Turkish Journal of Agriculture and Forestry Turk J Agric For (2018) 42: 262-271 http://journals.tubitak.gov.tr/agriculture/ © TÜBİTAK Research Article doi:10.3906/tar-1711-31

Environmental and soil variables affecting the structure and floristic woody composition of forests of northeastern

1, 2 Juan Antonio ENCINA-DOMÍNGUEZ *, José Ramón ARÉVALO SIERRA , 1 3 Eduardo ESTRADA-CASTILLÓN , Miguel MELLADO BOSQUE  1 Faculty of Forestry Sciences, Autonomous University of Nuevo Leon, Linares, Nuevo Leon, Mexico 2 Department of Botany, Ecology, and Physiology, Faculty of Sciences, University of La Laguna, Canary Islands, Spain 3 Department of Animal Nutrition, Antonio Narro Agrarian Autonomous University, Saltillo, , Mexico

Received: 07.11.2017 Accepted/Published Online: 28.03.2018 Final Version: 07.08.2018

Abstract: The objective of this study was to investigate the influence of environmental and soil factors on the structure and floristic woody composition of oak forests. Oak forests of the Sierra de Zapalinamé in northeastern Mexico (25°N) are distributed in canyons and northwest slopes with higher humidity, surrounded by montane chaparral. We carried out a vegetation inventory across an altitudinal gradient. All trees with diameter at breast height of ≥3 cm were identified and measured. In addition, the cover of understory species was measured in each plot. Using multivariate techniques, we detected two oak forest associations: Quercus greggii - Q. mexicana forest and Q. saltillensis - Q. laeta forest. The forests studied are rich in woody species, including 19 tree and 50 shrub species. The number of tree species decreased at lower elevations, but the shrub species increased. Environmental variables evaluated included elevation, precipitation, temperature, soil pH and electrical conductivity, and soil percentage of sand, clay, and silt. All these variables revealed significant differences for the two oak forest associations. With respect to biotic parameters, significant differences (P < 0.05) in basal area were observed. Multivariate analysis revealed the species distribution along a moisture gradient across elevation. The ecological study of oak forests provides the basis for future research on forest dynamics and can guide conservation efforts to maintain species diversity and endemism in the mountain studied.

Key words: Edaphic factors, elevation, forest structure, Quercus, species composition

1. Introduction Santacruz et al., 1996), Chihuahuan desert scrub (Huerta- Altitudinally defined climatic and soil factors are primary Martínez et al., 2004), and boreal forest (Seibert et al., 2007) determinants of differences in species composition and tropical rainforests (Fernandes-Abreu et al., 2012). At and community structure on undisturbed mountains local scales, species richness and the structure of forest (Fischer et al., 2014; Toledo-Garibaldi and Williams- landscapes are strongly influenced by geomorphology Linera, 2014). The occurrence of plant species is and elevation (Behera and Kushwaha, 2007) and also by dependent on various factors acting on different spatial soil physicochemical properties (Estrada-Castillón et al., scales. Elevation represents a complex gradient through 2015) and anthropogenic disturbances (Ramírez-Marcial which environmental variables change simultaneously et al., 2001). (Austin et al., 1996). Most important are temperature Mexico is a center of diversity of the genus Quercus and precipitation (Körner, 2007), both of which influence (Nixon, 1993). This genus forms pure oak or mixed - the available humidity, the properties of soils, and their oak stands, one of the most species-rich vegetation types in formation processes (Guerrero-Campo et al., 1999). Mexico and characteristic of temperate mountain ranges Edaphic factors have an important role in the throughout the country (Muller-Using, 1994; Rzedowski, distribution and floristic variations and the abundance 2006; Encina-Domínguez et al., 2011). In northeastern of is closely related to soil properties, especially Mexico, the Sierra de Zapalinamé is a mountain range and nutrient availability (Rahayu et al., 2012). Relationships a protected area in the category of ecological conservation, between soil properties and plant species abundance have enacted by the state government of Coahuila (Periódico been described in various grassland habitats (Aguado- Oficial, 1996). Here the oak forest is restricted to canyons

* Correspondence: [email protected] 262

This work is licensed under a Creative Commons Attribution 4.0 International License. ENCINA-DOMÍNGUEZ et al. / Turk J Agric For with higher humidity (Encina-Dominguez and Valdés- pinyon pine forest associated with xeric scrubland 9.55% Reyna, 2013). These oak forests contain 259 plant species (UAAAN, 1998). Oak forests are distributed in temperate (Encina-Domínguez et al., 2009), 28% of the flora of sites with more humidity at elevations between 2000 and this mountain range (Encina-Domínguez et al., 2016), 2600 m a.s.l. They are more abundant in the San Lorenzo including Quercus saltillensis Trel., which is endemic to and Boca Negra Canyons, and above Lomas de Lourdes southeastern Coahuila. Moreover, the conservation of (Encina-Domínguez and Valdés-Reyna, 2013). The most these forests is very important because they constitute common tree species in the oak forests are Quercus the main source of drinking water for the city of Saltillo, greggii (A.DC.) Trel., Q. mexicana Bonpl., Q. saltillensis and they offer a habitat for important wildlife such the with scattered Schltdl., Quercus laeta American black bear (Ursus americanus Pallas, 1780). Liebm., and Pinus greggii Engelm. ex Parl. According to Species composition and community structure and Encina-Domínguez et al. (2007), in these forests, the most their relationship with environmental factors are the basis abundant shrub genera are , Garrya, and Stevia, for studying forest dynamics. Understanding ecological and the most abundant herbaceous genera are Achillea, processes in forests is one of the most important goals Artemisia, and Polypodium. for proper management and biodiversity conservation 2.2. Vegetation sampling (Arévalo et al., 2012). Little work has been carried out to We estimated vegetation attributes by sampling 66 sites, determine the influence of environmental factors on the located along altitudinal gradients in canyons with a north structure and species composition of the oak forest in the or northwest exposition, where oak species dominate the Sierra de Zapalinamé region. canopy. At each site, we established a circular 500-m2 plot, We will test the following hypotheses: 1) that elevation where all shrubs were recorded and identified, and all is the most important variable in determining the structure trees with diameter at breast height (DBH) of ≥3 cm were and community composition because of its influence on identified, counted, and measured (Olvera-Vargas et al., ambient temperature and precipitation, and 2) that the 1996). Taxonomic identities of collected plant specimens physicochemical properties of the soils are similar through were determined and vouchers deposited at the ANSM oak forests of the study area. herbarium. For species names, we followed the checklist of native vascular plants of Mexico (Villaseñor, 2016). 2. Material and Methods Plot position and elevation were measured using 2.1. Study site a global positioning system (GPS; Etrex, Garmin Ltd., The Sierra de Zapalinamé is located in the southeast of Olathe, KS, USA). Chemical and physical soil factors were the state of Coahuila. It has an area of 45,000 ha, in the based on bulk samples taken from depths of 0–30 cm. municipalities of Saltillo and Arteaga. It is located south The soil samples were mixed, dried, and sifted through a of the city of Saltillo, between 25°15′00″N and 25°25′58″N 2-mm sieve; debris and stones were eliminated. Texture and between 100°47′14″W and 101°05′03″W (Figure (sand, clay, and silt) was determined using a Bouyoucos 1). It belongs to the Gran Sierra Plegada physiographic hydrometer. Organic matter content was determined by subprovince. The elevation ranges from 1590 m in the Walkley and Black method (Nelson and Sommers, the foothills to 3140 m in the Cerro El Penitente, with 1982) and pH was measured in a soil-to-water ratio of intermountain valleys averaging 2200 m. The rocks of 1:5 extract. Soil nitrogen, phosphorus, potassium, and the area are sedimentary, belonging to the Jurassic and electrical conductivity were determined. Qualitative Cretaceous periods; limestone covers 43% of the area, while levels baseline for nutrients obtained such as N, P, K, and 17% is sandstones and conglomerates. Alluvial soils occupy organic matter were according to SEMARNAT (2000) and 30% of the area, with variable depth, mainly found in the Fernández-Linares et al. (2006). plains with alluvial fans at the base of the mountains. Soils in Climatic data were obtained by interpolation from a the valleys are deep. There are also smaller areas of calcium linear regression analysis using records for the last 10 years and phaeozem calcaric xerosols. The dominant climate of from 45 weather stations adjacent to the study area in order the study area is the dry type (BSkw), while the upper parts to have greater variation for the study site (Trewin, 2007). of the mountain have a temperate type (C(w0)). The average Quantitative information was taken from database records annual temperature is 16.9 °C and the annual rainfall is 498 from CONAGUA (http://siga.cna.gob.mx/Cartografia. mm (UAAAN, 1998). The rains are convective and occur aspx). The variables used were elevation, based on a digital mainly in the warmest months of the year. terrain model (INEGI, 2013), as an independent variable Different plant communities have been recorded for and annual average temperature and precipitation as this area, including rosetophyllous scrub, pine forest, fir dependent variables; thus, the digital model of the average forest, oak forest, and montane chaparral. The pine forest annual precipitation and mean annual temperature values occupies 14.09% of the area, pinyon pine forest 12.54%, and was obtained.

263 ENCINA-DOMÍNGUEZ et al. / Turk J Agric For

Figure 1. Location of Sierra de Zapalinamé, in the state of Coahuila, northeastern Mexico (25°N).

264 ENCINA-DOMÍNGUEZ et al. / Turk J Agric For

2.3. Statistical analysis For each oak association, we calculated the basal area Classification of the forests was based on the density of and density of trees and shrubs. Using the density of species 69 woody species present in the 66 plots. The vegetation in the samples, we obtained an evenness index according assemblages were classified using WinTWINS Cluster to Magurran (2004). Finally, for environmental variables Analysis (two-way indicator species analysis, TWINSPAN for (elevation, soil pH, soil organic matter content, and Windows) version 2.3 (Hill and Šmilauer, 2005). TWINSPAN percentage of sand, silt, clay, nitrogen, phosphorus, and is a tool to classify samples by species composition. It potassium, as well as soil electrical conductivity) and for constructs an ordered two-way table from a site-by-species the structural attributes in each oak association, Student’s matrix that shows species synecological relations. t-test was performed to compare sites; significance was For ordination, detrended correspondence analysis declared at P < 0.05. (DCA) (Hill and Gauch, 1980) was performed to analyze The statistical methods using Student’s t-test for how species composition changed along the main gradient. comparison of two means and correlation analysis To reveal the relationship of the DCA axis I scores of the followed Zar (1984) and were implemented using the SPSS plots with elevation and edaphic variables, we obtained the computer package (SPSS, 1997). Pearson correlation coefficient among these variables. We used canonical correspondence analysis (CCA) to 3. Results examine the distribution and relationship between species The woody flora of the oak forests comprises 69 species and edaphic, climatic, and topographic factors (ter Braak, (19 tree species and 50 shrub species), in 24 families. The 1987). The analysis was based on the density values of 69 shrub species in these oak forests are also found in adjacent woody species, 66 sampling plots, and five environmental communities such as the montane chaparral (17 species), variables (elevation, precipitation, temperature, and soil and a few in the rosetophyllous scrub, pine, and fir forests. physicochemical variables such as K and percentage of Based on TWINSPAN, two oak associations were silt). To test the significance of the eigenvalue of the first discriminated: first, a Quercus greggii - Q. mexicana axis and to select the environmental variables explaining association, and second, a Quercus saltillensis - Q. laeta species composition, manual forward selection through a association. In general, site conditions were characterized Monte Carlo permutation test with 499 permutations (P by moderate slopes, because they are located in canyons, < 0.05 significance) was performed. The manual forward with an average soil depth of 20–50 cm, abundant leaf selection was performed by selecting the variables that litter, and low rockiness. The variables of elevation, explained the greatest inertia (ordered by CANOCO) of precipitation, ambient temperature, soil pH, soil electrical the total inertia of the CCA axis 1. Ordination analysis was conductivity, and percentages of sand, clay, and silt in the performed with CANOCO version 4.5 package software soil presented significant differences (P < 0.05) between (ter Braak and Šmilauer, 2002). the two associations (Table 1).

Table 1. Mean and standard deviation of environmental variables for two oak associations clustered from TWINSPAN. Differences between the two associations were compared with Student’s t-test (t).

Que gre - Que mex Que sal - Que lae t P Elevation (m) 2441.9 ± 91.1 2177.2 ± 106.0 10.696 P < 0.05 Precipitation (mm) 524.1 ± 23.9 459.25 ± 24.48 10.513 P < 0.05 Temperature (°C) 14.62 ± 0.33 15.59 ± 0.39 –10.635 P < 0.05 Organic matter (%) 5.29 ± 2.21 5.96 ± 2.36 –1.151 n.s. Nitrogen (mg/kg) 0.26 ± 0.11 0.30 ± 0.12 –1.180 n.s. Phosphorus (mg/kg) 12.67 ± 3.91 12.46 ± 2.62 0.232 n.s. Potassium (mg/kg) 185.5 ± 52.9 170.83 ± 26.85 1.263 n.s. Soil pH 6.24 ± 0.76 7.02 ± 0.49 –4.470 P < 0.05 Electrical conductivity (meq/100 g) 0.34 ± 0.10 0.44 ± 0.08 –3.821 P < 0.05 Sand (%) 49.17 ± 9.38 43.58 ± 11.35 2.153 P < 0.05 Clay (%) 19.38 ± 5.40 30.33 ± 9.59 –5.949 P < 0.05 Silt (%) 31.48 ± 6.62 26.08 ± 7.74 2.990 P < 0.05 Que gre - Que mex = Quercus greggii - Quercus mexicana; Que sal - Que lae = Quercus saltillensis - Quercus laeta; n.s. = nonsignificant.

265 Quercus mexicana Quercus saltillensis - Quercus laeta ENCINA-DOMÍNGUEZ et al. / Turk J Agric For

The soil pH showed significant differences between We graphically presented axis I (eigenvalue of 0.612 the Quercus greggii - Q. mexicana association (mean: and a cumulative percentage of variance of 17.9%) and 6.24; medium acidity) and the Quercus saltillensis - Q. axis II (eigenvalue of 0.278 and a cumulative percentage laeta association (mean: 7.02; neutral). Soils in the of variance of 26%) of the DCA (with a total inertia of sampled plots had more than 4% organic matter and were 3.418). Ordination of species with DCA, based on woody therefore extremely rich in this component. This property species density, revealed two clusters of sites that represent is correlated with the amount of N in soils, and the plots a centroid of both oak forests (Figure 3). Environmental had above 0.25% of total N and were considered rich in variables such as temperature (r2 = 0.96), precipitation (r2 = this element. The P content of soils was poor, with values 0.93), elevation (r2 = 0.72), soil pH (r2 = 0.31), percentage of of 9–16 mg/kg, and the K content was medium, at 101– clay (r2 = 0.29), soil electrical conductivity (r2 = 0.23), and 200 mg/kg. The soils were deemed nonsaline, with low percentage of silt (r2 = 0.11) had significant correlations (P electrical conductivity values (less than 2.5 mmhos/cm). < 0.01) with axis I. Regarding the biotic variables of these oak forests, The floristic group represented by high richness shrub the density of trees and shrubs, DBH, and total richness species was tightly clustered with high scores on axis I. did not differ between the two associations. However, Quercus saltillensis, Q. laeta, and Q. laceyi were abundant significant differences (P < 0.05) were observed in basal in canyons and on hillsides at low elevations, close to 2000 area for the tree species (Table 2). m, and this formation was the driest forest, including shrub Woody species richness and evenness were higher in species of xeric affinity common in adjacent scrublands. the Quercus saltillensis - Q. laeta association. The average In contrast, the other major floristic gradient, which was DBH in both associations was less than 10 cm. Quercus richer in tree species, was across a mesic zone of our study mexicana had a mean diameter of 14 cm, and Q. saltillensis area and appeared close to the center of the ordination 13 cm. Pinus greggii reached up to 54 cm in diameter; diagram. This floristic group was evenly distributed with however, its density was low (36 individuals/ha), and it low scores on axis I and dominated by Quercus greggii - grows in forests with more humidity. The basal area and Q. mexicana growing at an average elevation of 2400 m; it density of oak tree species is shown in Figure 2, where it is included tree and shrub species that grow in humid and observed that Quercus greggii and Q. saltillensis are the two temperate canyons such as the genera Pinus, Arbutus, and most important in the forest structure since they have Cupressus and shrubs such as Garrya, Holodiscus, and the highest total density and basal area. Lonicera (Figure 3). The density of shrubs was higher in theQuercus greggii Five environmental variables analyzed were selected - Q. mexicana forest, with 40 species, dominated by Garrya by the forward selection (P < 0.05). These were elevation, glaberrima Wangerin, Ageratina saltillensis (B.L.Rob.) precipitation, temperature, and soil physicochemical R.M.King & H.Rob., and A. ligustrina (DC.) R.M.King & variables such as K and percentage of silt. Cumulative H.Rob. with 1475 ind/ha, which represents 44.60% of the percentage variance of the species - environment total vegetation density. The Quercus saltillensis - Q. laeta relationship for axes 1 and 2 was 77.8, indicating that forest was the richest with 48 species, where the dominant most of the information was concentrated on the first shrubs were Ageratina saltillensis, Salvia regla Cav., two axes. Considering the correlations of environmental and Stevia berlandieri A.Gray, with 1174 ind/ha, which variables with axes, the first CCA axis was positively and represented 35.50% of the total vegetation density. strongly correlated with ambient temperature (r = 0.89)

Table 2. Mean ± standard deviation for structural attributes including species richness and diversity for woody species in both oak forests. Differences between the forests were compared with Student’s t-test.

Que gre - Que mex Que sal - Que lae t P Diameter at 1.30 m (cm) 10.019 ± 1.39 9.40 ± 1.29 1.75 n.s. Basal area (m2/ha) 21.9 ± 3.9 16.5 ± 6.7 4.13 P < 0.01 Density trees (ind/ha) 2323.8 ± 746.7 2231.7 ± 843.2 0.46 n.s. Density shrubs (ind/ha) 3374.3 ± 2443.9 3194.2 ± 1724.7 0.32 n.s. Species richness 14.95 ± 4.1 17.13 ± 4.8 -1.94 n.s. Evenness 0.70 0.76

Que gre - Que mex = Quercus greggii - Quercus mexicana; Que sal - Que lae = Quercus saltillensis - Quercus laeta; n.s. = nonsignificant.

266 ENCINA-DOMÍNGUEZ et al. / Turk J Agric For

Figure 2. Basal area and density of the main tree species of Quercus in the oak forest of Sierra de Zapalinamé.

DCA - COMPOSITION WOODY SPECIES 5 Yuc car Cer can

Pur pli Rhu vir Opu rob Opu ste Gym glu Cra bar Mim acu Bri ver Que lac Que lae Age cal Age sco All tri Cer fot Sal las Que cor Gar ova Sal gre Pru mex Lit par Mal den I

I All eut Rhu aro Pru ser Pin cem

S Cor sto Que sal I Fra bet Bud cor Ste ova X Gar gla Age hav Nol ces Bou ter A

Fra cus - Sym mic Pax myr Age sal Ste ber Lin mes A Arc pun Lon pil Aga gen

C Pop tre Que rug Age lig D Pin gre Hel glo Que pri Que hyp Que mex Arb xal Smi bon Cup ari Cea cae Aga asp

Que gre

Pse men Jun fla Hol dis Cer mon Que sid Bac sul Sal reg Que gri Chr mex

Opu eng -2

-4 6 DCA - AXIS I Figure 3. DCA showing 69 woody species of oak forest in Sierra de Zapalinamé; tree species appear in bold. The dashed-line polygon encloses the Quercus saltillensis - Q. laeta association and the solid line polygon encloses the Quercus greggii - Q. mexicana forest. A complete checklist of species appears in the Appendix. and negatively and strongly correlated with elevation temperatures (Figure 4). The second axis was positively (r = –0.89) and precipitation (r = –0.89), suggesting correlated with percentage of silt (r = 0.34) and negatively a topographic temperature gradient from low slopes correlated with K (r = –0.34). The test of significance for with highest temperatures to high canyons with lowest the first canonical axis was significant (P < 0.002).

267 ENCINA-DOMÍNGUEZ et al. / Turk J Agric For

CCA - SPECIES AND ENVIRONMENTAL VARIABLES 0

. Yuc car 1

Pur pli SILT Cer can Que sid Ste ova

Sal las Aga asp Que lac All eut Nol ces Opu rob Rhu vir

I Gar gla I Pru mex Que lae Pin gre Que sal

S Cra bar I Pop tre Hol dis Lon pil Pru seAr ge sal Gar ova Mim acu

X Lit par Mal den PREC Sym mic Que gre Pse men Rhu aro Lin mesGym glu TEMP A

- ELEV Que mex Smi bon Cer fot All tri Arb xal Pax myr Ste ber Opu ste A Age lig Aga gen Cup ari Age sco C Fra cus Que cor Sal gre Age cal Fra bet Age hav Bud cor C Cea cae Que hyp Bou ter Bac sul Pin cem Cer monJun fla Bri ver Cor sto Sal reg

Que rug K Que gri Que pri

Hel glo

Arc pun Chr mex 0 .

1 Opu eng -

-1.5 CCA - AXIS I 1.5 Figure 4. CCA for woody species present in the study site and the five most significant environmental variables affecting vegetation. Abbreviations of the species use the first three letters of the genus and plant species name (see acronyms in the Appendix). ELEV: Elevation, PREC: average precipitation, TEMP: average temperature, SILT: percentage of silt, and K: potassium.

Ageratina saltillensis, Stevia berlandieri, and Arbutus Several studies have reported that oak species xalapensis Kunth were the most widely distributed and distribution is affected by variation in temperature, abundant species across the oak forests and were placed precipitation, or soil moisture gradients and nutrients close to the center of the ordination diagram. This clearly (Diaz-Maroto et al., 2007; Aguilar-Romero et al., 2016), showed their generalist behavior, in contrast to species conditioning the communities in which these species such as Quercus sideroxyla Bonpl., Q. grisea Liebm., and are dominant. The most important environmental Q. rugosa Née, which were further away from the center of variables associated with the observed patterns of floristic the CCA biplot. We consider that they have greater habitat composition in the oak forests studied were elevation, specificity, based on their locally restricted geographic soil pH, and percentage of silt. Elevation was the most distribution. important determinant because it acts as a combination of other ecological factors with a more direct action on the 4. Discussion distribution of plant species (Arévalo et al., 2012). In the study area the distribution of the two oak forest Based on ordination analysis, in the study area Quercus associations was influenced mainly by elevation, species were distributed in an altitudinal gradient, from temperature, and precipitation as revealed by CCA. The Q. saltillensis and Q. laeta at lower to Q. greggii and Q. differences in basal area and density in the oak forests mexicana at medium and Q. sideroxyla Bonpl. at the studied can be attributed to such environmental variability, highest elevations, confirming the specialist behavior of which differs between the forests. This may be related Quercus species with regard to altitude (Olvera-Vargas et to a combination of a higher stem density with larger al., 2010). Altitude gradient was also an important factor diameters of such species, possibly correlated with the determining patterns of floristic composition in oak forests highest rainfall. Similarly, in oak forests in central Mexico, in west-central Mexico (Olvera-Vargas et al., 2010) and in Aguilar-Romero et al. (2016) observed a relationship the northern Oaxaca range in Mexico (Meave et al., 2006). between oak species distribution and temperature and The chemical properties of soils are affected by the precipitation. underlying geological material, climatic, and biotic factors,

268 ENCINA-DOMÍNGUEZ et al. / Turk J Agric For which determine soil fertility (Mengel and Kirkby, 2001). al., 2007). This forest, growing at low elevations, has a more In the forests studied, chemical properties such as organic open canopy and the oak species are deciduous; therefore matter and NPK nutrients are similar through the oak it has more genera of xeric affinity, similar findings forests; in this way, there are no significant differences, and having been registered by Vázquez and Givnish (1998). In this is because the soils of both forests are derived from addition, this forest has more human influences through limestone rocks. goat grazing and has experienced forest fires (Portes, 2001; The forests studied had a very high organic matter Encina-Domínguez et al., 2007). content. The soil pH was from moderate acid reaction The structure and composition of the Zapalinamé to neutral, and these values are close to those reported forests probably still reflect a carry-over effect of the past for oak forests of Mexico, which in general have soil pH history of timber harvesting, including the major logging between 5.5 and 6.5, with abundant leaf litter and high of oaks for railway sleepers in the late 19th century and organic matter content (Rzedowski, 2006). Possibly, the even the collection of beams, posts, and poles throughout small difference of pH values was associated with levels the early 20th century. In the forests studied, there are no of precipitation reported for the two oak forests. It is well recent records of logging, perhaps because of the difficult known that high rainfall provokes an increased leaching access to canyons. Today anthropogenic intervention of Ca and Mg, allowing the pH to decrease (Merry, 2009). comes through livestock grazing and recreation. A major The low values of density and basal area recorded in this fire occurred in 1998 causing a decrease in the Quercus study could be related to soil nutrient contents, because saltillensis - Q. laeta forest (Portes, 2001), with a quick plant growth is conditioned by macronutrients (Havlin expansion of montane chaparral. et al., 2014). Broad-leaved deciduous forests are believed Our results demonstrate the existence of a clear to be limited by P (Axmanová et al., 2011). In the forests environmental gradient influence on the composition and studied, soil N supply was not limiting, but P levels were structure of oak forests in the study area. A combination low and K levels were medium. P in soil for both forests of landscape features (especially elevation), climatic studied was low, which agrees with findings by Díaz- variables, and some soil properties were very important in Maroto et al. (2007), who mentioned that this probably can explaining the distribution of woody species. As a result be explained because the oak stands studied were mature of the ecological analysis in oak forests, we recommend and had not undergone any change in land use. However, that the ecological data shown here should be used for perhaps more important is the low rainfall, because this promoting the protection and restoring the impacted areas. mountain is located near the Chihuahuan Desert Region Conservation efforts through appropriate management (Henrickson and Johnston, 1986), which is characterized should concentrate on maintaining the species richness by low to moderate rainfall. According to Rzedowski and structure in these forests. (2006), most oak forests in Mexico grow in areas with rainfall greater than 600 mm, reaching 1500 mm or more Acknowledgments in neotropical montane oak forests, which have high basal The senior author thanks the National Council on areas and densities, including the oak forest highlands of Science and Technology for a scholarship-loan to conduct Chiapas (González-Espinosa et al., 2006) and northern these doctoral studies. We wish to thank the staff of the Oaxaca (Meave et al., 2006), and the humid montane oak Zapalinamé protected area for supporting this research, forests of west Mexico (Olvera-Vargas et al., 2010). especially Sergio C Marines G and Juan M Cárdenas. We The richness of vascular plants is highest in the oak also thank Rafael H Cárdenas, Julio Cesar Gómez, and forest of Quercus saltillensis - Q. laeta (Encina-Domínguez Zilmar A Zamora for assistance during field data collection. et al., 2007); also in this association, the soil pH and Onofre Pastrana prepared the map and Cristobal Flores temperature are higher. Similar findings were registered provided data of precipitation and temperature in the study by Chytrý et al. (2007) in forests at relatively warm sites area. Thanks to Timothy Synnott and Allen Coombes for with a high soil pH in continental southern Siberia. We improving the English. We appreciate the soil analyses observed that the number of tree species decreased at lower carried out by Antonio Ilizaliturri from the Universidad elevations, but the number of shrub species increased. The Autónoma Agraria Antonio Narro, Saltillo, Mexico. Many greatest shrub richness is found in the Quercus saltillensis thanks to the Universidad de La Laguna, Tenerife, Spain - Q. laeta association, because it is located in a transition for invaluable support during the preparation of this paper. zone with the montane chaparral (Encina-Domínguez et

269 ENCINA-DOMÍNGUEZ et al. / Turk J Agric For

References

Aguado-Santacruz, GA, García-Moya E, Velasco-González C, Flores- Estrada-Castillón E, Arévalo JR, Villarreal-Quintanilla JÁ, Salinas- Flores JL (1996). Importancia de los elementos climáticos en la Rodríguez MM, Encina-Domínguez JA, González-Rodríguez variación florística temporal de pastizales semidesérticos. Acta H, Cantú Ayala CM (2015). Classification and ordination of Bot Mex 35: 65-81 (in Spanish). main plant communities along an altitudinal gradient in the Aguilar-Romero RF, García-Oliva F, Pineda-García F, Torres I, Peña- arid and temperate climates of northeastern Mexico. Sci Nat Vega E, Ghilardi A, Oyama K (2016). Patterns of distribution 102: 59-70. of nine Quercus species along an environmental gradient in a Fernandes-Abreu M, Rodrigues-Pinto JR, Maracahipes L, Gomes fragmented landscape in central Mexico. Bot Sci 94: 471-482. L, Almeida de Oliveira E, Schwantes-Marimon B, Marimon- Arévalo JR, Cortés-Selva F, Chiarucci A (2012). Ecological Junior BH, de Farias J, Lenza E (2012). Influence of edaphic determinants of species composition in the forest vegetation of variables on the floristic composition and structure of the tree- Tuscany, Italy. Plant Ecol Evol 145: 323-331. shrub vegetation in typical and rocky outcrop cerrado areas in Serra Negra, Goiás State, Brazil. Braz J Bot 35: 259-272. Austin MP, Pausas JG, Nicholls AO (1996). Patterns of tree species richness in relation to environment in southeastern New South Fernández-Linares LC, Rojas-Avelizapa NG, Roldán-Carrillo TG, Wales, Australia. Aust J Ecol 21: 154-164. Ramírez-Islas ME, Zegarra-Martínez HG, Uribe-Hernández R, Reyes-Ávila, RJ, Flores-Hernández D, Arce-Ortega JM Axmanová I, Zelený D, Li CF, Chytrý M (2011). Environmental factors influencing herb layer productivity in Central European (2006). Manual de técnicas de análisis de suelos aplicadas a oak forests: insights from soil and biomass analyses and a la remediación de sitios contaminados. Mexico City, Mexico: phytometer experiment. Plant Soil 342: 183-194. Secretaría de Medio Ambiente y Recursos Naturales, Instituto Nacional de Ecología (in Spanish). Behera MD, Kushwaha SPS (2007). An analysis of altitudinal behavior of tree species in Subansiri district, eastern Himalaya. Fischer HS, Michler B, Ewald J (2014). Environmental, spatial and Biodivers Conserv 16: 1851-1865. structural components in the composition of mountain forest in the Bavarian Alps. Folia Geobot 49: 361-384. Chytrý M, Danihelka J, Ermakov N, Hájek M, Hájková P, Koči M, Kubešová S, Lustyk P, Otýpková Z, Papov D et al. (2007). Plant González-Espinosa M, Ramírez-Marcial N, Galindo-Jaimes L (2006). species richness in continental southern Siberia: effects of Secondary succession in montane pine-oak forests of Chiapas, pH and climate in the context of the species pool hypothesis. Mexico. In: Kappelle M, editor. Ecology and Conservation of Global Ecol Biogeogr 16: 668-678. Neotropical Montane Oak Forest. Ecological Studies Vol. 185. Berlin, Germany: Springer, pp. 209-221. Díaz-Maroto IJ, Fernández-Parajes J, Vila-Lameiro P (2007). Chemical properties and edaphic nutrients content in natural Guerrero-Campo J, Alberto F, Hodgson J, García-Ruiz JM, stands of Quercus pyrenaica Willd. in Galicia, Spain. Eurasian Montserrat-Martí G (1999). Plant community patterns in a Soil Sci 40: 522-531. gypsum area of NE Spain. I. Interactions with topographic Encina-Domínguez JA, Estrada-Castillón E, Villarreal-Quintanilla factors and soil erosion. J Arid Environ 41: 401-410. JA, Villaseñor JL, Cantú-Ayala CM, Arévalo JR (2016). Floristic Havlin JL, Tisdale SL, Nelson WL, Beaton JD (2014). Soil Fertility richness of the Sierra de Zapalinamé, Coahuila, Mexico. and Fertilizers: An Introduction to Nutrient Management. 8th Phytotaxa 283: 1-42. ed. Upper Saddle River, NJ, USA: Prentice Hall. Encina-Domínguez JA, Mata-Rocha E, Meave JA, Zárate-Lupercio Henrickson J, Johnston MC (1986). Vegetation and community A (2011). Community structure and floristic composition types of the Chihuahuan Desert. In: Barlow JC, Powell AM, of Quercus fusiformis and Carya illinoinensis forests of the Timmermann BN, editors. Second Symposium on Resources Northeastern Coastal Plain, Coahuila, Mexico. Rev Mex of the Chihuahuan Desert Region, United States and Mexico. Biodivers 82: 607-622. Alpine, TX, USA: Chihuahuan Desert Research Institute, pp. Encina-Domínguez JA, Valdés-Reyna J (2013). Vegetación de la 20-39. Sierra de Zapalinamé. In: Arizpe-Narro A, editor. Sierra Hill MO, Gauch HJ Jr (1980). Detrended correspondence analysis, Zapalinamé. Guía para conocer y valorar el área protegida an improved ordination technique. Vegetatio 42: 47-58. de la Sierra de Zapalinamé. Saltillo, Mexico: Elementocero ediciones, pp. 57-72 (in Spanish). Hill MO, Šmilauer P (2005). TWINSPAN for Windows Version 2.3. Huntingdon, UK: Centre for Ecology and Hydrology & Encina-Domínguez JA, Zárate-Lupercio A, Estrada-Castillón E, University of South Boehmia. Valdés-Reyna J, Villarreal-Quintanilla JA (2009). Composición y aspectos estructurales de los bosques de encino de la Sierra Huerta-Martínez FM, Vázquez-García JA, García-Moya E, López- de Zapalinamé, Coahuila, México. Acta Bot Mex 86: 71-108 (in Mata L, Vaquera-Huerta H (2004). Vegetation ordination at Spanish). the southern Chihuahuan Desert (San Luis Potosi, Mexico). Plant Ecol 174: 79-87. Encina-Domínguez JA, Zárate-Lupercio A, Valdés-Reyna J, Villarreal-Quintanilla JA (2007). Caracterización ecológica y INEGI (2013). Continúo de modelos digitales de elevación LIDAR de diversidad de los bosques de encino de la sierra de Zapalinamé, terreno con resolución de 15 m. Mexico City, Mexico: Instituto Coahuila, México. B Soc Bot Mex 81: 51-63 (in Spanish). Nacional de Estadística, Geografía e Informática (in Spanish).

270 ENCINA-DOMÍNGUEZ et al. / Turk J Agric For

Körner C (2007). The use of ‘altitude’ in ecological research. Trends Ramírez-Marcial N, González-Espinosa M, Williams-Linera G Ecol Evol 22: 569-574. (2001). Anthropogenic disturbance and tree diversity in montane rain forest in Chiapas, Mexico. Forest Ecol Manag Magurran AE (2004). Measuring Biological Diversity. Oxford, UK: 154: 311-326. Blackwell Publishing. Rzedowski J (2006). Vegetación de México. 1era. Edición digital. Meave JA, Rincón A, Romero-Romero MA (2006). Oak forests of the Mexico City, Mexico: Comisión Nacional para el Conocimiento hyper-humid region of La Chinantla, northern Oaxaca range y Uso de la Biodiversidad (in Spanish). Mexico. In: Kappelle M, editor. Ecology and Conservation of Neotropical Montane Oak Forest. Ecological Studies Vol. 185. Seibert J, Stendahl J, Sørensen R (2007). Topographical influences on Berlin, Germany: Springer, pp. 113-125. soil properties in boreal forests. Geoderma 141: 139-148. Mengel K, Kirkby EA (2001). Principles of Plant Nutrition. 5th ed. SEMARNAT (2000). Norma Oficial Mexicana NOM-021- Dordrecht, the Netherlands: Kluwer Academic. SEMARNAT-2000. Establece las especificaciones de fertilidad, salinidad y clasificación de suelos. Estudios, muestreo y Merry RH (2009). Acidity and alkalinity of soils. In: Sabljic A, editor. análisis. Diario Oficial de la Federación. Mexico City, Mexico: Environmental and Ecological Chemistry, Vol. 2; Encyclopedia Secretaría de Medio Ambiente y Recursos Naturales (in of Life Support Systems. Paris, France: UNESCO-EOLSS Spanish). Publishers, pp. 115-131. SPSS (1997). SPSS Base 7.5 Applications. Guide. Chicago, IL, USA: Muller-Using B (1994). Contribuciones al conocimiento de los SPSS Inc. bosques de encino y pino-encino en el Noreste de México. Reporte Científico No. 14. Linares, Mexico: Facultad de ter Braak CJF (1987). The analysis of vegetation-environment Ciencias Forestales, Universidad Autónoma de Nuevo León (in relationships by canonical correspondence analysis. Vegetatio Spanish). 69: 69-77. Nelson DW, Sommers LE (1982). Total carbon, organic carbon and ter Braak CJF, Šmilauer P (2002). CANOCO reference manual and organic matter. In: Page AL, Miller RH, Keeney DR, editors. CanoDraw for windows user’s guide: software for canonical Methods of Soil Analysis. Part 2. Chemical and Microbiological community ordination (version 4.5). Ithaca, NY, USA: Properties. 2nd ed. Madison, WI, USA, pp. 539-579. Microcomputer Power. Nixon KC (1993). The genus Quercus in Mexico. In: Ramamoorthy Toledo-Garibaldi M, Williams-Linera G (2014). Tree diversity TP, Bye R, Lot A, Fa J, editors. Biological Diversity of Mexico: patterns in successive vegetation types along an elevation Origins and Distribution. Oxford, UK: Oxford University gradient in the Mountains of Eastern Mexico. Ecol Res 29: Press, pp. 447-458. 1097-1104. Olvera-Vargas M, Moreno-Gómez S, Figueroa B (1996). Sitios Trewin B (2007). Función de las normales climatológicas en un clima permanentes para la investigación silvícola. Manual para su cambiante. Ginebra, Colombia: Organización Meteorológica establecimiento. Libros del Instituto Manantlán. Universidad Mundial (in Spanish). de Guadalajara (in Spanish). UAAAN (1998). Programa de manejo de la zona sujeta a conservación Olvera-Vargas M, Figueroa-Rangel BL, Vázquez-López JM (2010). Is ecológica “Sierra de Zapalinamé”. Secretaría de Desarrollo there environmental differentiation in the Quercus dominated Social, Gobierno del estado de Coahuila. Saltillo, Coahuila: forests of west-central Mexico? Plant Ecol 211: 321-335. Universidad Autónoma Agraria Antonio Narro (in Spanish). Periódico Oficial (1996). Decreto del área natural protegida, con Vázquez GJA, Givnish TJ (1998). Altitudinal gradients in tropical carácter de Zona Sujeta a Conservación Ecológica, un área de forest composition, structure, and diversity in the Sierra de la serranía conocida como Zapalinamé. Periódico Oficial del Manantlán. J Ecol 86: 999-1020. Estado, Tomo CIII, No. 83, pp. 69-75 (in Spanish). Villaseñor JL (2016). Checklist of the native vascular plants of Portes VL (2001). Evaluación del cambio de uso de suelo y del paisaje Mexico. Rev Mex Biodivers 87: 559-902. regional en la sierra Zapalinamé. Soc Rur Prod Medio Amb 2: Zar JH (1984). Biostatistical Analysis. Englewood Cliffs, NJ. USA: 41-51 (in Spanish). Prentice Hall. Rahayu SS, Rodzay AW, Kamariah AS, Burslem DFRP (2012). Habitat associations and community structure of dipterocarps in response to environment and soil conditions in Brunei Darussalam, northwest Borneo. Biotropica 44: 595-605.

271 ENCINA-DOMÍNGUEZ et al. / Turk J Agric For

Appendix. Woody species registered in the oak forests of Sierra de Zapalinamé in northeastern Mexico (25°N).

Scientific name Species abbreviations Life form Preferential habitat

Agave gentryi B.Ullrich Aga gen Shrub Oak forest

Ageratina havanensis (Kunth) R.M.King & H.Rob. Age hav Shrub

Ageratina ligustrina (DC.) R.M.King & H.Rob. Age lig Shrub

Ageratina saltillensis (B.L.Rob.) R.M.King & H.Rob. Age sal Shrub

Arbutus xalapensis Kunth Arb xal Tree

Baccharis sulcata DC. Bac sul Shrub

Alloberberis eutriphylla (Fedde) C.C.Yu & K.F.Chung All eut Shrub

Buddleja cordata Kunth. Bud cor Shrub

Ceanothus caeruleus Lag. Cea cae Shrub

Cercis canadensis L. Cer can Shrub

Cornus stolonifera Michx. Cor sto Shrub

Crataegus baroussana Eggl. Cra bar Tree

Frangula betulifolia (Greene) Grubov Fra bet Shrub

Fraxinus cuspidata Torr. Fra cus Tree

Garrya glaberrima Wangerin Gar gla Shrub

Holodiscus discolor (Pursh) Maxim. Hol dis Shrub

Litsea parvifolia (Hemsl.) Mez Lit par Shrub

Lonicera pilosa (Kunth) Spreng. Lon pil Shrub

Prunus mexicana S.Watson Pru mex Tree

Prunus serotina Ehrh. Pru ser Tree

Quercus greggii (A.DC.) Trel. Que gre Tree

Quercus grisea Liebm. Que gri Tree

Quercus laceyi Small Que lac Tree

Quercus laeta Liebm. Que lae Tree

Quercus mexicana Benth. Que mex Tree

Quercus rugosa Née Que rug Tree

Quercus saltillensis Trel. Que sal Tree

Quercus sideroxyla Bonpl. Que sid Tree

Rhus aromatica Aiton Rhu aro Shrub

Salix lasiolepis Benth. Sal las Shrub

Salvia greggii A.Gray Sal gre Shrub

Salvia regla Cav. Sal reg Shrub

Smilax bona-nox L. Smi bon Shrub

Stevia berlandieri A.Gray Ste ver Shrub

Stevia ovata Willd. Ste ova Shrub

Ageratina calophylla (Greene) R.M.King & H.Rob. Age cal Shrub Pine forest

Ageratina scorodonioides (A.Gray) R.M.King & H.Rob. Age sco Shrub

Arctostaphylos pungens Kunth Arc pun Shrub

Pinus cembroides Zucc. Pin cem Tree

Pinus greggii Engelm. ex Parl. Pin gre Tree

1 ENCINA-DOMÍNGUEZ et al. / Turk J Agric For

Appendix. (Continued).

Scientific name Species abbreviations Life form Preferential habitat

Cupressus arizonica Greene Cup ari Tree Fir forest

Garrya ovata Benth. Gar ova Shrub

Paxistima myrsinites (Pursh) Raf. Pax myr Shrub

Populus tremuloides Michx. Pop tre Tree

Pseudotsuga menziesii (Mirb.) Franco Pse men Tree

Symphoricarpos microphyllus Kunth Sym mic Shrub

Alloberberis trifoliolata (Moric.) C.C.Yu & K.F.Chung All tri Shrub Montane chaparral

Bouvardia ternifolia (Cav.) Schltdl. Bou ter Shrub

Brickellia veronicifolia (Kunth) A.Gray Bri ver Shrub

Cercocarpus fothergilloides Kunth Cer fot Shrub

Cercocarpus montanus Raf. Cer mon Shrub

Chrysactinia mexicana A.Gray Chr mex Shrub

Gymnosperma glutinosum (Spreng.) Less. Gym glu Shrub

Helianthemum glomeratum (Lag.) Lag. Hel glo Shrub

Juniperus flaccida Schltdl. Jun fla Tree

Lindleya mespiloides Kunth Lin mes Shrub

Malacomeles denticulata (Kunth) G.N.Jones Mal den Shrub

Mimosa aculeaticarpa Ortega Mim acu Shrub

Purshia plicata (D.Don) Henrickson Pur pli Shrub

Quercus hypoxantha Trel. Que hyp Shrub

Quercus cordifolia Trel. Que cor Shrub

Quercus pringlei Seemen Que pri Shrub

Rhus virens Lindh. ex A.Gray Rhu vir Shrub

Agave asperrima Jacobi Aga asp Shrub Rosetophyllous scrub

Nolina cespitifera Trel. Nol ces Shrub

Opuntia engelmannii Salm-Dyck ex Engelm. Op eng Shrub

Opuntia stenopetala Engelm. Opu ste Shrub

Yucca carnerosana (Trel.) McKelvey Yuc car Shrub

Opuntia robusta J.C.Wendl. Opu rob Shrub Cultivated

2