tested using Vitis rotundifolia because the leaf anatomy of this species is dorsoventral (asymmetric). Palisade parenchyma lies below the adaxial epidermis, followed by the spongy mesophyll and the abaxial epidermis. There is no abaxial palisade layer. Stomata are primarily on the abaxial surface. The adaxial surface has few stomata (3 stomata/0.6 mm2 leaf surface area), therefore the IRGA should measure little-to-no gas exchange on the adaxial surface if this method is effective. Each leaf surface was acclimated to 900 µmol photons · m–2 · s–1 for 10 min before measurement (N = 5). The effectiveness of the method was verified by a near-zero measurement of abaxial gas exchange (Fig. 1).
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):
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Nutrients and inclination angles
Leaves from internode positions 2–6 did not show significant differences in nitrogen concentration (y = 3.22 – 0.13 x, R2adj = 0.31, P = 0.06) or photosynthetic response (y = 24.7 – 1.11 x, R2adj = 0.08, P = 0.24) related to leaf age. Nitrogen and carbon concentration did not differ significantly for leaves borne over sand or vegetation patches (Table 2). Azimuth, drip, and elevation of leaves from each patch type were also not significantly different (Table 2).
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Photosynthetic response to light
The mean abaxial photosynthetic maximum (Pmax) was 2.6 times higher for leaves borne over sand then those borne over vegetation (Table 4), and, Pmax of abaxial surfaces were significantly lower than those of the adaxial surfaces (Fig. 2). The Pmax of adaxial surfaces, which received the same amount of direct sunlight, were not significantly different between reflected light environments (
= 0.05, P = 0.43, Fig. 2). The mean value for Pmax of the adaxial surfaces was 45% higher than that of the abaxial surfaces in sand patches and 76% higher than that of the abaxial surfaces in the vegetation patch (Table 4). Values for light compensation points (Ic) followed the same pattern as Pmax but did not differ significantly ( = 0.05, P = 0.08, Table 4) between abaxial and abaxial surfaces in sand and vegetation patches. Dark respiration of both leaf surfaces was statistically different between patches (P < 0.05, Table 4), however within a patch type there was no difference between the leaf surfaces.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Because there was no correlation between leaf age and photosynthetic response with nutrient content we conclude that fully expanded leaves within six internode positions were close enough in age to avoid nutrient discrimination. Nutrient content and angles of leaves in different patches did not significantly differ and therefore did not confound the effects of reflected light on photosynthesis.
In general, the more light flux, direct or reflected, a leaf surface intercepted, the thicker the palisade layer was. This is consistent with the generalization that sun leaves have thicker palisade layers than those of shade leaves (Oberbauer and Strain, 1986
). We expected leaves with the thickest palisade tissue layers to also have greatest total leave thickness, therefore we expected leaves of I. pes-caprae over sand to be thickest (Table 3). Overall thickness of the adaxial and abaxial palisade layers was greatest for I. pes-caprae leaves borne over sand. However, the mesophyll layer was thinner for leaves over sand than vegetation; consequently overall leaf thickness was greater for leaves over vegetation. The enhanced spongy mesophyll layer of the leaves over vegetation may be in response to greater air saturation deficit of the vegetation patches with respect to sand, and an indication of water stress. Spongy cells in I. pes-caprae are large and contain few chloroplasts. These types of cells often store water (Fahn, 1990
), and are considered a feature of xeromorphic plants that enables them to withstand periods of water stress in arid or saline environments (Wickens, 1998
).
Plants growing in high-light environments often absorb less light than plants from other environments because they tend to be at a higher risk for temperature stress (Ehleringer, 1981
). Abaxial and adaxial leaf surfaces of I. pes-caprae absorbed between 77 and 81% of photosynthetic photon flux density (PPFD) (Table 3). These values are slightly lower than the average absorptance of 85% recorded for broadleaf species common to the Sonoran desert (Ehleringer and Bjorkman, 1978
; Ehleringer, 1981
). It is unclear how I. pes-caprae regulates absorption because the leaves lack epidermal hairs and spines. Further investigation is needed to determine the mechanism by which light absorption is regulated.
Abaxial surfaces of leaves over sand showed a significantly higher Pmax than the leaves over vegetation. Our results for the effects of high and low reflected light flux on abaxial leaf surfaces concur with results published on the effects of direct and diffuse light on leaf surface response (DeLucia et al., 1991
; Poulson and DeLucia, 1993
), and to numerous studies of sun and shade leaves (Boardman, 1977
; Bjorkman, 1981
; Mulkey, 1986
; Oberbauer and Strain, 1986
; Marler et al., 1994
; Avalos and Mulkey, 1999
). Pmax may be greatest for leaf surfaces that received the most light because those leaves also had the thickest palisade tissue layers. Palisade tissues contain high-activity sun-type chloroplasts that have high concentrations of chlorophyll (Terashima and Yorinao, 1989
). Biochemical attributes of high photosynthetic capacity in sun-adapted leaves include the ratio of sun-to-shade chloroplasts (Terashima and Inoue, 1985
), high chlorophyll (Chl) a/b ratio (Boardman, 1977
), high carboxylation capacity (Terashima and Takenaka, 1986
), and high electron transport efficiency (Evans, 1988
). Chloroplast-type and biochemistry within the abaxial and adaxial parenchyma layers may adapt to the local light environment and contribute to differences in photosynthetic capacity between the two surfaces.
In comparison to other vines, the Pmax of I. pes-caprae is among the highest. The range of Pmax observed for vines species growing in tropical forest ecosystems is between 6.9 and 25 µmol CO2 · m–2 · s–1 (Castellanos, 1991
), and for temperate vines in open field pastures it ranges between 23 and 27 µmol CO2 · m–2 · s–1 (Carter and Teramura, 1988
). The adaxial Pmax of I. pes-caprae ranged between 13.4 and 23.0 µmol CO2 · m–2 · s–1. The high photosynthetic maxima may contribute to the fast rates of growth reported for this species (Devall, 1992
) and the overall success of I. pes-caprae as a pioneer species (St. John, 1970
; Devall and Thien, 1992
).
The compensation point (Ic) is the amount of light for which CO2 respired equals CO2 assimilated during gas exchange. Even the lowest average Ic for I. pes-caprae (56.87 µmol CO2 · m–2 · s–1 at 30.5°C, abaxial surface in the vegetation patches) is high in comparison to other plant species. The Ic value for sun leaves of tropical forest trees ranges from 15 to 25 µmol CO2 · m–2 · s–1 and for herbaceous heliophytes it ranges from 20 to 40 µmol CO2 · m–2 · s–1 (Larcher, 1995
). Vines tend to have Ic values near the high end of the range for all growth forms. The Ic value of Pueraria lobata, the weedy exotic vine commonly called Kudzu, is 43 µmol CO2 · m–2 · s–1 at 30°C (Carter and Teramura, 1988
). Vines adapted to the high light conditions of open fields in Maryland have Ic points that range from 25–35 µmol CO2 · m–2 · s–1 at 30°C (Carter et al., 1989
). Further studies of tropical dune and desert plants are needed to determine how CO2 compensation points for I. pes-caprae relate to other species from beaches and similar high-light environments.
Plasticity, as defined by Strauss-Debenedetti and Bazzaz (1996)
, is associated with the spatial component of phenotypic expression, and describes how individuals borne into different spatial locations respond to the variation in environmental conditions at those respective locations. Ipomoea pes-caprae exhibited a high degree of photosynthetic and anatomical plasticity in response to reflected light conditions in different spatial locations. A high degree of plasticity by vines in response to light variation is thought to be a characteristic that enables them to be successful when direct and diffuse light is heterogeneous (Castellanos, 1991
; Avalos and Mulkey, 1999
). Our study suggests that plasticity may be important for success when reflected light is heterogeneous as well. Additionally, plasticity is considered an important characteristic of pioneer species (Oberbauer and Strain, 1986
; Strauss-Debenedetti and Bazzaz, 1996
). Accordingly I. pes-caprae is considered a successful pioneer species (St. John, 1970
; Devall and Thien, 1992
). Ipomoea pes-caprae demonstrated the ability to harvest reflected light and exhibited a high degree of plasticity in response to variation in reflected light, undoubtedly these are features that contribute to its success in the dune environment.
In summary, we have identified how patchiness of groundcover substrates on the dune causes a heterogeneous reflected light environment, and in turn how a representative species from the dune, Ipomoea pes-caprae, demonstrates a high degree of leaf-level plasticity in response to the heterogeneous reflected light. These results contribute to our understanding of the microclimate dynamics of sand dune ecosystems because we have identified a link between resource heterogeneity and vegetation that was not previously considered. In a broader sense, the results of this study reveal that reflected light may be an important component of the light regime for vegetation from habitats that lack an overhead canopy and that are characterized by groundcover substrates with high albedo values, in addition to sand dunes these ecosystems may include deserts, rocky outcrops, and semi-arid habitats.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Boardman N. K. 1977 Comparative photosynthesis of sun and shade plants. Annual Review Plant Physiology 28: 355-377
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Sims S. A. R. W. Pearcy 1992 Response of leaf anatomy and photosynthetic capacity in Alocasia macrorrhiza (Araceae) to a transfer from low to high light. American Journal of Botany 79: 449-455[CrossRef][ISI]
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Terashima I. Y. Inoue 1985 Palisade tissue chloroplasts and spongy tissue chloroplasts in spinach: biochemical and ultrastructural differences. In Biological control of photosynthesis: proceedings from "Limburgs Snivesitair Centrum", 219–230. Diepenbeek, Belgium
Terashima I. A. Takenaka 1986 Organization of photosynthetic system of dorsiventral leaves as adapted to the irradiation from the adaxial side. In R. Marcelle, H. Clijsters, and M. Van Poucke [eds.], Biological control of photosynthesis, 219–230. Marinus Nigjoff Publishers, Dordrecht, Germany
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) abaxial surface only, high-density stomates present; (•) adaxial surface only low-density stomates
, abaxial 
) and vegetation (adaxial 
, abaxial •) during January– March 2000. Net photosynthetic gas exchange was measured as CO2 flux. Each symbol represents the mean (±1 SE indicated by error bars) of 15 observations