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Revista Chapingo serie ciencias forestales y del ambiente
versão On-line ISSN 2007-4018versão impressa ISSN 2007-3828
Rev. Chapingo ser. cienc. for. ambient vol.21 no.3 Chapingo Set./Dez. 2015
https://doi.org/10.5154/r.rchscfa.2015.01.001
Fragmentation effect in the leaf morphometry and environment of Quercus germana Schldl. & Cham. (Fagaceae) in Xalapa, Veracruz
Efecto de la fragmentación en la morfometría foliar y el ambiente de Quercus germana Schldl. & Cham. (Fagaceae) en Xalapa, Veracruz
Anantli Martínez-Munguía1*; Gustavo C. Ortiz-Ceballos2; Virginia Rebolledo-Camacho3; Antonio Andrade-Torres1; Lourdes G. Iglesias-Andreu1; Pablo Octavio-Aguilar4
1 Instituto de Biotecnología y Ecología Aplicada (INBIOTECA), Universidad Veracruzana. Campus para la Cultura, las Artes y el Deporte. Av. de las Culturas Veracruzanas núm. 101, col. Emiliano Zapata. C. P. 91090. Xalapa, Veracruz, MÉXICO. Correo-e: ing.anantli@gmail.com Tel.: (228) 842 27 73 (*Autora para correspondencia).
2 Facultad de Ciencias Agrícolas, Universidad Veracruzana. Circuito Gonzalo Aguirre Beltrán s/n, zona Universidad Veracruzana. C. P. 91090. Xalapa, Veracruz, MÉXICO.
3 Instituto de Investigaciones Forestales (INIFOR), Universidad Veracruzana. Parque Ecológico El Haya, camino antiguo a Zoncuantla s/n, col. Benito Juárez. C. P. 91070. Xalapa, Veracruz, MÉXICO.
4 Instituto de Ciencias Básicas e Ingeniería (ICBI), Universidad Autónoma del Estado de Hidalgo. Carretera Pachuca-Tulancingo km 4.5. C. P. 42184. Mineral de la Reforma, Hidalgo, MÉXICO.
Received: January 28, 2015.
Accepted: July 8, 2015.
ABSTRACT
Quercus germana is an endemic species from the cloud forest of Mexico. The selection pressure resulting from fragmentation and environmental changes suggests the presence of phenotypic differentiation. We evaluated the relationship between the environment and the leaf morphology of Q. germana at six sites in the area of Xalapa, Veracruz. Ten leafs of 30 specimens per site were collected. Ten leafs morphometric and seven environmental characteristics were measured and variance analyses were performed with a discriminant analysis. Additionally, UPGMA phylogenetic trees were constructed and the Mahalanobis distances were compared using a Mantel test to estimate the relationship between morphometry and the environment. The morphological variables that best separated the sites were mucrones, ribs and petiole size. Environmentally, the most discriminant variables were light, temperature and loss of humidity. The Mantel test did not show any relationship between the morphometric and the environmental differences (r = 0.090, P = 0.3060), so there is not any association between the two. Because morphological differences were found in sub-populations despite of the short distance between them, these may be affected by fragmentation even without environmental influences.
Keywords: Endemic species, phenotypic differentiation, environmental variables, morphological variation.
RESUMEN
Quercus germana es una especie endémica del bosque mesófilo de montaña de México. La presión de selección que la fragmentación y los cambios ambientales ejercen, sugieren diferenciación fenotípica. Por lo anterior, la relación de la diferenciación foliar de Q. germana con la fragmentación y las condiciones ambientales se evaluó en seis sitios del bosque mesófilo de Xalapa, Veracruz. Para ello, se colectaron 10 hojas de las ramas nones de 30 individuos por sitio; se midieron 10 características morfométricas foliares y siete ambientales. Los análisis de varianza se realizaron con el modelo linear generalizado; se utilizó un análisis discriminante, se construyeron árboles de ligamiento UPGMA y se proyectaron las poblaciones tridimensionalmente. Las distancias de Mahalanobis se compararon con una prueba de Mantel para estimar la relación morfométrica y ambiental. Las variables morfológicas que mejor separan los sitios son mucrones, nervaduras y tamaño del peciolo. Ambientalmente, las variables más discriminantes son luz, temperatura y pérdida de humedad. La prueba de Mantel no mostró relación entre las diferencias morfométricas y ambientales (r = 0.090, P = 0.306). Las subpoblaciones de Q. germana son morfológicamente diferentes a pesar de la distancia corta que las separa, lo cual indica que posiblemente son afectadas por la fragmentación aún sin influencia ambiental.
Palabras clave: Especie endémica, diferenciación fenotípica, variables ambientales, variación morfológica.
INTRODUCTION
The species of Quercus present morphological changes as a response to variation in the environmental conditions of the locations where they grow (Cardillo & Bernal, 2006; Li, Zhang, Liu, Luukkanen, & Berninger 2006; Sack, Melcher, Liu, Middleton, & Pardee, 2006). The genus Quercus is considered as having a high phenotypic plasticity and a large part of its phenotypic variation is associated with intrinsic biological characteristics such as long life cycles, wind pollination, crossing-over and hybridization (González-Rodríguez & Oyama, 2005; Tovar-Sánchez & Oyama, 2004). The morphological variation of the Quercus leaves is of high interest due to the fact that several species have been subjected to high local selection pressure, which has caused the differentiation between populations and individual subjects (González-Rodríguez & Oyama, 2005; Tovar-Sánches & Oyama, 2004; Sack et al., 2006). Leaves are the main photosynthetic organ of plants, which makes them highly sensitive to the changes in light (Álvarez, Sánchez-González, & Granados-Sánchez, 2009; Halloy & Mark, 1996), phenological cycles, growth rates (González-Rodríguez & Oyama, 2005; Nikolic, Krstic, Pajevic & Orlovic, 2006), time of the year and position of the leaf in the tree (Ponton, Dupoguey & Dreyer, 2004). In addition to the intrinsic biological characteristics of the tree, there is a genetic factor that explains the foliar plasticity by adaptive differential expression, which is a characteristic of the genus (González-Rodríguez & Oyama, 2005). The differential genetic expression, along with the evolutionary forces and the history of each population, is strengthened when the vegetation is fragmented. It has been suggested that there is a fragmentation effect in the differentiation because a relation has been found between the reduction of size of the foliar layer with the typical characteristics of fragmented environments such as: a rise in temperature, incidence of solar light, and decrease in humidity and nutrients (Borazan & Babac, 2003; Williams-Linera, 2002). This is why the studies on foliar plasticity contribute to the generation of information about the extent in which the population differentiation of Quercus has grown (González-Rodríguez & Oyama, 2005; Tovar-Sánchez & Oyama, 2004).
The differentiation among populations is closely related to fragmentation. It has been reported that on fragmented environments the gene flow in Q macrocarpa Michx., Q rubra L. (Dow & Ashley, 1998) and Q humboldtti Bonpl. (Fernández-M. & Sork, 2007) is substantially reduced, even within distances shorter than 100 m, which increases the level of population structure. The response of this structure to fragmentation events has been assessed in established differentiation zones based on the variation of foliar attributes (Sáenz-Romero, Snively, & Linding-Cisneros, 2003), due to the fact that at least one part of the phenotypic variation is related to the genetic adaptive variation (Hovenden & Vander, 2006; Warren, Tausz, & Adams, 2005).
In the last 50 years, the cloud mountain forest (CMF) has had the most structural and environmental changes due to fragmentation (Williams-Linera, 2002). This forest is important due to its high level of endemism, even though it only represents 1 % of the national area (Williams-Linera, 2002). White Oak Quercus germana Schdl. & Cham. is an endemic species of the CMF with great foliar variation, which makes it ideal to explore the effect in the changes of the environmental conditions as a result of fragmentation. Several studies on differentiation in some species of Quercus have been made in order to evaluate foliar variation, determining that the changes among populations are directly proportional to the environmental differences (Álvarez et al., 2009; González-Rodríguez & Oyama, 2005; Ponton et al., 2004; Tovar-Sánchez & Oyama, 2004). Even though environmental changes can be the result of fragmentation, the environment does not always determine the morphological changes as it has been shown in populations of Q robur L., where the variation of the foliar characteristics is attributed to interruptions in the gene flow without the presence of environmental differences (Nikolic et al., 2006). Due to the foregoing, it is probable that the morphological differentiation could be attributed both to the environment and to interruptions in the gene flow; both situations are present in fragmentation events.
The foliar characters of Quercus with more intra variation and populational variation in the presence of environmental changes are the size of the petiole and the length and width of the foliar layer. The sensitivity of these characters is due to the fact that the big leaves and the long petioles keep the leaves separated among themselves, facilitating the collection of light (González-Rodríguez & Oyama, 2005; Ponton et al., 2004; Tovar-Sánchez & Oyama, 2004). Therefore, the environmental changes included originated by fragmentations may have an effect on the variation of these characteristics of the leaves. In particular, the leaves of Q. germana present asymmetry in the distance between the midrib and the right and left borders, so the angle of insertion and the number of ribs should also be included, as it has been done with asymmetrical species such as Q laeta Liebm (Alvarez et al., 2009). Even though some studies of environmental variations do not include the number of mucrones of the leaf margin, works such as that of Alvarez et al. (2009) do report a relation between the mucrones and the size of the Q. laeta leaf.
This study compares the foliar morphological variation of Q. germana among residual sub-populations and evaluates the relation of the foliar differentiation with fragmentation and environmental conditions. The subjects studied were part of one population, so the term "sub-populations" shall be used to refer to them as it has been done in other studies that explore differentiation (Excoffier, 2001; Williams-Linera, 2002). Based on what has already been mentioned, it is expected that the leaves of the sub-populations of Q. germana present foliar variation derived from the process of local adaptation by phenotypic/genotypic selection (Bacilieri, Ducousso, & Kremer, 1995), strengthened by fragmentation events. Similarly, it is possible to find morphological differences among the locations, associated to environmental changes. If there is no evidence of foliar differentiation, then it means that fragmentation is so recent that it is not yet reflected, or that species is resilient to fragmentation.
MATERIALS AND METHODS
Field of study
The field of study is located in fragments of the cloud forest located along the Sierra Madre Oriental in the area surrounding the city of Xalapa, Veracruz (Figure 1); bordered to the north by the city of Naolinco (19° 38' 49" NL, 96° 52' 37" WL) and to the south by the city of Xico (19° 24' 05" NL, 96° 59' 45" WL). The average distance between fragments is 1,538 m. Six locations where Q. germana was present were selected for this study, all located in the sub-basin of the Decozalapa river. Table 1 presents the location of the sites as well as the description of their characteristics (Instituto Nacional de Estadística y Geografía [INEGI], 2012; Williams-Linera, 2002).
Study material
Plant material was collected in transects that represented each location. The transects were traced using the first Q. germana subject found when crossing each fragment from north to south as a starting point (Comisión Nacional para el Desarrollo de los Pueblos Indígenas [CDI], 2004); therefore, subjects exposed to several exogenous variables were included. The transects were divided into blocks of 20 x 10 m; only the subjects from odd block numbers were evaluated, in order to diminish the probabilities of picking related subjects.
Morphological analysis of Q. germana
30 adult subjects of Q. germana were selected by location, taken from around three to five transects. The trees selected had a trunk diameter of more than 30 cm, between 6 and 20 m tall, with mature leaves and acorns, and with similar physiological states, vigor, and reproductive stages, to minimize the effect of the endogenous variables over the foliar later. Each subject was georeferenced (Garmin, Etrex GPS, USA). From the treetop of each tree, 10 leaves were taken from odd numbered branches from north to east, in order to reduce the effect of micro-environmental variation. The collected leaves were herborized to preserve them until their evaluation. The morphometric variables measured were the following: leaf length (LL), maximum width (MW), right width of the maximum width (RW), left width of the maximum width (LW), size of the petiole (SP), insertion angle of the first right rib and left rib (ARR, ALR), number of mucrones of the margin (NM), and number of right and left ribs (NRR, NLR). All of the variables were measured with a vernier scale (Truper, Mexico).
Environmental analysis
The environmental analysis was done in the same transects as the morphological sampling, assigning a day to evaluate each site and procuring the same schedule. The measurements were done at the foot of each tree, during the rainy season in September and during the dry season in June 2014, registering the following variables: environmental temperature (T, °C), relative humidity (RH, %), vegetation cover (VEGCOV, %), soil temperature (ST, °C), soil humidity (SH, %), light intensity (FC, candela per square foot), and photosynthetically active radiation (PAR). These variables were selected due to their association with the effects of fragmentation (Williams-Linera, 2002). The T and RH variables were measured with a digital thermo-hygrometer (Cole Parmer, EUA); the VEGCOV variable with a forest densitometer (Suunto Forestry suppliers, EUA); the ST variable was measured with a thermometer stem for soil (Metron, México) with a depth of 15 cm. The SH variable was obtained through the weight loss of 100 g of fresh soil after 48h at 70 °C. Finally, the FC and PAR variables were obtained with a luminometer with dual range (Fisher Scientific, EUA).
Statistical analysis
The differences between locations were determined with a discriminant factorial analysis, a multiple variation measure. The centroids were graphed by location through canonical correspondence, both for the morphometric variables and for the environmental variables. The differentiation measures between locations (Mahalanobis distances) allowed a group formation through the UPGMA model. The relation of the morphological foliar variation with the environment was determined through estimations of the Mahalanobis distances for the environmental attributes and a Mantel test with 10,000 iterations (P = 0.05) and an assignment model of the cases within the locations, considering the matrixes of environmental and morphological dissimilarity. The analyses were done with the STATISTICA v.7.0 program (StatSoft, 2004).
RESULTS AND DISCUSSION
Morphological analysis
Table 2 presents the mean values of the morphological variables of Q. germana in each sub-population. The morphometric variables that best divide and characterize the study locations (P ≤ 0.05) are related to the size of the leaf (LL and SP), number of mucrones (NM), and the symmetry (NRR, NLR) (Table 3), coinciding with what was found in other species of Quercus (Alvarez et al., 2009; González-Rodríguez & Oyama 2005; Tovar-Sánchez & Oyama, 2004). The MW, LW and RW were not significant. Table 3 shows the explanatory roots of the variation as a result of the discriminant analysis. The first three discriminant functions explain 96 % of the variance. The significant variables of function 1 are LL, NM, SP and NRR. For function 2, the only significant variable is NLR, while for function 3 the variables are NM, NLR, NRR and SP.
Figure 2 presents the conglomerate obtained through the UPGMA method, in which it is observed that the Coapexpan and USBI sites are morphologically similar. This first group is similar to the one formed by Museo and Xolostla, but different than the Hsevilla and Santuario sites. Figure 3 shows the sub-populations distributed based on the explanatory roots. The median classes of the canonical morphometric variables, estimated by location, showed that the higher values are related to: root one with NM, root two with NLR, NRR, and root three with SP; these four morphometic characteristics can be used to differentiate the study sites, assuming that the negative correlation of these variables indicates that the high values represent locations with fewer number or size of the character.
The results also showed that the leaves of the most dissimilar location are those of Santuario, because they contain the highest number of mucrones, big leaves and fewer ribs such as has been reported in Q laeta (Alvarez et al., 2009). Coapexpan presented fewer mucrones and bigger petioles, being very similar to USBI when it comes to mucrones. Museo and Xolostla are similar in the number of mucrones and ribs, but Xolostla showed the bigger petioles, which could be associated to fewer incidences of light and temperature (Figure 3), corresponding to what was reported by González-Rodríguez and Oyama (2005). Finally, Hsevilla presents intermediate characteristics in all sites. All these results suggest that there are foliar morphological differences among the locations, despite the short distances that separate the fragments.
Environmental analysis
The environmental variables that best divide and characterize the study sites are: T, RH and TS (Wilks's lambda = 0.145; P ≤ 0.05) both for the rainy season (2) and for the dry season (2). Table 4 shows that these variables are related to light (FC1, PAR1), the environmental temperature of the dry season (T2) and humidity (T1,RH1). The variables VEGCOV, SH, FC and PAR were not significant. The first three discriminant functions explain 96 % of the variance. The significant variables of function 1 are FC1, PAR1 and T2. For function 2, the only significant variable is T2, while for function 3 the significant variables are T1 and RH1.
Figure 4 shows that, based on the UPGMA, Xolostla and Museo are environmentally similar. There is another group formed by Hsevilla, USBI and Santuario; both groups are different to Coapexpan.
The median classes of the environmental canonical variables estimated per location showed how the higher values are related: root one with light (FC1 and PAR1, T2), root two with the temperature of the dry station (T2), and root three with humidity (T1, HR1). These six environmental characteristics can be used to differentiate the study sites, assuming that the light root presents a negative correlation to the scale in Figure 5; therefore, higher values in this axis represent a lower amount of light.
The results also show that the populations of Xolostla and Museo present a lower amount of light and temperature in the dry season; similarly, Muse is the site that loses a lower amount of humidity. USBI and Hsevilla are the locations with the most alike environment and are similar to Santuario in regards to the amount of light that they receive. Coapexpan is the location with greater environmental differences in comparison to the rest of the locations (Figure 5).
Analysis of the morphological and environmental relation
Regarding the existing relation between the morphological and the environmental variations, the square distances of Mahalanobis were compared through the Mantel test to obtain the regression value between both matrixes. The Mantel test showed a positive regression value but it was not significant (r = 0.9008, P = 0.3060). The Museo, Hsevilla and Coapexpan sites, that are environmentally different, have lesser morphological differentiation than expected, under the model of regression with markov chains. Other studies have reported morphological differences in the species exposed to climatic variation, due to this the differences in size and symmetry are usually associated to the environment in which each sub-population grows (Alvarez et al., 2009; Halloy & Mark, 1996). Furthermore, in other species of oak, it has been reported that the size of the leaf is related to humidity; the leaves are bigger in humid places and their size decreases gradually in relation to the increase of dryness (González-Rodríguez & Oyama, 2005; Uribe-Salas, Sáenz-Romero, González-Rodríguez, Téllez-Valdés, & Oyama, 2008). In other regions of the world, covariations between the size of the leaf and precipitation and temperature of the site have been reported (Calagari, Modirrahmati, & Asadi, 2006; Li et al., 2006; Royer, Wilf, Janesko, Kowalski, & Dilcher, 2005). In other species, the fewer number of mucrones and the bigger size of the petiole could be a strategy of the tree to diminish the loss of humidity and facilitate the capture of solar energy, associated with a lower amount of light and temperature (González-Rodríguez & Oyama, 2005). However, in this study, only morphological differences without significant relation to the environmental ones were found. Therefore, the environmental differences do not seem to affect the morphometric characteristics in the same manner in all locations (Hoff & Rambal, 2003). Due to the closeness and common origin of the sub-populations of Q germana, the morphological differences should not be present even in different environments. Consequently, the hypothesis that the morphological differences among the locations may be strengthened by fragmentation is accepted, even when they are not associated with the environment. Alvarez et al. (2009) found a relation between the environmental and morphological variables of Q laeta in populations with a greater geographical distance, so that the effect of fragmentation and the environment is significant. Conversely, in this study, the differences found in the foliar morphology are significant but have no relation to the environment.
CONCLUSIONS
It is noteworthy that even though the distances are short between each sub-population of Q germana, morphological and environmental differences can be observed; however, there is no association between both types of differences. In this manner, fragmentation could be affecting foliar morphology without it being related to the environmental conditions. The morphological variables that determine this differentiation are the number of mucrones, the number of ribs and the size of the petiole.
REFERENCES
Álvarez, E. Á., Sánchez-González, A., & Granados-Sánchez, D. (2009). Análisis de la variación morfológica foliar en Quercus laeta Liebm. en el parque nacional Los Mármoles, Hidalgo, México. Revista Chapingo Serie Ciencias Forestales y del Ambiente, 15(2), 87-93. Obtenido de http://www.chapingo.mx/revistas/forestales/contenido.php?id_revista_numero=40. [ Links ]
Bacilieri, R., Ducousso, A., & Kremer, A. (1995). Genetic, morphological, ecological and phenological differentiation between Quercus petraea (Matt.) Liebl. and Quercus robur L. in a mixed stand of northwest of France. Silvae Genetica, 44, 1-10. Obtenido de http://allgemeineforstundjagdzeitung.com/fileadmin/content/dokument/archiv/silvaegenetica/44_1995/44-1-1.pdf. [ Links ]
Borazan, A., & Babaç, M. T. (2003). Morphometric leaf variation in oaks (Quercus) of Bolu, Turkey. Annales Botanici Fennici, 40, 233-242. Obtenido de http://www.annbot.net/PDF/anbf40/anbf40-233.pdf. [ Links ]
Calagari, M., Modirrahmati, A. R., & Asadi, F. (2006). Morphological variation in leaf traits of Populus auphratica Oliv. Natural populations. International Journal of Agricultural and Biological Engineering, 8, 754-758. Obtenido de http://www.fspublishers.org/published_papers/14745_..pdf. [ Links ]
Cardillo, E., & Bernal, C. J. (2006). Morphological response and growth of cork oak (Quercus suber L.) seedlings at different shade levels. Forest Ecology and Management, 222, 296-301. doi: 10.1016/j.foreco.2005.10.026 [ Links ]
Comisión Nacional para el Desarrollo de los Pueblos Indígenas (CDI). 2004. Consultado 06-01-2014 en http://www.cdi.gob.mx/pnuma/c3_06.html.
Dow, B. D., & Ashley, M. V. (1998). High levels of gene flow in bur oak revealed by paternity analysis using microsatellites. Journal of Heredity, 86, 62-70. doi:10.1093/jhered/89.1.62. [ Links ]
Excoffier, L. (2001). Analysis of population subdivision. In D. J. Balding, M. Bishop, & C. Cannings (Eds.) Handbook of statistical genetics (pp. 271-307). New York, USA: John Wiley & Sons, Ltd. [ Links ]
Fernández-M. J., & Sork, V. L. (2007). Genetic variation in fragmented forest stands of the Andean Oax Quercus humbodtii Bonpl. (Fagaceae). Biotropica, 39(1), 72-78. doi: 10.1111/j.1744-7429.2006.00217.x. [ Links ]
González-Rodríguez, A., & Oyama, K. (2005). Leaf morphometric variation in Quercus affinis and Q. laurina (Fagaceae), two hybridizing Mexican red oaks. Botanical Journal of the Linnean Society, 147, 427-435. doi:10.1111/j.1095-8339.2004.00394.x. [ Links ]
Halloy, S. R. P., & Mark, A. F. (1996). Comparative leaf morphology spectra of plant communities in New Zealand, the Andes and the European Alps. Journal of the Royal Society of New Zealand, 26, 41-78. doi:10.1080/03014223.1996.9517504. [ Links ]
Hoff, C., & Rambal, S. (2003). An examination of the interaction between climate, soil and leaf area index in a Quercus ilex ecosystem. Annals of Forest Science, 60, 153-161. doi: 10.1051/forest:2003008. [ Links ]
Hovenden, M. J., & Vander S. J. K. (2006). The response of leaf morphology to irradiance depends on altitude of origin in Nothofagus cunninghamii. New Phytologist, 169, 291-297. doi: 10.1111/j.1469-8137.2005.01585.x. [ Links ]
Instituto Nacional de Estadística y Geografía (INEGI). Consultado 06-01-2012 en http://www.inegi.org.mx/geo/contenidos/mapadigital/.
Li, C., Zhang, X., Liu, X., Luukkanen, O., & Berninger, F. (2006). Leaf morphological and physiological responses of Quercus aquifolioides along an altitudinal gradient. Silva Fennica, 40, 5-13. Obtenido en http://210.75.237.14/handle/351003/21866. [ Links ]
Nikolic, N. P., Krstic, B. D., Pajevic, S. P., & Orlovic, S. S. (2006). Variability of leaf characteristics in different pedunculate oak genotypes (Quercus robur L.). Proceedings for Natural Sciences, Matica Srpska Novi Sad, 110, 95-105. doi: 10.2298/ZMSPN0611095N. [ Links ]
Ponton, S., Dupoguey, J., & Dreyer, E. (2004). Leaf morphology as species indicator in seedlings of Quercus robur L. and Q. petrea (Matt.) Liebl.: Modulation by irradiance and growth flush. Annals of Forest Science, 61, 73-80. doi: 10.1051/forest:2003086. [ Links ]
Royer, D. L., Wilf, P., Janesko, D. A., Kowalski, E. A., & Dilcher, D. L. (2005). Correlations of climate and plant ecology to leaf size and shape: Potential proxies for the fossil record. American Journal of Botany, 92, 1141-1151. doi: 10.3732/ajb.92.7.1141. [ Links ]
Sack, L., Melcher, P. J., Liu, W. H., Middleton, E., & Pardee, T. (2006). How strong is intracanopy leaf plasticity in temperate deciduous trees? American Journal Botany, 93, 829-839. doi: 10.3732/ajb.93.6.829. [ Links ]
Sáenz-Romero, C., Snively, A. E., & Linding-Cisneros, R. (2003). Conservation and restoration of pine forest genetic resources in Mexico. Silvae Genetica, 52, 233-237. Obtenido de: http://www.germanjournalofforestresearch.com/fileadmin/content/dokument/archiv/silvaegenetica/52_2003/52-5-6-233.pdf. [ Links ]
StatSoft. (2004). STATISTICA, version 7.0. User guide and documention. Oklahoma, USA: Author. [ Links ]
Tovar-Sánchez, E., & Oyama, K. (2004). Natural hybridization and hybrid zones between Quercus crassifolia and Quercus crassipes (Fagaceae) in México: Morphological and molecular evidence. American Journal of Botany, 91, 1352-1363. doi: 10.3732/ajb.91.9.1352. [ Links ]
Uribe-Salas, D., Sáenz-Romero, C., Gonzáles-Rodríguez, A., Téllez-Valdéz, O., & Oyama, K. (2008). Foliar morphological variation in the white oak Quercus rugosa Née (Fagaceae) along a latitudinal gradient in Mexico: Potential implications for management and conservation. Forest Ecology and Management, 256, 2121-2126. doi: 10.1016/j.foreco.2008.08.002. [ Links ]
Warren, Ch. R., Tausz, M., & Adams, M. A. (2005). Does rainfall explain variation in leaf morphology and physiology among populations of red ironbark (Eucalyptus sideroxylon subsp. tricarpa) grown in a common garden? Tree Physiology, 25, 1369-1378. doi: 10.1093/treephys/25.11.1369. [ Links ]
Williams-Linera, G. (2002). Tree species richness complementarity, disturbance and fragmentation in a Mexican tropical montane cloud forest. Biodiversity Conservation, 11, 1825-1843. doi: 10.1023/A:1020346519085. [ Links ]