Occurrence of homobaric and heterobaric leaves in two forest types of southern Brazil

Boeger, Maria Regina Torres; Silva, Maiara Matilde; Nogueira, Guilherme; Alvarenga, Allan; Pereto, Suellen Silva

doi:10.1590/0102-33062016abb0064

ABSTRACT

In ombrophilous forests, light stratification provokes different adjustments by plants for better use of the environmental conditions of each stratum. Among the morphological traits that vary with strata, the presence of bundle sheath extensions (BSEs) is related to water transport, photosynthesis, and leaf mechanical support and classifies leaves as homobaric or heterobaric. This study analyzed the proportion of these types of leaves in a Lowland Ombrophilous Dense Forest (LLODF) and a Mixed Ombrophilous Forest (MOF), and among the strata of each forest type. The morphological leaf traits of 89 LLODF tree species and 57 MOF tree species were examined. The proportion of homobaric and heterobaric leaves did not differ between forests. However, in both forest types, the distribution of species with heterobaric or homobaric leaves depended on strata, with heterobaric species occurring mainly in higher strata, and homobaric species in lower strata. Thus, light stratification acts as an ecological filter on the composition of the vegetation of these forests, favoring heterobaric species in places with higher light intensity and temperature, such as the highest strata of canopy. On the other hand, homobaric species are more frequent in lower strata, where light is less available and humidity higher.

Keywords
bundle sheath extension; leaf morphological traits; light stratification; Lowland Ombrophilous Dense Forest; Mixed Ombrophilous Forest

Introduction

Environmental factors affect the growth and survival of plants (Valladares & Niinemets 2008Valladares F, Niinemets Ü. 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution and Systematics 39: 237-257. ) and influence their internal organization (Dickson 2000Dickson WC. 2000. Integrative plant anatomy. San Diego, Academic Press.). In forests, variation in abiotic features along vertical stratification provokes different adjustments by plants for better use of the environmental conditions of each stratum (Valladares & Niinemets 2008Valladares F, Niinemets Ü. 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution and Systematics 39: 237-257. ; Niinemets 2010Niinements Ü. 2010. A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecological Research 25: 693-714. ; Inoue et al. 2015Inoue Y, Kenzo T, Tanaka-Oda A, Yoneyama A, Ichie T. 2015. Leaf water use in heterobaric and homobaric leafed canopy tree species in a Malaysian tropical rain forest. Photosynthetica 53: 177-186.). Such adjustments can be morphological, physiological, and/or phenological. Among such morphological traits, the presence of bundle sheath extensions (BSEs) is related to water transport (Zwieniecki et al. 2007Zwieniecki MA, Brodribb TJ, Holbrook NM. 2007. Hydraulic design of leaves: insights from rehydration kinetics. Plant Cell Environment 30: 910-921), photosynthesis (Pieruschka et al. 2010Pieruschka R, Chavarría-Krauser A, Schurr U, Jahnke S. 2010 Photosynthesis in lightfleck areas of homobaric and heterobaric leaves. Journal of Experimental Botany 61: 1031-1039. ), and leaf mechanical support (Turner 1994Turner IM. 1994. A quantitative analysis of leaf form in woody plants from the world's major broad leaved forest types. Journal of Biogeography 21: 413-419.).

Bundle-sheath extensions (BSEs) are formed by parenchyma or sclerenchyma cells that extend from the vascular bundle to both sides of the leaf epidermis (Karabourniotis et al. 2000Karabourniotis G, Bornman JF, Nikolopoulos D. 2000. A possible optical role of the bundle sheath extensions of the heterobaric leaves of Vitis vinifera and Quercus coccifera. Plant, Cell and Environment 23: 423-430.; Nikolopoulos et al. 2002Nikolopoulos D, Liakopoulos G, Drossopoulos I, Karabourniotis G. 2002. The relationship between anatomy and photosynthetic performance of heterobaric leaves. Plant Physiology 129: 235-243. ). Leaves are classified as homobaric or heterobaric depending on the condition of the BSEs (Kenzo et al. 2007Kenzo T, Ichie T, Watanabe Y, Hiromi T. 2007. Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. American Journal of Botany 94: 764-775.). The former lack, or have incomplete, BSEs and their mesophyll is more homogeneous. The latter have complete BSEs and their mesophyll is divided into several photosynthetic compartments (Karabourniotis et al. 2000Karabourniotis G, Bornman JF, Nikolopoulos D. 2000. A possible optical role of the bundle sheath extensions of the heterobaric leaves of Vitis vinifera and Quercus coccifera. Plant, Cell and Environment 23: 423-430.; Nikolopoulos et al. 2002Nikolopoulos D, Liakopoulos G, Drossopoulos I, Karabourniotis G. 2002. The relationship between anatomy and photosynthetic performance of heterobaric leaves. Plant Physiology 129: 235-243. ; Kenzo et al. 2007Kenzo T, Ichie T, Watanabe Y, Hiromi T. 2007. Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. American Journal of Botany 94: 764-775.). Homobaric leaves have a continuous mesophyll (Terashima 1992Terashima I. 1992. Anatomy of non-uniform leaf photosynthesis. Photosynthesis Research, 31: 195-212. doi: 10.1007/BF00035537.
https://doi.org/10.1007/BF00035537... ).

Such structural differences are reflected in the functional proprieties of these leaf types (Kenzo et al. 2007Kenzo T, Ichie T, Watanabe Y, Hiromi T. 2007. Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. American Journal of Botany 94: 764-775.; Pieruschka et al. 2010Pieruschka R, Chavarría-Krauser A, Schurr U, Jahnke S. 2010 Photosynthesis in lightfleck areas of homobaric and heterobaric leaves. Journal of Experimental Botany 61: 1031-1039. ; Lynch et al. 2012Lynch DJ, McInerney FA, Kouwenberg LL, Gonzalez-Meler MA. 2012. Plasticity in bundle sheath extensions of heterobaric leaves. American Journal of Botany 99: 1197-1206.; Inoue et al. 2015Inoue Y, Kenzo T, Tanaka-Oda A, Yoneyama A, Ichie T. 2015. Leaf water use in heterobaric and homobaric leafed canopy tree species in a Malaysian tropical rain forest. Photosynthetica 53: 177-186.). The presence of BSEs can protect leaf lamina from hydric stress and increase light absorption and mechanical support (Terashima 1992Terashima I. 1992. Anatomy of non-uniform leaf photosynthesis. Photosynthesis Research, 31: 195-212. doi: 10.1007/BF00035537.
https://doi.org/10.1007/BF00035537... ; Karabourniotis 1998Karabourniotis G. 1998. Light-guiding function of foliar sclereids in the evergreen sclerophyll Phillyrea latifolia: a quantitative approach. Journal of Experimental Botany 49: 739-746. ; Nikolopoulos et al. 2002Nikolopoulos D, Liakopoulos G, Drossopoulos I, Karabourniotis G. 2002. The relationship between anatomy and photosynthetic performance of heterobaric leaves. Plant Physiology 129: 235-243. ; Rhizopoulou & Psaras 2003Rhizopoulou S, Psaras G. 2003. Development and structure of drought-tolerant leavesof the Mediterranean shrub Capparis spinosa L. Annals of Botany 92: 377-383. ). Yet in homobaric leaves, gas diffusion in the mesophyll can be more efficient due the absence of BSEs (Pieruschka et al. 2006Pieruschka R, Schuur U, Jensen M, Wolff WF, Jahnke S. 2006. Lateral diffusion of CO2from shaded to illuminate leaf parts affects photosynthesis inside homobaric leaves. New Phytologist 169: 779-788. ). Also, BSEs have been linked to light distribution within the mesophyll, allowing investments in thicker and, consequently, smaller leaves (Nikolopoulos et al. 2002Nikolopoulos D, Liakopoulos G, Drossopoulos I, Karabourniotis G. 2002. The relationship between anatomy and photosynthetic performance of heterobaric leaves. Plant Physiology 129: 235-243. ).

Despite the light heterogeneity that characterizes Brazilian forests, the occurrence of heterobaric leaves in many plant formations of these biomes and their relation to light gradients is still poorly studied. This study reports on the morpho-anatomical traits of tree species from a Lowland Ombrophilous Dense Forest and a Mixed Ombrophilous Forest in order to investigate the presence and proportion of homobaric and heterobaric leaves in both forest types. Our hypotheses are: a) the frequency of heterobaric leaves is similar in the two studied forest types since both experience similar environmental conditions (annual precipitation and light stratification), independent of their floral composition; b) the distribution and frequency of homobaric and heterobaric leaves vary among different forest strata in response to light stratification, with heterobaric leaves occurring mainly in upper strata and c) leaf type is dependent upon micro-environmental features more so than taxonomic group, as represented by families and/or genus.

Materials and methods

This study was based on leaf morphological data collected during previous studies in two forest sites: a Lowland Ombrophilous Dense Forest (LLODF), located at Volta Velha Reserve (26º04'S, 48º38'W), within the city of Itapoá, SC (a detailed description can be found in Boeger et al. 2004Boeger MRT, Alves LC, Negrelle RRB. 2004. Leaf morphology of 89 tree species from a lowland tropical rain forest (Atlantic forest) in South Brazil. Brazilian Archives of Biology and Technology 47: 933-943. ); and a Mixed Ombrophilous Forest (MOF), located in the Botanical Garden Francisca Maria Garfunkel Rischbieter (25º23'10"S, 49º12'58''W), within the boundaries of the city of Curitiba, PR (for more details, see Silveira et al. 2015Silveira TA, Boeger MRT, Maranho LT, Melo Jr. JCF, Soffiatti P. 2015. Functional leaf traits of 57 woody species of the Araucaria Forest, Southern Brazil. Brazilian Journal of Botany 38: 357-366. ). The environmental characteristics of each forest type are summarized in Tab. 1. All species included in this study were selected according to two criteria: 1) higher values of importance based on a previous phytosociological survey and 2) the presence of at least three individuals in the forest type. All specimens of collected from LLODF were deposited in UPCB (Herbarium of Department de Botany, UFPR, Curitiba, PR) and specimens from MOF were deposited in MBM (Herbarium of Municipal Botanical Museum, Curitiba, PR).

Thumbnail

Table 1
Environmental features of studied sites. Legend: LLODF - Lowland Ombrophilous Dense Forest; MOF: Mixed Ombrophilous Forest. Climate type according to Köppen classification.

Morphological data, such as leaf area, leaf thickness, and the presence of homobaric and heterobaric leaves, were collected from 89 LLODF (Tab. 2) and 57 MOF tree species (Tab. 3). Leaves with complete BSEs were classified as heterobaric while leaves with incomplete and/or no BSEs were classified as homobaric leaves, according to Kenzo et al. (2007Kenzo T, Ichie T, Watanabe Y, Hiromi T. 2007. Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. American Journal of Botany 94: 764-775.). The nomenclature and taxonomic classification of each species were checked against International Plant Names Index (www.ipni.org).

Thumbnail

Table 2
Presence and absence of bundle sheath extension (BSE) on tree species from Lowland Ombrophilous Dense Forest, by stratum.

Thumbnail

Table 3
Presence and absence of bundle sheath extension (BSE) on tree species from Mixed Ombrophilous Forest, by stratum.

All species were classified according to their occurrence in four strata. Species of LLODF were classified into: Stratum 1, <5 m; Stratum 2, 5 - 9.99 m; Stratum 3, 10 - 14.99 m and Stratum 4, >15 m. Species of MOF were classified into: Stratum 1, <7 m; Stratum 2, 7 - 14.99 m; Stratum 3, 15 - 26 m and Stratum 4, >26 m. In MOF, photosynthetically active radiation (PAR) was 28.2 ± 3.46 µmol s^-1m^-2 (2.3% irradiance) in Stratum 1; 36.2 ± 24.3 µmol s^-1m^-2 (3.8% irradiance) in Stratum 2; 73.6 ± 22.8 µmol s^-1m^-2 (10% irradiance) in Stratum 3 and 744.3 ± 68.4 µmol s^-1m^-2 (100% irradiance) in Stratum 4 (canopy). In LLODF, PAR was 55.2 ± 25.8 µmol s^-1m^-2 (4.3% irradiance) in Stratum 1; 297.4 ± 56.1 µmol s^-1m^-2 (23% irradiance) in Stratum 2; 480.5 ± 91.1 µmol s^-1m^-2 (37.3% irradiance) in Stratum 3 and 1286.8 ± 79.9 µmol s^-1m^-2 (100% irradiance) in Stratum 4 (canopy).

The mean values for the distinct strata of each forest type were compared through One-way ANOVA followed by Tukey test. Leaf area and leaf thickness of homobaric and heterobaric leaves of each forest type were compared using t-test. Both analyses were performed on PAST software (Hammer et al. 2001Hammer O, Harper DAT, Ryan PD. 2001. PAST: Palaeontological statistics software package for education and data analysis. Palaeontologia Eletronica 4: 9. ). The independent distribution analysis of heterobaric leaves among forests and strata employed the χ² test (P < 0.05). Since MOF Stratum 4 included only one species, Araucaria angustifolia (Bertol.) Kuntze, it was excluded from this test, which aimed to verify the distribution of heterobaric leaves among plant families. The independent distribution analysis was performed using the RCMDR package (2, 1-7) for R program (version 3.1.2, R Foundation for Statistical computing, Vienna Austria).

Results

Of the 89 LLODF species studied, 22 (25%), belonging to 10 families, had heterobaric leaves (Fig.1A-B), while 67 species (75%) from 30 families had homobaric leaves (Fig.1C-D; Tab. 4). Out of the 58 MOF species studied, 16 (28%), belonging to 11 families, had heterobaric leaves, while 42 (72%) from 26 families had homobaric leaves (Fig. 1A-B; Tab. 4). The proportion of species with each leaf type (homobaric/heterobaric) did not differ between the studied forests (χ² test, P = 0.75, GL = 1, N = 146 species). For MOF, all heterobaric leaves had sclerenchymatous BSEs (Fig. 1B), except Ficus luschnathiana and Myrsine coriacea, which had parenchymatous BSEs. In LLODF, all heterobaric leaves had sclerenchymatous BSE, and Gomidesia schaueriana had incomplete BSE; in this species, BSE occurred only on the adaxial side of the lamina.

Figure 1
Surface and cross sections of homobric and heterobaric leaves. A. Surface of heterobaric leaf of Ocotea porosa, showing the division of the lamina in small areas by bundle sheath extension (BSE). B. Cross section of heterobaric leaf of Ocotea porosa, showing BSE. C. Surface of homobaric leaf of Lonchocarphus muehlbergianus, showing a homogeneous lamina. D. Cross section of homobaric leaf of Tibouchina sellowiana. Bars: A and C = 2 mm; B = 30 μm; D = 50 μm

Thumbnail

Table 4
Number and percentage of species with homobaric and heterobaric leaves by forest type and stratum. Legend: LLODF - Lowland Ombrophilous Dense Forest; MOF - Mixed Ombrophilous Forest.

The distribution of species with heterobaric leaves among forest strata differed significantly in LLODF (χ2 test, P=0.013, DF=3, N=89 species). The highest proportion of heterobaric leaves was found in Stratum 4 (Tab. 4), and the number of heterobaric leaves was directly proportional to light stratification. In MOF, despite the fact that heterobaric leaves were not significantly distributed among strata (χ2 test, P=0.0662, DF=3, N=57 species), an increase in heterobaric leaves was directly related to light intensity, with the highest proportion of heterobaric of leaves being in Stratum 3, since the frequency of heterobaric leaves was 0% in Stratum 4, which was composed of a single species (A. angustifolia) with only homobaric leaves. The lower strata had higher proportions of homobaric leaves in both forests (Tab. 4).

For all species considered in LLODF, leaf area did not differ among Strata 1, 2, and 3, but was higher in Stratum 4 (Tab. 5). When we excluded species with leaf area > 100 cm², [Ormosia arborea in Stratum 1; Aparisthmium cordatum and Cupania oblongifolia in Stratum 2; Miconia cabucu in Stratum 3 and Coccoloba warmingii in Stratum 4], the average leaf area of Stratum 4 differed from Strata 2 and 3. Although these species occur in small numbers in each stratum, they significantly affected average leaf area, as shown by the standard deviations (Tab. 5). In MOF, there was no variation in leaf area among lower strata; only Stratum 4 differed due to the reduced leaf area of A. angustifolia leaves (Tab. 5).

Thumbnail

Table 5
Average height, average values and respective standard deviations of leaf area and leaf thickness by stratum, leaf types and forest type. Legend: LLODF - Lowland Ombrophilous Dense Forest; MOF - Mixed Ombrophilous Forest. (*) Leaf area and leaf thickness averages with the exclusion of leaves > 100 cm², only in LLODF. Different letters in the same column, within the forest type, represent statistical difference, Tukey test (p<0.05).

In LLODF, leaf thickness did not exhibit the same pattern of variation among strata as leaf area. Only Stratum 3 differed by having thinner leaves than the other strata. When we excluded the species with leaf area > 100 cm², mean leaf thickness varied as follows: Stratum 1 = Stratum 2 > Stratum 3 > Stratum 4. In MOF, Stratum 4 had thicker leaves than the other strata (Tab. 5).

The comparison of homobaric and heterobaric leaves, independently of strata, indicates that homobaric leaves were thicker than heterobaric leaves in both forests types (LLODF - t test: t = 19.65, P < 0.001; MOF - t test t = 18.79, P < 0.001), when leaves > 100 cm² are excluded (Tab. 5).

The distribution of heterobaric leaves among some plant families was also evaluated (χ² test, P < 0.0001, GL = 7, N = 81 species from eight families with more than five species, Tab. S01 in supplementary material). In this study, all species of Lauraceae had heterobaric leaves, independently of strata (Fig. 2), except Endlicheria paniculata, which had heterobaric leaves in Stratum 1 at LLODF.

Besides Lauraceae, Euphorbiaceae, Fabaceae, Myrtaceae, Primulaceae, and Sapotaceae also had species with both leaf types, with heterobaric leaves being mainly distributed in Strata 2 and 3. No species of Aquifoliaceae and Melastomataceae, which occurred mainly in Strata 1 and 2, had heterobaric leaves.

Figure 2
Percentage of homobaric and heterobaric leaves among plant families with more than five species. Black bars represent homobaric leaves and grey bars represent heterobaric leaves.

Discussion

Both forest types exhibited similar proportions of species with homobaric and heterobaric leaves, with a greater occurrence of the former. Heterobaric leaves are generally associated with deciduous forests with cold or dry, well-defined seasons (Terashima 1992Terashima I. 1992. Anatomy of non-uniform leaf photosynthesis. Photosynthesis Research, 31: 195-212. doi: 10.1007/BF00035537.
https://doi.org/10.1007/BF00035537... ). On the other hand, homobaric leaves occur in evergreen forests, generally found in humid and hot regions (Kenzo et al. 2007Kenzo T, Ichie T, Watanabe Y, Hiromi T. 2007. Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. American Journal of Botany 94: 764-775.). Thus, our data corroborate a previous study that found a higher proportion of homobaric leaves in humid forests with high precipitation throughout the year (Kenzo et al. 2007Kenzo T, Ichie T, Watanabe Y, Hiromi T. 2007. Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. American Journal of Botany 94: 764-775.), such as our study sites. Although heterobaric leaves are associated with drier, deciduous forests, they are also present in humid forests, such as was found in our study sites. The distribution of these two types of leaves among strata in the present study was similar to that observed by Kenzo et al. (2007)Kenzo T, Ichie T, Watanabe Y, Hiromi T. 2007. Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. American Journal of Botany 94: 764-775. in a rain forest at Sarawak, Malasia.

The distribution analysis indicated that heterobaric leaves are more common in Strata 3 and 4 in MOF and LLODF, respectively, while homobaric leaves were more common in Strata 1 and 2. This distribution of homobaric and heterobaric leaves in different strata appears to be due to micro-environmental gradients associated with the various forest strata (Kenzo et al. 2007Kenzo T, Ichie T, Watanabe Y, Hiromi T. 2007. Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. American Journal of Botany 94: 764-775.). Such gradients include light availability, temperature, vapor pressure deficit, and wind (Théry 2001Théry M. 2001. Forest light and its influence in habitat selection. Plant Ecology 153: 251-261. ; Kitajima & Poorter 2010Kitajima K, Poorter L. 2010. Tissue-level leaf toughness, but not lamina thickness, predicts sapling leaf lifespan and shade tolerance of tropical tree species. New Phytologist 186: 708-721.; Bennett et al. 2015Bennett AC, McDowell NG, Allen CD, Anderson-Teixeira KJ. 2015. Larger trees suffer most during drought in forest worldwide. Nature Plants 1: 15139. doi:10.1038/nplants.2015.139.
https://doi.org/10.1038/nplants.2015.139... ; Inoue et al. 2015Inoue Y, Kenzo T, Tanaka-Oda A, Yoneyama A, Ichie T. 2015. Leaf water use in heterobaric and homobaric leafed canopy tree species in a Malaysian tropical rain forest. Photosynthetica 53: 177-186.). Of these, light availability is particularly important because it can influence the growth, survival, and subsequent reproduction of young individuals (Chazdon et al. 1996Chazdon RL, Pearcy RW, Lee DW, Fetcher N. 1996. Photosynthetic responses of tropical forests plants to contrasting light environments. In: Mulkey SS, Chazdon RL, Smith AP. (eds.) Tropical Forest Ecophysiology. New York, Chapman and Hall. p. 5-55.; Valladares & Niinemets 2008Valladares F, Niinemets Ü. 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution and Systematics 39: 237-257. ).

In the canopy, for example, plants are subjected to intense light and heat, which can be stressful during some periods of the day and/or year (Théry 2001Théry M. 2001. Forest light and its influence in habitat selection. Plant Ecology 153: 251-261. ; Valladares & Niinemets 2008Valladares F, Niinemets Ü. 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution and Systematics 39: 237-257. ). The presence of heterobaric leaves in the higher strata of a forest can be advantageous because sclerenchymatous BSEs can give additional mechanical support, due to the strength given by the sclerenchyma cells (Dickson 2000Dickson WC. 2000. Integrative plant anatomy. San Diego, Academic Press.; Cutler et al. 2008Cutler DF, Botha T, Stevenson DW. 2008. Plant Anatomy - an applied approach. Malden, Blackwell Publishing.), and help to maintain leaf shape and volume (Roth 1984Roth I. 1984. Stratification of tropical forests as seen in leaf structure. Tasks for vegetation Science. Vol. 6. Hague-Boston-Lancaster, Dr. W. Junk Publishing.), as well as protect against herbivores (Sack & Scoffoni 2013Sack L, Scoffoni C. 2013. Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New phytologist 198: 983-1000. ). Secondarily, BSEs can perform optic functions such as facilitating the dispersion of light within the compartments of the leaf (Karabourniotis et al. 2000Karabourniotis G, Bornman JF, Nikolopoulos D. 2000. A possible optical role of the bundle sheath extensions of the heterobaric leaves of Vitis vinifera and Quercus coccifera. Plant, Cell and Environment 23: 423-430.; Nikolopoulos et al. 2002Nikolopoulos D, Liakopoulos G, Drossopoulos I, Karabourniotis G. 2002. The relationship between anatomy and photosynthetic performance of heterobaric leaves. Plant Physiology 129: 235-243. ), thereby enhancing photosynthetic rate (Nikolopoulos et al. 2002Nikolopoulos D, Liakopoulos G, Drossopoulos I, Karabourniotis G. 2002. The relationship between anatomy and photosynthetic performance of heterobaric leaves. Plant Physiology 129: 235-243. ; Liakoura et al. 2009Liakoura V, Fotelli MN, Rennenberg H, Karabourniotis G. 2009. Should structure -function relations be considered separately for Homobaric vs. Heterobaric leaves? American Journal of Botany 96: 612-619.; Buckley et al. 2011Buckley TN, Sack L, Gilbert ME. 2011. The role of bundle sheath extensions and life form in stomatal responses to leaf water status. Plant Physiology 156: 962-973. ).

Plants restricted to lower strata, on the other hand, are subjected to low levels of heterogeneous light (Théry 2001Théry M. 2001. Forest light and its influence in habitat selection. Plant Ecology 153: 251-261. ; Kenzo et al. 2007Kenzo T, Ichie T, Watanabe Y, Hiromi T. 2007. Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. American Journal of Botany 94: 764-775.; Valladares & Niinemets 2008Turner IM. 1994. A quantitative analysis of leaf form in woody plants from the world's major broad leaved forest types. Journal of Biogeography 21: 413-419.). These conditions are beneficial to homobaric leaves with their well-developed spongy parenchyma (Fig. 1D), as observed in the studied species [spongy:palisade parenchyma ratio for MOF homobaric leaves (2.1 ± 0.9); for MOF heterobaric leaves (1.5 ± 0.6); for LLODF homobaric leaves (5.3 ± 3.2) and for LLODF heterobaric leaves (3.9 ± 1.7)]. A thicker spongy parenchyma is advantageous for capturing diffused light because the irregular-shaped cells reflect light rays within the mesophyll, thereby facilitating more efficient absorption (Vogelmann et al. 1996Vogelman TC, Nishio JN, Smith WK. 1996. Leaves and light capture: light propagation and gradients of carbon fixation within leaves. Trends Plant Science 1: 65-70. ). Homobaric leaves also increase the proportion of photosynthetic areas in the mesophyll (Terashima 1992Terashima I. 1992. Anatomy of non-uniform leaf photosynthesis. Photosynthesis Research, 31: 195-212. doi: 10.1007/BF00035537.
https://doi.org/10.1007/BF00035537... ), which may contribute to more efficient photosynthesis and water use (Pieruschka et al. 2006Pieruschka R, Schuur U, Jensen M, Wolff WF, Jahnke S. 2006. Lateral diffusion of CO2from shaded to illuminate leaf parts affects photosynthesis inside homobaric leaves. New Phytologist 169: 779-788. ; Pieruschka et al. 2010Pieruschka R, Chavarría-Krauser A, Schurr U, Jahnke S. 2010 Photosynthesis in lightfleck areas of homobaric and heterobaric leaves. Journal of Experimental Botany 61: 1031-1039. ; Lynch et al. 2012Lynch DJ, McInerney FA, Kouwenberg LL, Gonzalez-Meler MA. 2012. Plasticity in bundle sheath extensions of heterobaric leaves. American Journal of Botany 99: 1197-1206.) Thus, under limited light conditions, species with homobaric leaves perform better than those with heterobaric leaves (Kenzo et al. 2007Kenzo T, Ichie T, Watanabe Y, Hiromi T. 2007. Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. American Journal of Botany 94: 764-775.).

The distribution of species with homobaric and heterobaric leaves was weakly correlated with taxonomic group. Although Lauraceae is present in all strata of LLODF and in the first three strata of MOF, it is the only family that is represented by a larger number of heterobaric leaf species. All the species of the families Aquifoliaceae and Melastomataceae, which are commonly found in under-canopy strata, had homobaric leaves. Even though they comprise species with both leaf types, the families Euphorbiaceae, Myrtaceae, Primulaceae, and Sapindaceae did not show a distributional pattern related to strata. The one exception was Fabaceae, whose species with heterobaric leaves were present in Stratum 3 in MOF. These results indicate that the leaf types of each species are more dependent on habitat and/or life form type than phylogenetic relationships. Environmental filters have convergent effects and seem to favor functional diversity due the habitat heterogeneity, especially in tropical forest communities (Manel et al. 2014Manel S, Couvreur TLP, Munoz F, Couteron P, Hardy OJ. 2014. Characterizing the phylogenetic tree community structure of a protected tropical rain forest area in Cameroon. PLoS ONE 9(6): e98920. doi:10.1371/journal.pone.0098920
https://doi.org/10.1371/journal.pone.009... ).

In conclusion, the occurrence of homobaric and heterobaric leaves seems to be related to light stratification. The distribution of homobaric and heterobaric leaves in the different forest strata shows that light stratification acts as an ecological filter on the composition of the vegetation. Heterobaric leaves tend to occur in hotter strata that are more exposed to light, while homobaric leaves are more frequent in the under-canopy and more humid strata. This difference indicates that both leaf types occupy different positions on the "leaf economic spectrum", based on the balance between the cost of investiment in structural tissues and the investiment in photosynthetic tissues for carbon fixation via photosynthesis (sense Wright et al. 2004Wright IJ, Reich PB, Villar R. 2004. The worldwide leaf economics spectrum. Nature 428: 821-827. ).

Besides environmental influences, the occurrence of leaf types is weakly related to taxonomic group. Only Lauraceae included a large number of heterobaric species. These results show that these two leaf types (homobaric/heterobaric) are more dependent on habitat and/or life form than phylogenetic relationships. Environmental filters seem to shape functional diversity due to habitat heterogeneity, especially in tropical forest communities.

Acknowledgements

The authors are grateful to the "Coordenação de Aperfeiçoamento de Pessoal de Nível Superior" (CAPES) for scholarship to the co-authors and to the productivity fellowship to the first author (process nº 301971/2013-7).

References

Bennett AC, McDowell NG, Allen CD, Anderson-Teixeira KJ. 2015. Larger trees suffer most during drought in forest worldwide. Nature Plants 1: 15139. doi:10.1038/nplants.2015.139.
» https://doi.org/10.1038/nplants.2015.139
Boeger MRT, Alves LC, Negrelle RRB. 2004. Leaf morphology of 89 tree species from a lowland tropical rain forest (Atlantic forest) in South Brazil. Brazilian Archives of Biology and Technology 47: 933-943.
Buckley TN, Sack L, Gilbert ME. 2011. The role of bundle sheath extensions and life form in stomatal responses to leaf water status. Plant Physiology 156: 962-973.
Chazdon RL, Pearcy RW, Lee DW, Fetcher N. 1996. Photosynthetic responses of tropical forests plants to contrasting light environments. In: Mulkey SS, Chazdon RL, Smith AP. (eds.) Tropical Forest Ecophysiology. New York, Chapman and Hall. p. 5-55.
Cutler DF, Botha T, Stevenson DW. 2008. Plant Anatomy - an applied approach. Malden, Blackwell Publishing.
Dickson WC. 2000. Integrative plant anatomy. San Diego, Academic Press.
Hammer O, Harper DAT, Ryan PD. 2001. PAST: Palaeontological statistics software package for education and data analysis. Palaeontologia Eletronica 4: 9.
Inoue Y, Kenzo T, Tanaka-Oda A, Yoneyama A, Ichie T. 2015. Leaf water use in heterobaric and homobaric leafed canopy tree species in a Malaysian tropical rain forest. Photosynthetica 53: 177-186.
Karabourniotis G. 1998. Light-guiding function of foliar sclereids in the evergreen sclerophyll Phillyrea latifolia: a quantitative approach. Journal of Experimental Botany 49: 739-746.
Karabourniotis G, Bornman JF, Nikolopoulos D. 2000. A possible optical role of the bundle sheath extensions of the heterobaric leaves of Vitis vinifera and Quercus coccifera Plant, Cell and Environment 23: 423-430.
Kenzo T, Ichie T, Watanabe Y, Hiromi T. 2007. Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. American Journal of Botany 94: 764-775.
Kitajima K, Poorter L. 2010. Tissue-level leaf toughness, but not lamina thickness, predicts sapling leaf lifespan and shade tolerance of tropical tree species. New Phytologist 186: 708-721.
Liakoura V, Fotelli MN, Rennenberg H, Karabourniotis G. 2009. Should structure -function relations be considered separately for Homobaric vs. Heterobaric leaves? American Journal of Botany 96: 612-619.
Lynch DJ, McInerney FA, Kouwenberg LL, Gonzalez-Meler MA. 2012. Plasticity in bundle sheath extensions of heterobaric leaves. American Journal of Botany 99: 1197-1206.
Manel S, Couvreur TLP, Munoz F, Couteron P, Hardy OJ. 2014. Characterizing the phylogenetic tree community structure of a protected tropical rain forest area in Cameroon. PLoS ONE 9(6): e98920. doi:10.1371/journal.pone.0098920
» https://doi.org/10.1371/journal.pone.0098920
Niinements Ü. 2010. A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecological Research 25: 693-714.
Nikolopoulos D, Liakopoulos G, Drossopoulos I, Karabourniotis G. 2002. The relationship between anatomy and photosynthetic performance of heterobaric leaves. Plant Physiology 129: 235-243.
Pieruschka R, Schuur U, Jensen M, Wolff WF, Jahnke S. 2006. Lateral diffusion of CO₂from shaded to illuminate leaf parts affects photosynthesis inside homobaric leaves. New Phytologist 169: 779-788.
Pieruschka R, Chavarría-Krauser A, Schurr U, Jahnke S. 2010 Photosynthesis in lightfleck areas of homobaric and heterobaric leaves. Journal of Experimental Botany 61: 1031-1039.
Rhizopoulou S, Psaras G. 2003. Development and structure of drought-tolerant leavesof the Mediterranean shrub Capparis spinosa L. Annals of Botany 92: 377-383.
Roth I. 1984. Stratification of tropical forests as seen in leaf structure. Tasks for vegetation Science. Vol. 6. Hague-Boston-Lancaster, Dr. W. Junk Publishing.
Sack L, Scoffoni C. 2013. Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New phytologist 198: 983-1000.
Silveira TA, Boeger MRT, Maranho LT, Melo Jr. JCF, Soffiatti P. 2015. Functional leaf traits of 57 woody species of the Araucaria Forest, Southern Brazil. Brazilian Journal of Botany 38: 357-366.
Terashima I. 1992. Anatomy of non-uniform leaf photosynthesis. Photosynthesis Research, 31: 195-212. doi: 10.1007/BF00035537.
» https://doi.org/10.1007/BF00035537
Théry M. 2001. Forest light and its influence in habitat selection. Plant Ecology 153: 251-261.
Turner IM. 1994. A quantitative analysis of leaf form in woody plants from the world's major broad leaved forest types. Journal of Biogeography 21: 413-419.
Valladares F, Niinemets Ü. 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution and Systematics 39: 237-257.
Vogelman TC, Nishio JN, Smith WK. 1996. Leaves and light capture: light propagation and gradients of carbon fixation within leaves. Trends Plant Science 1: 65-70.
Wright IJ, Reich PB, Villar R. 2004. The worldwide leaf economics spectrum. Nature 428: 821-827.
Zwieniecki MA, Brodribb TJ, Holbrook NM. 2007. Hydraulic design of leaves: insights from rehydration kinetics. Plant Cell Environment 30: 910-921

Publication Dates

Publication in this collection
Apr-Jun 2016

History

Received
29 Feb 2016
Accepted
04 May 2016

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] Bennett AC, McDowell NG, Allen CD, Anderson-Teixeira KJ. 2015. Larger trees suffer most during drought in forest worldwide. Nature Plants 1: 15139. doi:10.1038/nplants.2015.139.
» https://doi.org/10.1038/nplants.2015.139

[2] Boeger MRT, Alves LC, Negrelle RRB. 2004. Leaf morphology of 89 tree species from a lowland tropical rain forest (Atlantic forest) in South Brazil. Brazilian Archives of Biology and Technology 47: 933-943.

[3] Buckley TN, Sack L, Gilbert ME. 2011. The role of bundle sheath extensions and life form in stomatal responses to leaf water status. Plant Physiology 156: 962-973.

[4] Chazdon RL, Pearcy RW, Lee DW, Fetcher N. 1996. Photosynthetic responses of tropical forests plants to contrasting light environments. In: Mulkey SS, Chazdon RL, Smith AP. (eds.) Tropical Forest Ecophysiology. New York, Chapman and Hall. p. 5-55.

[5] Cutler DF, Botha T, Stevenson DW. 2008. Plant Anatomy - an applied approach. Malden, Blackwell Publishing.

[6] Dickson WC. 2000. Integrative plant anatomy. San Diego, Academic Press.

[7] Hammer O, Harper DAT, Ryan PD. 2001. PAST: Palaeontological statistics software package for education and data analysis. Palaeontologia Eletronica 4: 9.

[8] Inoue Y, Kenzo T, Tanaka-Oda A, Yoneyama A, Ichie T. 2015. Leaf water use in heterobaric and homobaric leafed canopy tree species in a Malaysian tropical rain forest. Photosynthetica 53: 177-186.

[9] Karabourniotis G. 1998. Light-guiding function of foliar sclereids in the evergreen sclerophyll Phillyrea latifolia: a quantitative approach. Journal of Experimental Botany 49: 739-746.

[10] Karabourniotis G, Bornman JF, Nikolopoulos D. 2000. A possible optical role of the bundle sheath extensions of the heterobaric leaves of Vitis vinifera and Quercus coccifera Plant, Cell and Environment 23: 423-430.

[11] Kenzo T, Ichie T, Watanabe Y, Hiromi T. 2007. Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. American Journal of Botany 94: 764-775.

[12] Kitajima K, Poorter L. 2010. Tissue-level leaf toughness, but not lamina thickness, predicts sapling leaf lifespan and shade tolerance of tropical tree species. New Phytologist 186: 708-721.

[13] Liakoura V, Fotelli MN, Rennenberg H, Karabourniotis G. 2009. Should structure -function relations be considered separately for Homobaric vs. Heterobaric leaves? American Journal of Botany 96: 612-619.

[14] Lynch DJ, McInerney FA, Kouwenberg LL, Gonzalez-Meler MA. 2012. Plasticity in bundle sheath extensions of heterobaric leaves. American Journal of Botany 99: 1197-1206.

[15] Manel S, Couvreur TLP, Munoz F, Couteron P, Hardy OJ. 2014. Characterizing the phylogenetic tree community structure of a protected tropical rain forest area in Cameroon. PLoS ONE 9(6): e98920. doi:10.1371/journal.pone.0098920
» https://doi.org/10.1371/journal.pone.0098920

[16] Niinements Ü. 2010. A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecological Research 25: 693-714.

[17] Nikolopoulos D, Liakopoulos G, Drossopoulos I, Karabourniotis G. 2002. The relationship between anatomy and photosynthetic performance of heterobaric leaves. Plant Physiology 129: 235-243.

[18] Pieruschka R, Schuur U, Jensen M, Wolff WF, Jahnke S. 2006. Lateral diffusion of CO₂from shaded to illuminate leaf parts affects photosynthesis inside homobaric leaves. New Phytologist 169: 779-788.

[19] Pieruschka R, Chavarría-Krauser A, Schurr U, Jahnke S. 2010 Photosynthesis in lightfleck areas of homobaric and heterobaric leaves. Journal of Experimental Botany 61: 1031-1039.

[20] Rhizopoulou S, Psaras G. 2003. Development and structure of drought-tolerant leavesof the Mediterranean shrub Capparis spinosa L. Annals of Botany 92: 377-383.

[21] Roth I. 1984. Stratification of tropical forests as seen in leaf structure. Tasks for vegetation Science. Vol. 6. Hague-Boston-Lancaster, Dr. W. Junk Publishing.

[22] Sack L, Scoffoni C. 2013. Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New phytologist 198: 983-1000.

[23] Silveira TA, Boeger MRT, Maranho LT, Melo Jr. JCF, Soffiatti P. 2015. Functional leaf traits of 57 woody species of the Araucaria Forest, Southern Brazil. Brazilian Journal of Botany 38: 357-366.

[24] Terashima I. 1992. Anatomy of non-uniform leaf photosynthesis. Photosynthesis Research, 31: 195-212. doi: 10.1007/BF00035537.
» https://doi.org/10.1007/BF00035537

[25] Théry M. 2001. Forest light and its influence in habitat selection. Plant Ecology 153: 251-261.

[26] Turner IM. 1994. A quantitative analysis of leaf form in woody plants from the world's major broad leaved forest types. Journal of Biogeography 21: 413-419.

[27] Valladares F, Niinemets Ü. 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution and Systematics 39: 237-257.

[28] Vogelman TC, Nishio JN, Smith WK. 1996. Leaves and light capture: light propagation and gradients of carbon fixation within leaves. Trends Plant Science 1: 65-70.

[29] Wright IJ, Reich PB, Villar R. 2004. The worldwide leaf economics spectrum. Nature 428: 821-827.

[30] Zwieniecki MA, Brodribb TJ, Holbrook NM. 2007. Hydraulic design of leaves: insights from rehydration kinetics. Plant Cell Environment 30: 910-921

Feature	LLODF	MOF
Average moisture (%)	85	81
Annual precipitation (mm)	2170	1662
Soil type	Spodosol no hidromorphic. with moderate sandy texture and low concentrations of exchangeable cations.	Cambisoil humic aluminic and gleisolic typical clay soil.
Altitude (m)	9	947
Mean temperature (°C)	20.3	17.9
Climate type	Cfb	Cfb

Family	Species	Stratum	BSE
Anacardiaceae	Tapirira guianensis Aubl.	3	Absent
Annonaceae	Annona cacans E. Warming	4	Absent
	Guatteria australis A. St. Hil.	1	Absent
	Xylopia brasiliensis Spreng.	3	Present
Aquifoliaceae	Ilex dumosa Reissek	2	Absent
	Ilex integerrima Reissek	2	Absent
	Ilex pseudobuxus Reissek	2	Absent
	Ilex theezans Mart.	2	Absent
Araliaceae	Oreopanax capitatus Decne. & Planch.	2	Absent
Burseraceae	Protium kleinii Cuatrec.	2	Present
Calophyllaceae	Calophyllum brasiliense Cambess.	1	Absent
Celastraceae	Maytenus robusta Reissek	2	Absent
Clethraceae	Clethra scabra Pers.	3	Present
Clusiaceae	Clusia parviflora Engl.	2	Absent
	Garcinia gardneriana Planch. & Triana	1	Absent
Cunoniaceae	Weinmannia paulliniifolia Pohl ex Ser.	3	Absent
Elaeocarpaceae	Sloanea guianensis Benth.	2	Present
Erytroxilaceae	Erythroxylum vaccinifolium Mart.	1	Absent
Euphorbiaceae	Alchornea triplinervia Müll. Arg.	2	Present
	Aparisthmium cordatum (A. Juss.) Baill.	2	Absent
	Maprounea guianensis Aubl.	2	Absent
	Pera glabrata ex Baill.	2	Absent
Fabaceae	Andira anthelminthica Benth.	2	Present
	Copaifera trapezifolia Hayne	3	Absent
	Ormosia arborea Harms	1	Absent
	Pithecellobium langsdorffii Benth.	2	Absent
Lauraceae	Aiouea saligna Meisn.	3	Present
	Aniba firmula (Nees & Mart.) Mez	2	Present
	Endlicheria paniculata (Spreng.) J.F.Macbr.	1	Absent
	Nectandra grandiflora Nees & Mart.	2	Present
	Nectandra megapotamica Mez	3	Present
	Nectandra oppositifolia Nees & Mart.	4	Present
	Ocotea aciphylla Mez	2	Present
	Ocotea dispersa (Nees & Mart.) Mez	2	Present
	Ocotea elegans Mez	2	Present
	Ocotea glaziovii Mez	2	Present
	Ocotea odorifera (Vell.) Rohwer	2	Present
	Ocotea pulchella Mart.	2	Present
	Ocotea pulchra (Ekman & Schmidt) Alain	4	Present
Malpighiaceae	Byrsonima ligustrifolia A. Juss.	2	Absent
Melastomataceae	Miconia cabucu Hoehne	3	Absent
	Miconia cubatanensis Hoehne	1	Absent
	Miconia hymenonervia (Raddi) Cogn.	1	Absent
	Miconia sellowiana Naudin	1	Absent
	Mouriri chamissoana Cogn.	2	Absent
Meliaceae	Cabralea canjerana (Vell.) Mart.	1	Absent
Meliaceae	Guarea macrophylla Vahl	2	Absent
Monimiaceae	Mollinedia uleana Perkins	1	Absent
Myristicaceae	Virola oleifera (Schott) A.C.Sm.	2	Absent
Myrtaceae	Blepharocalyx salicifolius (Kunth.) O.Berg	2	Absent
	Calyptranthes concinna DC.	2	Absent
	Calyptranthes lucida Mart. ex DC.	1	Absent
	Campomanesia guaviroba (DC.) Kiaersk.	3	Present
	Eugenia cerasiflora Kurz.	2	Absent
	Eugenia obovata Wall. ex Duthie	2	Absent
	Eugenia subavenia O.Berg	3	Absent
	Eugenia tristis D.Legrand	1	Absent
	Eugenia umbelliflora O.Berg	2	Absent
	Gomidesia affinis (Cambess) D.Legrand	2	Absent
	Gomidesia schaueriana O.Berg	1	Present
	Marlierea eugeniopsoides (Kausel & D.Legrand) D.Legrand	1	Absent
	Marlierea reitzii D.Legrand	2	Absent
	Myrceugenia campestris (D.C.) D.Legrand & Kausel	2	Absent
	Myrceugenia reitzii D.Legrand & Kausel	2	Absent
	Myrcia acuminatissima Hieron.	2	Absent
	Myrcia fallax DC.	2	Present
	Psidium cattleyanum Sabine	3	Absent
Ochnaceae	Ouratea parviflora Engl.	1	Absent
Olacaceae	Heisteria silvianii Schwake	2	Absent
Olacaceae	Tetrastylidium grandifolium (Baill.) Sleumer	2	Absent
Pentaphylacaceae	Ternstroemia brasiliensis Cambess.	3	Absent
Phyllantaceae	Hieronyma alchorneoides Allem.	4	Present
Polygonaceae	Coccoloba warmingii Meisn.	4	Present
Primulaceae	Conomorpha peruviana A.DC.	1	Absent
	Rapanea ferruginea Mez	4	Absent
	Rapanea venosa Elmer	2	Absent
Rosaceae	Prunus sellowii Koehne	2	Absent
Rubiaceae	Amaioua guianensis Aubl.	2	Present
	Faramea marginata Mart.	1	Absent
	Rudgea villiflora K.Schum. ex Standl.	1	Absent
Rutacea	Esenbeckia grandiflora Mart.	1	Absent
Sapindaceae	Cupania oblongifolia Turcz.	2	Absent
	Matayba guianensis Aubl.	1	Absent
Sapotaceae	Manilkara subsericea (Mart.) Dubard	3	Absent
	Pouteria beaurepairei (Glaz. & Raunk) Baehni	2	Absent
	Pouteria venosa (Mart.) Baehni	2	Absent
Solanaceae	Solanum inaequale C. Presl	2	Absent
Styracaceae	Styrax glabratus Warb.	3	Absent
Winteraceae	Drimys brasiliensis Miers.	2	Absent

Family	Species	Stratum	BSE
Anacardinaceae	Lithraea molleoides (Vell.) Engl.	2	Absent
	Schinus terebinthifolius Raddi	2	Present
Aquifoliaceae	Ilex paraguariensis A.St.-Hil.	1	Absent
Araucariaceae	Araucaria angustifolia (Bertol.) Kuntze	4	Absent
Asteraceae	Gochnatia polymorpha (Less.) Cabrera	2	Present
Bignoniaceae	Jacaranda puberula Cham.	1	Absent
Canellaceae	Capsicodendron dinisii (Schwacke) Occhioni	3	Absent
Cannabaceae	Celtis iguanaea (Jacq.) Sarg.	1	Absent
Cardiopteridaceae	Citronella paniculata (Mart.) R.A.Howard	2	Absent
Celastraceae	Maytenus ilicifolia Mart. ex Reissek	1	Absent
Elaeocarpaceae	Sloanea monosperma Benth.	1	Present
Euphorbiaceae	Sebastiania brasiliensis Spreng.	1	Absent
	Sebastiania commersoniana (Baill.) L.B.Sm. & Downs	1	Absent
Fabaceae	Dalbergia brasiliensis Vogel	2	Absent
	Erythrina falcata Benth.	3	Present
	Inga marginata Willd.	2	Absent
	Lonchocarpus muehlbergianus Hassl.	3	Present
Lamiaceae	Vitex megapotamica (Spreng.) Moldenke	2	Present
Lauraceae	Nectandra megapotamica Mez	1	Present
	Ocotea porosa (Nees) Angely	3	Present
	Ocotea puberula Nees	2	Present
Lythraceae	Lafoensia pacari A.St.-Hil.	2	Absent
Malvaceae	Luehea divaricate Mart.	2	Present
Melastomataceae	Miconia sellowiana Naudin	1	Absent
	Tibouchina sellowiana Cogn.	1	Absent
Meliaceae	Cedrela fissilis Vell.	3	Present
Monimiaceae	Mollinedia clavigera Tul.	1	Absent
Moraceae	Ficus luschnathiana Miq.	2	Present
Myrtaceae	Calyptranthes concinna DC.	1	Absent
	Campomanesia guaviroba (DC.) Kiaersk	2	Present
	Campomanesia xanthocarpa O.Berg	2	Absent
	Eugenia pluriflora Mart.	2	Absent
	Eugenia pyriformis Cambess.	2	Present
	Eugenia uniflora O.Berg	2	Absent
	Myrceugenia miersiana (Gardner) D.Legrand & Kausel	1	Absent
	Myrcia cymoso-paniculata Kiaersk	3	Absent
	Myrcia hatschbachii D.Legrand	2	Absent
	Myrcia rostrata DC.	3	Present
	Psidium cattleyanum Sabine	1	Absent
Oleaceae	Chionanthus filiformis (Vell.) P.S.Green	3	Absent
Picramniaceae	Picramnia parvifolia Engl.	2	Absent
Piperaceae	Piper gaudichaudianum Kunth ex C.DC.	1	Absent
Podocarpaceae	Podocarpus lambertii Klotzsch ex Endl.	2	Absent
Primulaceae	Myrsine coriacea Nadeaud	1	Present
	Myrsine umbellate Mart.	1	Absent
Proteaceae	Roupala Montana Willd.	2	Absent
Rosaceae	Prunus brasiliensis Schott ex Spreng.	2	Absent
	Prunus sellowii Koehne	2	Absent
Salicaceae	Casearia decandra Jacq.	1	Absent
	Casearia sylvestris Sw.	1	Absent
Sapindaceae	Allophylus edulis Radlk. ex Warm.	2	Absent
	Allophylus guaraniticus Radlk.	2	Absent
	Cupania vernalis Cambess.	1	Absent
	Matayba elaeagnoides Radlk.	2	Present
Solanaceae	Solanum pseudoquina A.St.-Hil.	1	Absent
	Solanum sanctae-catharinae Dunal	2	Absent
	Solanum swartzianum Roem. & Schult.	2	Absent
Verbenaceae	Duranta vestita Cham.	3	Absent

Forest type	Stratum	Height (m)	Leaf area (cm²)	Leaf area *(cm²)	Leaf thickness (mm)	Leaf thickness (mm)*
LLODF	1 (<5m)	3.4 (1.4)	29.3 (25.1)b	23.1 (11.0)ab	0.31 (0.1)a	0.30 (0.1)a
	2 (5-9.9m)	7.5 (1.5)	30.5 (25.4)b	27.5 (19.6)a	0.32 (0.2)a	0.32 (0.2)a
	3 (10-14.9m)	11.7 (1.1)	35.3 (56.0)b	19.1 (11.2)b	0.23 (0.1)b	0.21 (0.1)b
	4 (> 15m)	16.3 (1.6)	81.5 (81.3)a	25.4 (30.1)a	0.31 (0.1)a	0.16 (0.1)c
Homobaric leaves	all	-	32.5 (35.6)a	15.0 (11.9)b	0.30 (0.15)a	0.31 (0.16)a
Heterobaric leaves	all	-	39.6 (46.3)a	19.6 (14.0)a	0.30 (0.12)a	0.29 (0.10)b
MOF	1 (<7 m)	5.2 (1.8)	14.7 (12.3)a		0.18 (0.1)b
	2 (7-14.9 m)	9.2 (3.3)	18.3 (13.4)a		0.19 (0.1)b
	3 (15-26 m)	12.7 (9.2)	16.2 (11.1)a		0.18 (0.0)b
	4 (>26 m)	30.1(12.0)	1.04(0.2)b		0.36 (0.07)a
Homobaric leaves	all	-	15.0 (11.9)a		0.20 (0.08)a
Heterobaric leaves	all	-	19.6 (14.1)a		0.15 (0.04)b

Brasil

Brasil

Occurrence of homobaric and heterobaric leaves in two forest types of southern Brazil

ABSTRACT

Introduction

Materials and methods

Results

Discussion

Acknowledgements

References

Publication Dates

History

Forest type	Stratum	Nº of species with heterobaric leaves	Nº of species with homobaric leaves	Total	Species with heterobaric leaves (%)
LLODF	1 (< 5m)	0	21	21	0
	2 (5.0-9.9m)	3	35	38	7.9
	3 (10-14.9m)	5	9	14	35.7
	4 (> 15m)	14	2	16	87.5
Total		22	67	89	25.0
MOF	1 (< 7m)	3	18	21	14.3
	2 (7 - 14.9m)	4	19	23	17.4
	3 (15 - 26m)	9	4	13	69.2
	4 (> 26m)	0	1	1	0
Total		16	42	58	28