Incomplete lateral anisophylly in Miconia and Leandra (Melastomataceae): inter- and intraspecific patterns of variation in leaf dimensions Author(s): Adriane Esquivel Muelbert, Isabela Galarda Varassin, Maria Regina Torres Boeger, and Renato Goldenberg Source: The Journal of the Torrey Botanical Society, 137(2):214-219. 2010. Published By: Torrey Botanical Society DOI: 10.3159/09-RA-063R.1 URL: http://www.bioone.org/doi/full/10.3159/09-RA-063R.1
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Journal of the Torrey Botanical Society 137(2–3), 2010, pp. 214–219
Incomplete lateral anisophylly in Miconia and Leandra (Melastomataceae): inter- and intraspecific patterns of variation in leaf dimensions Adriane Esquivel Muelbert1, Isabela Galarda Varassin, Maria Regina Torres Boeger, and Renato Goldenberg Departamento de Botaˆnica, Setor de Cieˆncias Biolo´gicas, Centro Polite´cnico, UFPR, Caixa Postal 19031, Jardim das Ame´ricas, Curitiba, PR, 81531-970, Brazil MUELBERT, A.E., I.G. VARASSIN, M.R. BOEGER and R. GOLDENBERG (Departamento de Botaˆnica, Setor de Cieˆncias Biolo´gicas, Centro Polite´cnico, UFPR, Caixa Postal 19031, Jardim das Ame´ricas, Curitiba, PR, 81531-970, Brazil). Incomplete lateral anisophylly in Miconia and Leandra (Melastomataceae): inter- and intraspecific patterns of variation in leaf dimensions. J. Torrey Bot. Soc. 137: 214–219. 2010.—Anisophylly can be defined as the unequal growth of two leaves in a pair from a single branch node. It occurs in several opposite-leafed taxa, even in those with apparently no phylogenetic proximity. We have intended here to classify and describe the anisophylly found in ten species of Melastomataceae from two genera, Leandra and Miconia, using morphometric data. We developed a method to quantify the level of anisophylly in these species, using a parameter called ‘‘Anisophylly Index’’ (AI), with values ranging from nearly 0 (isophyllous) to 1 (strongly anisophyllous). A comparison between the leaves from the erect and lateral branches of Leandra barbinervis showed that this species has incomplete lateral anisophylly; i.e., only the lateral branches are anisophyllous, and in these only the pairs positioned in a dorso-ventral position are unequal, while pairs positioned in a horizontal position are isophyllous. The lateral branches of all species showed incomplete anisophylly. There is no apparent relation between anisophylly levels and area of the leaves. Anisophylly seems to be related to an increase in the efficiency on light capture, and perhaps is controlled by auxins. Its occurrence does not imply a gain or a loss of photosynthetic area of the anisophyllous pair, when compared to the isophyllous pairs in the lateral branches because total leaf area is equal (Table 1). Since the incomplete lateral anisophylly found in Leandra and Miconia is a character whose expression may vary according to environmental conditions and also between different regions of the same plant, it can not be considered as a reliable taxonomic character. Key words: anisophylly, light capture, Melastomataceae, morphometry.
Anisophylly can be defined as the unequal growth of two leaves in a pair from a single branch node (Cremers 1995, Dengler 1999). It minimizes mutual shading of the leaves in one branch and at the same time maximizes light entrapment (Givnish 1984). Anisophylly occurs in several, non related groups of Angiosperms that have opposite leaves, like Gesneriaceae, Melastomataceae, Rubiaceae and Urticaceae (Givnish 1984, Dengler 1999). The Melastomataceae usually have opposite leaves, but some species have verticillate and a very few have pseudo-alternate ones. Anisophylly has been frequently described for some species of neotropical Clidemia and Maieta, with strongly unequal, opposite leaves (Wurdack 1980, Wurdack et al. 1993, Cremers 1995). Paleotropical Catanthera and Heteroblemma are also strongly anisophyllous, but the smaller leaf in each pair is caducous, 1 Author for correspondence: E-mail: adriane.
[email protected] Received for publication November 27, 2009, and in revised form March 16, 2010.
resulting in a pseudo-alternate phyllotaxys (Clausing & Renner 2001). These pseudoalternate leaves have been regarded as restricted to scandent species (Renner 1993), but it does occur in epiphytic/rupiculous Bertolonia (R.G., pers. obs.). Cremers (1995) described anisophylly in several genera of Melastomataceae (Clidemia, Loreya, Macrocentrum, Maieta, Miconia, Tococa) in French Guyana and proposed an anisophylly classification based on two categories plus subcategories, following two 19th century authors (J. Wiesner and K. Goebel). These categories are (1) habitual, or autonomous anisophylly, where the pairs from all branches in one plant are anisophyllous (reported for Bertolonia, Clidemia, Macrocentrum, Maieta and Miconia), and (2) lateral anisophylly, where only the lateral branches are anisophyllous. Lateral anisophylly could be complete, where all pairs are unequal (reported for some species of Tococa) or incomplete, where only the pairs positioned in a dorso-ventral position are unequal, while
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pairs positioned in a horizontal position are not anisophyllous (reported for Clidemia, Loreya and Miconia). Differences in the shape and area of the leaves in a pair may be facultative, as a response to environmental conditions (Cremers 1995, Dengler 1999), perhaps induced by gravity (Bilderback 1984, Cremers 1995, Dengler 1999). On the other hand, the anisophylly may be stable enough to be regarded as a taxonomic character in some taxa (Cremers, 1995, Dengler, 1999). For Melastomataceae, apart from the habitual anisophylly found in Maieta and Clidemia, it has been also used to distinguish species in genera where it is not so common like Miconia and Leandra. As an example, Cogniaux (1886–1888, 1891) distinguished the species that are part of the complex around Leandra carassana (DC.) Cogn. (Leandra dispar (Gardn.) Cogn, Leandra sublanata Cogn. and Leandra variabilis Raddi) by the unequal leaves in each pair. Nevertheless, this is not a good choice for a taxonomic character, since the plants in this complex apparently present incomplete lateral anisophylly, with lateral branches showing anisophyllous pairs alternating with isophyllous pairs (R.G., pers. obs.). We have intended here to classify and describe the anisophylly found in ten species of Melastomataceae from two genera, Leandra and Miconia. Since we found no numerical parameters in literature to evaluate anisophylly, we developed a method to quantify the level of anisophylly in these species using morphometric data. We also discuss the applicability of this character as taxonomic tool and the ecological implications of the anisophylly in tropical plants. Methods. Populations of ten species were studied in two localities, both covered with Tropical Rain Forest (‘‘Floresta Ombro´fila Densa’’, following the official Brazilian classification, Veloso et al. 1991). Leandra barbinervis Cham. Cogn., L. carassana DC., L. gracilis Cogn., Miconia cinerascens Miq., M. hyemalis Naudin, M. petropolitana Cogn., M. pusilliflora DC. Naudin and M. sellowiana Naudin were studied in the ‘‘Mananciais da Serra’’, an area protected by the ‘‘Companhia de Saneamento do Parana´’’ (SANEPAR) in the municipality of Piraquara, state of Parana´, approximately at 48u599W and 25u299S. Miconia cabucu Hoehne and M. latecrenata
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(DC.) Naudin were studied in a private area, owned by ‘‘Piscicultura Panama´’’, municipality of Paulo Lopes, state of Santa Catarina, approximately at 48u419W and 27u579S. Vouchers are available at the herbarium UPCB (Universidade Federal do Parana´). The first analysis was made only with Leandra barbinervis, in order to determine which of Cremer’s categories the anisophylly found in these Melastomataceae belongs (whether autonomous, lateral + complete or lateral + incomplete). We sampled 10 individuals, from which we compared the leaf pairs from one erect and one lateral branch (Fig. 1). From each one of these branches we measured three leaf pairs, avoiding those heavily damaged by herbivores and also immature ones. For the lateral branches, we noted each leaf’s position, whether ‘‘dorsal’’ or ‘‘ventral’’ in vertically oriented pairs, and whether ‘‘left’’ or ‘‘right’’ in horizontally oriented pairs. For the erect branches there was no distinction of the pairs as for orientation: all pairs and leaves were noted as ‘‘central’’. For each leaf we measured the blade’s length (BL) and width (BW). We estimated the blade area (BA) through the expression BA 5 p [(BL 3 BW)/ 2] (assuming that all the leaves are elliptic). We established a quantitative parameter, the ‘‘Anisophylly Index’’ (AI), estimated from the ratio between the difference and the sum of the blade area of two leaves in each pair. AI varies from 0 and 1, where values close to 0 indicate that the leaves in each pair have similar areas and values close to 1 indicate strong anisophylly. In order to compare the erect and the lateral branches, we compared the mean AI values for each one of the two groups, through the nonparametric Wilcoxon test (Zar 1998), after arcsin tranformation. In order to verify if there is any difference in leaf area between isophyllous and anisophyllous leaf pairs, we summed BA values for both leaves in each kind of leaf pair (central, horizontal and vertical). The differences between the mean values were tested through ANOVA, followed by Tukey after log transformation (Zar 1998). For the other species we did not measure the erect branches, since they follow the same pattern of Leandra barbinervis. We sampled three individuals under similar light conditions from each species, from which we selected three lateral branches. Each one of these lateral branches had all leaf pairs measured from the apex to the base, until reaching its
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Table 1. Sum of blade area (SBA) of central, horizontal and vertical leaf pairs and Anisophylly Index (AI) in Leandra barbinervis. Mean values (standard deviation). Branches and leaf pairs position, sum of blade area and Anisophylly Index. SBA (cm)
Erect branches Central leaf pair Lateral branches Horizontally oriented leaf pairs Vertically oriented leaf pairs Significance tests
300.5 (6 237.75) 213.9 (6 168.4) 197.6 (6 156.6) F2 5 4.68, q 5 2.37, P , 0.05
first branching. The measurements taken from the leaves were the same as described above for L. barbinervis, as well as the leaf area and anisophylly index estimates. The occurrence of anisophylly was tested either through Wilcoxon’s test (Zar 1998) for Miconia cabucu, or through Student’s t-test (Zar 1998) for L. carassana, L. gracilis, M. cinerascens, M. hyemalis, M. latecrenata, M. petropolitana, M. pusiliflora, and M. sellowiana. The difference between the total leaf areas of the horizontal and vertical pairs was investigated as described above for L. barbinervis, except for the test, since we used Student’s t (Zar 1998) instead of Tukey. Since leaf area varies among the species, we determined if the occurrence of anisophylly is related to the area of the leaf. Do species with larger leaves have a higher anisophylly than those with smaller leaves? The AI values found for the vertical pairs for each species were plotted against three morphometric parameters that represent the species leaf size: mean
AI
0.09 (6 0.07) 0.10 (6 0.10) 0.40 (6 0.17) U2 5 93.27, P , 0.05
values of (1) the lateral leaves blade’s length, (2) the ventral leaves blade’s length, (3) the sum of the leaf areas of the vertical pairs. Results. Vertically oriented leaf pairs from lateral branches of Leandra barbinervis had greater anisophylly (AI 5 0.40) than leafs from horizontally oriented pairs from lateral branches (AI 5 0.10) or leaves from erect branches (AI 5 0.09, U2 5 93.2719, P , 0.05, Table 1). The anisophylly in the vertical pairs is associated neither with loss nor a gain of leaf area. There is no difference in BA of anisophyllous vertical pairs of leaves compared to the horizontal pairs (Table 1). Nevertheless, the leaf area of the central pairs (from the erect branches) is significantly larger than both pair types from lateral branches (F2, 163 5 4.68, q 5 2.37, P , 0.05, Table 1, Fig. 2). All the other species except Miconia sellowiana, showed higher AI values for the vertical than for the horizontal pairs (Table 2).
FIG. 1. Central (1) and Lateral (2) branches of Leandra barbinervis. The lateral branches (2) have either vertical anisophyllous pairs with dorsal (A) and ventral (C) leaves, or horizontal pairs (B) with isophyllous leaves.
FIG. 2. Mean values of blade area (after log transformation) in central, horizontal and vertical pairs of leaves of Leandra barbinervis.
For all species, the ventral leaves always showed higher BA mean values than the dorsal ones (Table 2). The leaves on the horizontal pairs always showed intermediate BA values between the dorsal and ventral leaves from the vertical pairs (Table 2). As for Leandra barbinervis, we found neither gain nor loss in the vertical pairs leaf area when comparing to the horizontal ones of most species. The exceptions were M. latecrenata and M. pusilliflora, where the isophyllous pairs had an area significantly larger than the anisophyllous pairs (Table 2). Leaf area does not influence the degree of anisophylly, since there is no relation between AI values from each species and the size of its leaves, whether considering the lateral leaves mean value of BL (r2 5 0.1068, F 5 0.1319, GL 5 1, P . 0.05), the ventral leaves mean BL (r2 5 0.1039, F 5 0.1526, P . 0.05), the sum of the leaf areas of the vertical pairs (r2 5 20.0043, F 5 0.1459, GL 5 1. 200, P . 0.05).
Discussion. The anisophylly in Leandra barbinervis is lateral and incomplete. It is restricted to lateral branches and found only in vertically positioned leaf pairs (Cremers 1995). Anisophylly occurs in all the species studied here, and it is frequent among Leandra and Miconia. Plants from tropical rain forests located at the canopy or undercanopy are subject to a limited light supply, which can be drastically reduced inside the forest to 2–5% of the total incident radiation (Larcher 2000). Moreover, the quality of the light under these conditions is very heterogeneous (Pearcy 2007), which induces the species to adjust
Leandra Leandra Leandra Miconia Miconia Miconia Miconia Miconia Miconia Miconia
barbinervis carassana gracilis cabucu cinerascens latecrenata petropolitana hyemalis pusilliflora sellowiana
Species
132.4 62.7 44.9 458.3 44.1 41.5 9.4 25.3 29.2 3.5
(6 (6 (6 (6 (6 (6 (6 (6 (6 (6
(6 (6 (6 (6 (6 (6 (6 (6 (6 (6
(6 (6 (6 (6 (6 (6 (6 (6 (6 (6
(6 (6 (6 (6 (6 (6 (6 (6 (6 (6
156.6) 25.5) 18.5) 204.7) 18.7) 19.8) 10.2) 9.5) 11.0) 3.6)
SvBA (cm2)
84.8) 197.6 16.8) 93.7 9) 69.9 149.7) 696.4 12.5) 68.9 12.3) 65.2 4.5) 13.8 6) 38.5 9.2) 42.6 1.8) 5,4
LBA (cm2)
57.8) 106.9 12.7) 52.1 10.5) 34.2 72.2) 403.9 8.3) 39.7 7.6) 44.3 3.3) 7.8 4) 19.7 5.2) 26.6 1.6) 2.7
dBA (cm2)
104.1) 65.16 16.1) 31 11.1) 24.9 139) 238.2 12.7) 24.8 14.6) 23.5 7) 4.7 7) 13.2 7.1) 13.4 2.1) 2
vBA (cm2)
213.9 104.3 68.4 807.7 79.4 88 15.8 39.4 53.2 5.5
(6 (6 (6 (6 (6 (6 (6 (6 (6 (6
168.4) 31) 16.5) 257.9) 23.9) 22.4) 8.7) 11.3) 15) 3.3)
ShBA (cm2)
t125 t29 t44 t28 t32 t25 t28 t26 t26 t30
5 5 5 5 5 5 5 5 5 5
0.56 1.02 0.29 1.27 0.40 2.66* 0.55 0.21 2.13* 0.003
SBA t ests
0.40 0.35 0.31 0.31 0.28 0.29 0.36 0.32 0.38 0.33
(6 (6 (6 (6 (6 (6 (6 (6 (6 (6
vAI
0.17) 0.15) 0.06) 0.07) 0.12) 0.15) 0.12) 0.13) 0.13) 0.19)
Species of Miconia and Leandra, mean values, standard derivation and tests of Blade area and Anisophylly index.
0.10 0.11 0.09 0.13 0.12 0.10 0.08 0.08 0.19 0.26
(6 (6 (6 (6 (6 (6 (6 (6 (6 (6
hAI
0.10) 0.07) 0.17) 0.10) 0.11) 0.06) 0.08) 0.06) 0.10) 0.16)
29
96
5 5 t24 5 U1 5 t 29 5 t25 5 t28 5 t16 5 t 26 5 t 29 5
t t
12.07* 5.83* 5.51* 14.98* 3.97* 4.14* 7.23* 5.88* 4.43* 0.77
AI tests
Table 2. Mean values, standard deviation and tests of Blade area and Anisophylly index. Ventral (vBA), dorsal (dBA), and lateral blade area (lBA), sum of vertical (SvBA) and horizontal blade area (ShBA), t test among SvBA and ShBA (SBA test), Anisophylly Index for vertically oriented pair of leaves, (AIv) and horizontally oriented pair of leaves (AIh), t- or Wilcoxon test among AIv and AIh (AI tests) and among DPv and DPh (DP tests). Mean values (standard deviation). * Significant results (P , 0.05).
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their foliar architecture, in order to improve light capture (Givnish 1984). Among several leaf architectural features, the phyllotaxis is one that is directly related to light capture (Valladares & Brites 2004). Opposite, decussate phyllotaxis seems to be less advantageous, since it enhances self-shading due to the overlapping of the leaves (Ga´lvez & Pearcy 2003). The same authors reported that light capture in plants with opposite leaves is 55% less efficient than in others with alternate leaves, which in turn improves energy costs, in terms of carbon assimilation. The anisophylly found in Leandra and Miconia reduces this self-shading effect, and enhances light capture efficiency in groups that have this type of phyllotaxis (Givnish 1984, Falster & Westoby 2003). Nevertheless, the asymmetrical distribution of the leaf area allows the plant to avoid self-shading, at least when related to the vertical orientation of the leaves. Moreover, the anisophylly is related to an adjustment of several features, such as shape and area of the blade. These features are related to the optimization of light capture and improvement of carbon assimilation through photosynthesis (Ali & Kikuzawa 2005). Anisophylly can be regarded as an adaptation for decreasing self-shading and to a more efficient biomass allocation when the plants are subject to some degree of shading (Ali & Kikuzawa 2005). The area reduction of one of the leaves in a pair could be regarded, at first sight, as a loss in the total leaf photosynthesizing area, but this does not occur in the species studied here, since there is a compensation by the larger ventral leaf resulting in an equal total blade area available in both horizontal and vertical leaf pairs Mechanisms inducing incomplete lateral anisophylly may be related to the auxins negative phototropism. Plant growth regulators like the auxins can affect foliar expansion (Sa´nchez-Burgos and Dengler 1988). Larger concentrations of auxins in shaded regions may cause cell expansion, which in turn can promote asymmetrical cell growth, as well as the production of ethylene, that obstructs the transversal transport of the auxins to the lightpoor side (Awad 1992). Although we have not tested for auxins in Leandra and Miconia, we suggest that there may be a higher concentration of auxins in the lower side of the vertical pairs, which in turn would induce more growth of the leaf at the ventral position. On
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the other hand, in the horizontal pairs there would be no difference among the concentrations of the auxins, and therefore they would be isophyllous. Although anisophylly is frequent among these genera, it is not a reliable taxonomic character, since it varies throughout the plant body. That is the case of the species complex around Leandra carassana (cited in the introduction), whose species are in part recognized by the occurrence of anisophylly (Cogniaux 1886–1888, 1891). This kind of confusion is more frequent among large-leafed plants, since a single herbarium sheet can sometimes fit only one pair of leaves, whereas exsicatae of small-leafed materials bear several pairs that clearly show the variation among the pairs. Nevertheless, there is no apparent relationship between the intensity and frequency of anisophylly and the leaf size, as showed by our data. Another aspect that limits the anisophylly as a taxonomic character is that its expression can vary according to environmental conditions (Givnish 1988), since the physiology and resources allocated depend on the amount and quality of light that the plants receive. Literature Cited ALI, M. S. AND K. KIKUZAWA. 2005. Shoot morphology of Aucuba japoˆnica incurred by anisophylly: ecological implications. J. Plant. Res. 118: 329–338. AWAD, M. AND P. R. C. CASTRO. 1992. Introduc¸a˜o a` Fisiologia Vegetal. Nobel. Sa˜o Paulo –SP. 177 p. BILDERBACK, D. E. 1984. Phototropism of Selaginella: The Differential Response to Light Am. J. Bot. 71: 1323–1329. CLAUSING, G. AND S. RENNER. 2001. Evolution of growth form in epiphytic Dissochaeteae (Melastomataceae). Org. Divers. Evol. 1: 45–60. COGNIAUX, A. 1886–1888. Melastomataceae, p. 1– 626. In C. F. P. Martius, A. G. Eichler, and I. Urban [eds.], Flora Brasiliensis. XIV. 3–4. Frid. Fleischer, Mu ¨ nchen, Vienna and Leipzig, Austria. COGNIAUX, A. 1891. Melastomataceae, p. 1–1256. In A. de Candolle and C. de Candolle [eds.], Monographie Phanerogamarum. XII G Masson, Paris, France. CREMERS, G. 1995. Connections between anisophylly and vegetative architecture from some Melastomaceae: Their taxonomic value. Acta Botanica Gallica 142: 183–190. DENGLER, N. G. 1999. Anisophylly and dorsiventral shoot symmetry. Int. J. Plant. Sci. 160: 67–80. FALSTER, D. S. AND M. WESTOBY. 2003. Leaf size and angle vary widely across species: what consequences for light interception? New Phytologist 158: 509–525. GA´LVEZ, D. AND R. W. PEARCY. 2003. Petiole twisting in the crows of Psychotria limonensis:
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