Altitudinal gradient effect on morphometric variation and leaf symmetry of Platanus mexicana Moric

 

Efecto del gradiente altitudinal sobre la variación morfométrica y la simetría foliar de Platanus mexicana Moric

 

Dulce Ma. Galván-Hernández¹; J. Armando Lozada-García^2*; Norma Flores-Estévez¹; Jorge Galindo-González¹; S. Mario Vázquez-Torres³

 

¹ Instituto de Biotecnología y Ecología Aplicada (INBIOTECA), Universidad Veracruzana. Av. de las Culturas Veracruzanas núm. 101, col. Emiliano Zapata. C. P. 91090. Xalapa, Veracruz, MÉXICO.

² Facultad de Biología Xalapa, Universidad Veracruzana. Circuito Aguirre Beltrán s/n, Zona Universitaria. C. P. 91090. Xalapa, Veracruz, MÉXICO. Correo-e: alozada@uv.mx, Tel.: 01 (228) 8421748 (*Autor para correspondencia).

³ Centro de Investigaciones Tropicales, Universidad Veracruzana. Ex-hacienda Lucas Martín, privada de Araucarias s/n, col. Periodistas. C. P. 91019. Xalapa, Veracruz, MÉXICO.

Received: August 19, 2014.
Accepted: May 26, 2015.

 

ABSTRACT

Morphometric variation and leaf symmetry was characterized in a population of Platanus mexicana along a riparian altitudinal gradient in Veracruz. A total of eight morphometric characters were evaluated in 1,800 leaves from 15 trees per site, collected at 70, 200,600 and 1,700 m. Morphometric differences among sites (F_{(24, 5189)} = 21.1, P < 0.05) were determined using a discriminant function analysis. Characters related to length and width of leaves showed significant intrapopulation differences (P ≤ 0.05). Based on Mahalanobis distances, the site located at 70 m is the most distant morphometrically. Cluster analysis showed ten different leaf groups along the altitudinal gradient. Differences in leaf size were observed, the leaves are larger at 70 m and decrease with altitude. The index of leaf symmetry of P. mexicana showed no significant differences (P > 0.05) among sites in the altitudinal gradient of the Colipa river. The results determine the responsiveness of P. mexicana to the environmental heterogeneity along the altitudinal gradient of the Colipa river.

Keywords: Leaf differentiation, phenotypic plasticity, leaf groups, morphological adaptation.

 

RESUMEN

La variación morfométrica y simetría foliar de una población de Platanus mexicana se caracterizaron en un gradiente altitudinal ripario del estado de Veracruz. Ocho caracteres morfométricos se evaluaron en 1,800 hojas provenientes de 15 individuos por sitio (70, 200, 600 y 1,700 m de altitud). Las diferencias morfométricas entre sitios (F_{(24, 5189)} = 21.1, P < 0.05) se determinaron con un análisis de funciones discriminantes. Los caracteres relacionados con el largo y ancho de las hojas determinaron diferencias significativas (P ≤ 0.05) a nivel intrapoblacional. Con base en las distancias de Mahalanobis, el sitio ubicado a 70 m de altitud es el más distante morfométricamente. El análisis de conglomerados mostró 10 grupos foliares diferentes entre sí a lo largo del gradiente altitudinal. Existen diferencias en el tamaño foliar de mayor a menor altitud, indicando que hay hojas más grandes a 70 m. El índice de simetría foliar de P. mexicana no mostró diferencias significativas (P > 0.05) entre sitios del gradiente altitudinal del río Colipa. Los resultados fueron útiles para determinar la capacidad de respuesta de P. mexicana ante la heterogeneidad ambiental a lo largo del gradiente altitudinal del río Colipa.

Palabras clave: Diferenciación foliar, plasticidad fenotípica, grupos foliares, adaptación morfológica.

 

INTRODUCTION

Natural water flows promote changes in topography. On the sides of these flows we found vegetation areas known as gallery forests or riparian vegetation. This type of vegetation has environmental variations that are associated with the altitudinal gradients, having a dynamic and important ecosystem for the flow of energy and nutrients (Ward, Tockner, Arscott, & Claret, 2002). Platanus mexicana Moric is a dominant arboreal species from riparian forests in Veracruz. Usually, this species is found at altitudes of 600 to 1800 m; mainly at the Colipan river, P. mexicana has altitudinal distribution up to 70 m. This is rare, so maybe the conditions of altitudinal gradient on the river could influence the variation and adaptation of P. mexicana.

Altitudinal gradients, indirectly, lead to variations in plant organisms that are distributed along them. The plants have adaptations to their morphological attributes in response to changes in specific conditions of temperature, moisture, atmospheric pressure or solar incidence, among other abiotic aspects. Therefore, the organisms produce adaptive peaks to meet their requirements in an optimal manner (Körner, 2007). These adaptations or variations include physiological and morphological features, as a result of differential gene expression, or phenotypic plasticity (Cavieres, 2000; Luo, Zang, & Li, 2006; Watkins, Cardelu, Colwell, & Moran, 2006; Xu, Guo, Xu, & Wang, 2008). Altitudinal gradients have an effect on various aspects of plant morphology; the leaf is one of the organs with greater variation in response to the environment. The differences in temperature and moisture affect the diameter and size of the leaves, because they tend to be more narrow and small when temperature is high and moisture is low (Álvarez, Sánchez-González, & Granados, 2009; Sattarian, Reza, Zarafshar, Bruschi, & Fayyaz, 2011). Foliar comparisons have been useful in taxonomic classifications to determine both hybridization among species and morphological differences influenced by contrasting enviroments (Andrade, Mayo, Kirkup, & Van den Berg, 2008; Depypere, Chaerle, Breyne, Vander, & Goetghebeur, 2009; Xu et al., 2008; Álvarez et al., 2009).

There are certain elements that allow us to infer the degree of stability of a population, including the estimation of the bilateral symmetry (Moller & Shykoff, 1999). As altitudinal gradients are associated with environmental changes, leaf symmetry could be an indicator of stress due to variations in the index of symmetry reflect if environmental conditions are stable or unstable (Canché-Delgado, García-Jain, Vaca-Sánchez, & Cuevas-Reyes, 2011; Lorenzo, Mantuano, & Mantovani, 2010). For example, Hao and Xiangrong (2006) evaluated the leaf symmetry of the hybrid Platanus x acerifolia Aiton in contrasting environments and prove that leaves are indicators of environmental influence.

At present, is scarce the information on the morphological variation within populations of P. mexicana. Therefore, the aim of this study is to determine the morphometric variation and leaf symmetry in a wild population of P. mexicana, regarding the altitudinal gradient as a source of differentiation.

 

MATERIALS AND METHODS

Study species

Platanus mexicana is a deciduous tree commonly known as "beech". The P. mexicana is a monoecious wind-pollinated species with orthodox seed; with peltate and lobed leaves. This tree grows on the banks of streams and rivers in different types of vegetation such as deciduous forest, evergreen tropical forest, cloud forest and gallery forests. The species is distributed in central Mexico in the states of Hidalgo and Puebla, continuing into the Gulf of Mexico including Veracruz, Chiapas, Oaxaca and Guatemala (Nee, 1981).

Study area

The study was conducted in the Colipa river located northeast of the state of Veracruz, Mexico. Figure 1 shows the location of the four sites selected along the gradient (from highest to lowest altitude): 1,700 m at "Barranca del Maíz" Chiconquiaco (19° 47' 28'' N, 96° 48' 50'' W); 600 m at "Dos Caminos", Yecuatla (19° 49' 26'' N, 96° 47' 43'' W); 200 m at "rancho La Esmeralda", Yecuatla (19° 53' 15'' N, 96° 44' 57'' W); and 70 m at "rancho San Jerónimo" Colipa (19° 58' 36'' N, 96° 40' 58'' W). Table 1 shows the environmental conditions of each site.

Material collection and morphometric measurements

A total of 15 trees of P. mexicana were randomly selected in each study site; 30 leaves in good condition were collected from the first branch of each tree. Later, the leaves were pressed to be dried and measured (Hao & Xiangrong, 2006). A total of eight morphometric variables were recorded: leaf blade length (L), perpendicular maximum width of the axis of the midrib (W), perpendicular distance from the midrib to the right margin (y), perpendicular distance from the midrib to the left margin (x), distance to the right lateral vein into the main vein (WR), distance from the left side vein into the main vein (WL), length of the right side vein (SR) and length of the left side vein (SL) (Ellis et al, 2009;. Franiel & Wieski, 2005). Figure 2 shows these variables.

Leaf symmetry

Leaf symmetry was determined from the following variables: y, x, WR, WL, SR, SL, plus the angle the right secondary vain with respect to main vein (°D) and the angle of the left secondary vein with respect to the main vein (°I) (Figure 2b). The index of symmetry is calculated from the division of the variables on the right side of the leaf (y, °D, WR and SR) divided by the variables from the left side (x, °I, WL and SL). For each site, we calculated an overall average of these divisions with values close to the unit.

Multivariate analysis

Differences among sites were determined by an analysis of discriminating factors. The analysis was conducted using morphometric variables transformed by the natural logarithm in order to normalize them, which was corroborated by Kolmogorov-Smirnov tests. Later, a canonical correspondence analysis was conducted to define the change to a lower dimensionality. The roots resulting from the predictive model were analyzed by Chi-square test step by step to determine their contribution to the factorial model. Then, Mahalanobis distances were calculated to determine the similarity among sites and the effectiveness of the allocation model was tested. Moreover, an analysis of classification was conducted within the sites to determine a second level of variability through a hierarchical cluster analysis, after Bartlett sphericity test to ensure the relevance of the clusters; quadratic Euclidean distance was used as dissimilarity measure and the Ward's method as linkage algorithm. These clusters were compared by a second canonical analysis and maximum likelihood analysis was performed based on the Mahalanobis distances among groups to establish relationships within and among sites. The analyses were performed using the program STATISTICA v. 8.0 (StatSoft, 2011).

Analysis of symmetry

Average symmetry indices among sites were compared with the nonparametric Kruskal-Wallis test. In order to determine whether the symmetry indices differ from the unit (1 = symmetrical), we proceeded to perform a Two-tailed Student'st-test:

where:

x = Mean population expected

µ = Mean of the sample

σ = Standard deviation of the population

n = Total of components of the sample.

If the index of symmetry differs significantly from the unit (IS> 1), the leaves will be asymmetrical with predominance on the right side of the leaf; if there are no significant differences, the leaves will be symmetrical (IS = 1); and if the index is significantly lower than the unit (IS <1), the leaves will be asymmetrical, with predominance on the left side of the leaf. All analyzes were performed using the program STATISTICA v. 8.0 (StatSoft, 2011).

 

RESULTS AND DISCUSSION

In total 1,800 leaves of P. mexicana from Colipa river were analyzed. The results show significant differences among the leaves of the four sites of the altitudinal gradient (Lambda de Wilk: 0.76,(F_{(24, 5189)} = 21.1, P < 0.05). The length of the leaf (F = 40.6, P < 0.05), the length of the right side vein (F = 13.3, P < 0.05) and the perpendicular distance from the midrib to the left margin (F = 12.27, P < 0.05) had the highest variation to the model.

The canonical analysis identified the characteristics that most contributed to the order of the leaves. Table 2 shows that the first root account for 66 % of the variability and the second 22 %, which, together, account for 88 % of the morphometric variability of P. mexicana leaves. In the first canonical root, the variable length of the leaf blade (L) has greater contribution to the model, however, variables related to leaf width (WL and W) contribute to the second and third root. As in other species such as the genus Theobroma (Carvalho, Luiz, & Correa, 2012) and the African tree Vitellaria paradoxa C. F. Gaertn. (Gwali et al., 2012), measurements of width and length of the leaf allow to distinguish among populations and species or even may differ genotypes within the same region, as has been observed in Hibiscus sabdariffa L. (Alarcon & Legaria, 2013). However, even when the roots resulting from the canonical analysis are significant, not all variables have the same contribution to the model, therefore, with this analysis is not possible to differentiate P. mexicana leaves among altitude sites (Table 2). Evaluation of other variables is needed such as leaf area which may have greater contribution, since it has been observed that this variable along with the width and length of the leaf explain the differences among species of the genus Theobroma (Carvalho et al., 2012).

Analysis of allocation of each leaf to its respective site of origin was not significant (P = 0.25), since there is much variation within them. Leaves classified as belonging to the site of 200 m accounted for 36.2 %, at 600 and 1,700 m accounted for 41.1 % and finally at 70 m, 49.1 %. These values are low, a more appropriate allocation of 50 % is expected as in the case of the tree Parrotia persica C. A. Mey whose foliar ranking among populations is in the range of 70-100 % (Sattarian et al., 2011). The highest percentage of correct qualifying allocation is recorded at 70 m, which indicates greater homogeneity in leaf size at this altitude.

According to Table 3, Mahalanobis distances identified the gradient difficult areas are the most distant morphometrically. By relating this to the results of cluster analysis, the formation of different leaf groups (Table 4) is observed. At 70 to 200 m, the characteristics of the leaves were concentrated into three groups; however, at 600 and 1,700 m were grouped into two. Acosta- Hernández et al. (2011) assume this cluster formation as an indicator of morphometric variation in two populations of Juglans pyriformis Liebm, therefore, we may assume that P. mexicana is more variable morphometrically at sites with lower elevation of the gradient analyzed.

Figure 3 shows the result of the second discriminant analysis within the sites (among clusters), which identified morphometric differences in the population of P. mexicana (Lambda de Wilk: 0.19, F(_{72, 10840)} = 46.9, P < 0.05). Regarding the morphometric variables with the highest values in the four altitudes (L, W, SR and SL), Table 4 shows a trend of increase in leaf size from the highest to the lowest altitude. Figure 4 shows the maximum likelihood diagram which identified the relationship among clusters of each site; it is observed that the group of leaves collected at 70 m is farthest from other sites.

Leaf size differences are related to environmental variables such as temperature, precipitation and radiation (Álvarez et al., 2009; Richards, 1996; Xu, Guo, Xu, Wei & Wang, 2009). It has been observed that in species like Quercus laeta Liebm. and P. persica, the leaves tend to be more narrow and small due to increased temperature and low humidity (Alvarez et al, 2009; Sattarian et al., 2011), however, the width of the leaves of Q. acutissima Carruth varies with the solar incidence, being wider in places with low radiation (Xu et al., 2008). It has been shown that there is little variation of temperature and precipitation in the gradient analyzed (García, 1996; Vidal-Zepeda, 1990), so it is possible that radiation may be the cause of leaf morphometric variation observed in P. mexicana at the Colipa river. Moreover, differences among leaf groups of each altitudinal gradient suggests the presence of ecotypes. This has also been observed in Pinus hartwegii Lindl. whose morphological heterogeneity among populations represent particular phenotypic forms expressed by the interaction of genes with specific environments (Iglesias, Solís-Ramos, & Viveros-Viveros, 2012). It is possible that the change in size and width of the P. mexicana leaf involves both phenotypic plasticity and genetic diversity (Canché-Delgado et al., 2011; Uribe-Salas, Sáenz-Romero, González-Rodríguez, Téllez- Valdéz, & Oyama, 2008).

According to the nonparametric Kruskal-Wallis test, no significant differences in leaf symmetry among sites (H_{(3, N=1800)} = 2.32, P = 0.05) were observed. Also, according to Table 5, the Student t test was not significant (P > 0.05) between the index values for each site symmetry with respect to the unit; therefore, leaves of the population of P. mexicana are symmetrical. It was expected that in the river Colipa, the presence of trees below the altitudinal limit recorded for the species, would lead to differences in the index of symmetry among sites or altitudes. It is widely accepted that the environmental conditions in which a tree grows are important for its development and adaptation; however, many of these conditions can provoke stress (Palmer & Strobeck, 1997). In this study, the leaf symmetry is considered as an indicator that would infer if there was stress on the altitudinal gradient at the Colipa river. With no differences in the index of symmetry of P. mexicana along the altitudinal gradient, it follows that this species is highly responsive to environmental changes. This has also been observed in the species P. persica, whose plasticity tolerates environmental conditions that may be causing stress (Sattarian et al., 2011); however, it is necessary to consider other indicators mainly biochemical, molecular and physiological indicators.

 

CONCLUSIONS

Variables related to the length and width of leaves were crucial to differentiate and allocate foliar groups within the population of P. mexicana on the altitudinal gradient. This difference is evident in leaves collected at 70 m compared to the rest of the sites. The set of environmental interactions along the altitudinal gradient, encourage leaf morphometric variation. This variation may result from the responsiveness of P. mexicana to environmental variations and which results from genotypic differences among trees. At the Colipa river, P. mexicana leaves tend to be symmetrical without differences along the gradient. If we rely on the values of leaf symmetry we could rule out any stressful effect; however, it is important to consider other indicators assessing (biochemical, molecular or physiological) to corroborate this state, mainly at the site with smaller altitude at the Colipa river.

 

ACKNOWLEDGMENTS

We would like to thank Consejo Nacional de Ciencia y Tecnología the Program for the Improvement of Teaching (PROMEP in Spanish) for the support provided for this study; also thanks to Dr. Pablo Octavio Aguilar and Dr. Cristian Venegas for the advices to perform statistical analyzes; and thanks to Dr. Marco A. Espinoza for its contribution with environmental data.

 

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