ISSN e: 2007-4018 / ISSN print: 2007-4018

English | Español

     

 
 
 
 
 
 
 
 

Vol. XXIII, issue 2 May - August 2017

ISSN: ppub: 2007-3828 epub: 2007-4018

Original article

Survival and growth of three Quercus species under contrasting coverage conditions in southern Mexico

http://dx.doi.org/10.5154/r.rchscfa.2017.01.001

Rivas-Rivas, Maximino B. 1 ; Ramírez-Marcial, Neptalí 1 * ; Perales, Hugo 1 ; Levy-Tacher, Samuel I. 1 ; Bonfil, Consuelo 2

  • 1El Colegio de la Frontera Sur. Carretera Panamericana y Periférico Sur s/n. C. P. 29290. San Cristóbal de Las Casas, Chiapas, México.
  • 2Universidad Nacional Autónoma de México, Facultad de Ciencias. Ciudad Universitaria, Circuito exterior s/n. C. P. 04510. Coyoacán, Ciudad de México, México.

Corresponding autor. Email: nramirezm@ecosur.mx

Received: January 02, 2017; Accepted: April 12, 2017

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

Abstract

Introduction:

Intensive use modifies the composition and structure of the forests of southern Mexico, limiting the natural repopulation of Quercus species.

Objective:

The feasibility of Quercus crispipilis, Q. ocoteifolia and Q. segoviensis in forest restoration was evaluated under three canopy conditions: secondary pine-oak forest, shrubland and grassland.

Materials and methods:

Survival, growth and biomass production of young plants of the three Quercus species were determined in three conditions, with three replications each, for 14 months. A total of 33 individuals of each species were transplanted per replication.

Results and discussion:

Survival was relatively high (> 88 %) in all three conditions. The relative growth rate (RGR) in height of Q. crispipilis and Q. ocoteifolia was higher under forest and shrubland conditions. RGR in basal diameter of the three species was higher under grassland conditions, as was the biomass of Q. crispipilis and Q. segoviensis roots.

Conclusions:

The presence of canopy influences the microclimatic variables of the sites. Quercus crispipilis and Q. segoviensis have higher survival and growth under shrubland and grassland conditions, while Q. ocoteifolia is favored under forest canopy.

Keywords:Chiapas highlands; pine-oak forest; Baccharis shrubland; induced grassland; forest restoration.

Introduction

Deforestation due to changes in land use and intensive use of some tree species modify the operation and structure of forest ecosystems, their recovery through natural processes is not always possible (Bustamante, Badano, & Pickett, 2012; Cayuela, Rey-Benayas, & Echeverría, 2006; Ramírez-Marcial, Camacho-Cruz, & González-Espinosa, 2008). At local level, changes are seen both under microclimatic and edaphic conditions and under the modification of other biotic interactions that affect seed germination and plant establishment (Bonfil & Soberón, 1999; Ramos-Palacios & Badano, 2014). Selective use of trees, at the highlands of Chiapas, has led to a reduction in the density and dominance of adult trees, mainly oaks (Quercus spp.), developing the regeneration and dominance of pines (Alba-López, González-Espinosa, Ramírez-Marcial, & Castillo-Santiago, 2003; Galindo-Jaimes, González-Espinosa, Quintana-Ascencio, & García-Barrios, 2002).

The restoration of degraded forest ecosystems is intended to restore their structure, function and productivity, as well as ecological processes and ecosystem services (Lamb, Stanturf, & Madsen, 2012; Stanturf, Palik, Williams, Dumroese, & Madsen, 2014; Torres-Miranda, Luna-Vega, & Oyama, 2011). Reforestation with multiple taxa is a viable option when woody species cannot be established naturally; this process allows to reconstruct the structure of the woody flora (Ramírez-Marcial et al., 2008).

Vegetation density, local abiotic environment conditions and existing disturbance regime are some factors that limit the establishment of species (Guo, Wang, Zhu, Wang, & Guo, 2011). For the purposes of restoration, it is necessary to understand the effect of climatic, edaphic and biotic conditions of the site on the survival and growth of the species used (Cardillo & Bernal, 2006; Pulsford, Lindenmayer, & Driscoll, 2016). Some Quercus species, due to their phenotypic plasticity, have potential to be used in forest restoration projects under different edaphic conditions (González-Espinosa et al., 2012) and canopy (Cardillo & Bernal, 2006; Ramírez-Marcial, Camacho-Cruz, González-Espinosa, & López-Barrera, 2006; Sánchez-Velásquez, Ramírez-Bamonde, Andrade-Torres, & Rodríguez-Torres, 2008). However, physical damage caused by grazing (Ramírez-Marcial, González-Espinosa, & García-Moya, 1996; Sánchez-Velásquez, Domínguez-Hernández, Pineda López, & Lara-González, 2011) water stress, degree of environmental disturbance, conditions of the substrate (Bonfil & Soberón, 1999; Flores-Cano, Badano, & Flores, 2012), and size and vigor of the seedlings (Bonfil, Rodríguez de la Vega, & Peña, 2000; Ramírez-Contreras & Rodríguez-Trejo, 2004) are factors that affect survival and growth.

An alternative that facilitates the establishment of the plants is the use of nurse shrubs or trees, since they improve microclimatic conditions and favor the initial growth (Bonfil & Soberón, 1999; Ramírez-Contreras & Rodríguez-Trejo, 2009; Ramírez-Marcial et al., 1996). Therefore, the yield analysis of plants along an environmental gradient, associated to human disturbance, allows to identify some barriers that prevent the establishment in sites with limited availability of propagules (Ramírez-Marcial et al., 2008; Ramos-Palacios & Badano, 2014).

The objective of this research was to evaluate the survival and growth of three oak species under three canopy conditions: forest, shrubland and grassland. The three species, characteristic of mountain ecosystems in southern Mexico and Guatemala, are in some category of endangered species (González-Espinosa, Meave, Lorea-Hernández, Ibarra-Manríquez, & Newton, 2011; Ramírez-Marcial et al., 2010). Quercus ocoteifolia Liebm., unlike Q. crispipilis Trel. and Q. segoviensis Liebm., is an evergreen species and requires canopy coverage conditions, cool temperatures and higher humidity for establishment (González-Espinosa et al., 2011; Gutiérrez & Trejo, 2014; Ramírez-Marcial et al., 2010). Therefore, the survival of Q. ocoteifolia is expected to be higher under forest canopy, while Q. crispipilis and Q. segoviensis have higher survival under more open canopy conditions.

Materials and methods

Study area

The study was carried out at the Parque Ecológico El Encuentro (PEE) located at the northeast portion of San Cristóbal de Las Casas (16° 43’ 54.72” - 16° 44’ 08.38” N and 92° 38’ 52.59” - 92° 38’ 24.52” W), at an average altitude of 2,270 m. The mean annual precipitation is 1,090.5 mm with an annual mean temperature of 15.0 °C (Comisión Nacional del Agua [CONAGUA], 2017). The PEE was under logging of Pinus for wood production and Quercus spp. and other broad-leaved species for firewood; it was also a sheep grazing site until 2010. The soil is moderately deep, derived from calcareous rocks and corresponding to Rendzina and Luvisol soils. The present vegetation includes secondary forests dominated by Pinus pseudostrobus Lindl., P. tecunumanii F. Schwerdtf. ex Eguiluz & J. P. Perry, Q. segoviensis, Q. crispipilis and Q. rugosa Née (De la Mora-Estrada, Ruiz-Montoya, Ramírez-Marcial, Morón-Ríos, & Mayorga-Martínez, 2017).

The study evaluated three canopy coverage conditions: pine-oak forest, Baccharis vaccinioides Kunth shrubland and grassland. A total of three plots of 100 to 150 m2 were established under each condition, which were considered experimental replications. The size varied according to the availability of the land, depending on the homogeneity of the coverage; grassland plots were the smallest and those of the forest were the largest. Conditions of canopy coverage, soil moisture and soil and air temperature were characterized in each plot. Canopy coverage was obtained from the analysis of six hemispherical photographs per plot, taken at 1 m height with a hemispherical lens (OptekaTM 0.20x, EUA) attached to a digital camera (Nikkon® modelo D5200, Singapur) and processed using the program HemiView (Rich, Wood, Vieglais, Burek, & Webb, 1999). Soil moisture and temperature were recorded by means of 20 readings per plot during the rainy season (October 2015) and 20 during the dry season (April 2016). Humidity was measured with Theta Meter® (model HH1, USA) and temperature with a digital dual-output thermometer J/K Extech Instruments® (model 421502, USA). Air temperature of each condition was continuously recorded one meter above the ground with a sensor HOBO TM® (Onset Computer Corporations, USA).

Plantation design

We used Q. crispipilis, Q. ocoteifolia and Q. segoviensis plants obtained from seeds collected in November and December 2013 and germinated in forest nurseries at El Colegio de la Frontera Sur (ECOSUR) in San Cristóbal de Las Casas. Quercus crispipilis and Q. segoviensis are found in Chiapas and Guatemala forming associations of pine-oak forests between 1,800 and 2,400 m, while Q. ocoteifolia is found in Oaxaca and Chiapas forming associations of pine-oak and cloud forest in wetter and cooler places, between 2,000 and 2,600 m (Ramírez-Marcial et al., 2010). Plants were kept for 15 months in the nursery and two months outside for their acclimatization. Root pruning in nursery was not applied. The three species were transplanted using a root ball during the last week of July 2015, to take advantage of the growth period (Ramírez-Marcial et al., 2006). A total of 33 plants per species were placed in each plot, randomly distributed at 1 m of equidistance. The amount per plot was determined based on the availability of plants of the three species studied.

Measurement variables

One week after transplantation, height and diameter of each plant were measured; these values were considered as the starting point of the experiment. Survival and growth assessments were repeated at 2, 4, 7, 9, 12, and 14 months after transplanting. Individual growth was measured through the maximum height and basal diameter of the stem. With these values, the relative growth rates (RGR) of both variables were calculated using the formula used by Hunt et al. (2002): RGR = [ln final growth (cm) - ln initial growth (cm)] / evaluation time (months).

At the end of the last evaluation (September 2016), biomass accumulated in stems, leaves and roots was quantified in a random sample of five plants per species and replication (a total of 135 plants). The collected plants were weighed per component; leaves, stem and root. Subsequently, the fractions were placed in an oven at 70 °C for 72 h for drying. At the end of this period, samples were weighed again using a scale with precision of 0.01 g, to obtain the dry weight.

Data analysis

A completely randomized design with 3 x 3 factorial arrangement (coverage and species type) was used. Compliance with the statistical assumptions of normality, homoscedasticity and independence was verified. Environmental variables among conditions were analyzed using the Kruskal-Wallis test; and comparison among pairs of coverage types, with the Wilcoxon rank test. The proportion of surviving plants was analyzed in each condition using the nonparametric Kaplan-Meier log rank test (Crawley, 2013). RGRs were analyzed, 14 months after transplantation, with ANOVA considering species and condition as main factors. Once significant differences among species (P < 0.05) were observed, another one-way ANOVA was used and the effect of the condition in each species was evaluated. Differences in biomass accumulated per fraction of each species, among conditions, were also evaluated with ANOVA. All analyzes were carried out using the program R version 3.2.2 (R Development Core Team, 2015).

Results and discussion

Microclimatic characteristics of sites

Table 1 shows the microclimatic conditions in the three coverage studied. The variables differed among transplant sites and seasons of the year; soil temperatures were significantly (P < 0.001) cooler in the forest. In autumn, soil moisture was similar (P = 0.32) in all three sites; however, at the beginning of spring, significant differences (P < 0.001) were observed with lower moisture in the shrubland compared to the forest and grassland.

Table 1. Temperature and percentage of soil moisture under three coverage conditions in San Cristóbal de Las Casas, Chiapas.

Microclimatic variable Period Coverage Kruskal-Wallis X 2 P Value
Forest Shrubland Grassland
Soil temperature (°C) October 2015 15.9 ± 0.05 a 16.6 ± 0.12 b 18.8 ± 0.08 c 122.03 P < 0.001
April 2016 18.2 ± 0.18 a 20.2 ± 0.20 b 22 ± 0.24 c 94.53 P < 0.001
Soil moisture (%) October 2015 64 ± 1.59 a 61 ± 1.83 a 65 ± 1.63 a 2.24 P = 0.32
April 2016 31 ± 1.43 a 23 ± 1.03 b 28 ± 1.47 a 12.93 P < 0.001
Different letters denote significant differences among coverage sites for each evaluation period (P < 0.001). ± standard error of the mean.

On the other hand, the mean air temperature was significantly lower (P < 0.05) in the forest and shrubland compared to the grassland (Figure 1). With regard to photosynthetically active radiation (PAR), the values were significantly (P = 0.05) higher for grassland, intermediate for shrubland and lower for forest (Figure 2).

Figure 1. Air temperature recorded at 1 m above ground level (October 2015-September 2016) in San Cristóbal de Las Casas, Chiapas. Each point corresponds to the average monthly value (± standard error). Different letters denote significant differences among coverages by means of the Wilcoxon test (P < 0.05), after the Kruskal-Wallis analysis.

Figure 2. Profile of the monthly distribution of photosynthetically active radiation under three conditions of coverage (January 2016-December 2016) in San Cristóbal de Las Casas, Chiapas. Different letters denote significant differences among coverage by means of the Wilcoxon test (P < 0.05). ± standard error of the mean.

The results indicate that the microclimatic conditions vary according to the type of cover, which can affect the yield of the plants (Dickson, 1990). The absence of canopy is reflected in higher temperature, radiation and evapotranspiration, leading to considerable soil stress and desiccation, and lower plant growth (Arosa, Ceia, Costa, & Freitas, 2015; Ramírez-Marcial et al., 2008).

Survival of Quercus

Species survival after 14 months of evaluation was high under all three study conditions (> 90 %), except for Q. ocoteifolia (88 %) under grassland conditions (Figure 3). The follow-up period of the study allows to affirming that Quercus species had the ability to establish itself effectively under the three conditions; however, these trends can be modified based on the seasonality or growth stage of the plants used (Alvarez-Aquino & Williams-Linera, 2012; Espelta, Riba, & Retana, 1995).

Figure 3. Survival curves of three Quercus species during a 14-month period from transplanting under forest, shrubland and grassland conditions in San Cristóbal de Las Casas, Chiapas. Different letters indicate significant differences among survival curves using the nonparametric Kaplan-Meier log rank test (P < 0.05).

Short-term studies have shown that survival is influenced by microclimatic conditions created by the presence of trees, shrubs and native species of early succession. Such conditions may modify microbial and microclimatic conditions of the soil (Castro, Zamora, & Hódar, 2006; Ramírez-Contreras & Rodríguez-Trejo, 2009), improving the yield of plants under canopy conditions (Avendaño-Yáñez, Sánchez-Velázquez, Meave, & Pineda-López, 2014; Bonfil et al., 2000; Camacho-Cruz, González-Espinosa, Wolf, & de Jong, 2000; Castro et al., 2006).

Growth of Quercus

RGR and biomass differed significantly (P < 0.001) among species and canopy coverage (Table 2), suggesting a differentiated effect of the microenvironmental situations of each condition.

Table 2. Analysis of variance of the relative growth rate (RGR) of height and diameter and biomass accumulated of three Quercus species (Q. ocoteifolia, Q. crispipilis and Q. segoviensis) established in three sites with different microenvironmental conditions (forest, shrubland and grassland) in San Cristóbal de Las Casas, Chiapas.

Factor Degrees of freedom RGR height RGR diameter Biomass
F P F P F P
Species 2 15.52 <0.001 13.82 <0.001 19.22 <0.001
Site 2 11.09 <0.001 71.53 < 0.001 17.85 <0.001
Species*Site 4 1.59 0.17 4.45 < 0.01 1.88 0.11

Figure 4 shows the RGR in height and diameter of the three Quercus species per coverage. RGR in height of Q. crispipilis and Q. ocoteifolia were higher in conditions with radiation and intermediate and low temperature (shrubland and forest). Quercus segoviensis had the lowest increase in RGR in height and showed no differences (P < 0.05) among sites. In the case of RGR in diameter, the three species increased at the site with the highest radiation (grassland) followed by shrubland and forest. This pattern was repeated in the accumulation of biomass in Q. crispipilis and Q. segoviensis, mainly in roots (Figure 5).

Figure 4. Relative growth rate (RGR) in height and diameter of Quercus species after 14 months of field growth in San Cristóbal de Las Casas, Chiapas. Different letters indicate significant differences among sites using the Tukey test (P < 0.05). ± standard error of the mean.

Figure 5. Biomass accumulated of three Quercus species grown under three coverage conditions (forest, shrubland and grassland) in San Cristóbal de Las Casas, Chiapas. Different letters indicate significant differences among sites, according to the Tukey test (P < 0.05). ± standard error of the mean (n = 45).

These results suggest a direct association between increased basal diameter and increased root biomass in Q. crispipilis and Q. segoviensis, in addition to an inverse relationship among RGR in height and basal diameter of Q. crispipilis and Q. ocoteifolia. The highest increases in height, in contrast to diameter, were associated with low and intermediate levels of solar radiation ranging from 5 to 50 % (Cardillo & Bernal 2006; Neufeld, 1983) and low temperature and humidity fluctuations under forest canopy (Padilla & Pugnaire, 2006; Ramírez-Contreras & Rodríguez-Trejo, 2009). Although light is considered a necessary resource for growth, increased radiation does not necessarily mean an increase in plant size (Espelta et al., 1995). The results indicate that, in oaks, the growth in basal diameter, associated with the increase in the radical biomass, is more common than the growth in height, shortly after transplanting, which coincides with that observed by Bonfil and Soberón (1999) and Kabeya and Sakai (2003).

The increase in biomass of each component (leaves, stem and root) of Q. crispipilis and Q. segoviensis was higher under grassland conditions compared to shrubland and forest conditions (Figure 5). The highest biomass increase in established plants at sites with higher solar radiation can be attributed to the fact that they suffer more stress, stem growth slows down and carbohydrates are distributed to lower parts (Dickson, 1990); in addition, under these conditions, plants reach higher photosynthetic rates (Feltrin et al., 2016; Kabeya & Sakay, 2003; Ramírez-Contreras & Rodríguez-Trejo, 2009). The component that reached the highest biomass was the root; the importance of this organ lies in the ability to store most of the carbohydrates the plant will use during periods of adverse conditions (Arosa et al., 2015, Kabeya & Sakay, 2003). The reserves stored in the roots allow oaks to regrow in case of death or partial removal of the aerial part (Bonfil & Soberón 1999; Cardillo & Bernal, 2006; Vázquez de Castro, Oliet, Puértolas, & Jacobs, 2014).

The three species of Quercus had high values of survival under the three experimental situations; although microclimatic variables are different among the studied conditions, it cannot be said that those are the only factors that affect survival, since herbivory and soil fertility can also influence them (Lei et al., 2013). As Q. crispipilis and Q. segoviensis showed higher biomass increases in the site with greater illumination, the use of these species in the restoration of abandoned grasslands is recommended; while Q. ocoteifolia would be more successful in restoring degraded secondary forests, because yield improves in the shade of forest canopy.

Conclusions

The presence of canopy influences the microclimatic variables of the sites; less coverage at the site will receive higher radiation and ambient and soil temperature. Despite the above, the survival of Q. crispipilis and Q. segoviensis was not affected by canopy coverage. As expected, relative growth rates of height and diameter changed according to the canopy coverage. The height of Q. crispipilis and Q. ocoteifolia was higher under forest and shrubland conditions; the diameter of the three species and the biomass of each component in Q. crispipilis and Q. segoviensis were higher under grassland, intermediate under shrubland and lower under the forest conditions. The three species seem to adapt to the different radiation conditions, temperature and humidity of each site. Quercus crispipilis and Q. segoviensis have better survival and growth responses under shrubland and grassland conditions, while Q. ocoteifolia is favored by the presence of forest canopy.

Acknowledgements

  • The authors wish to thank the Consejo Nacional de Ciencia y Tecnología for the scholarship granted to the first author to carry out his master's studies (No. 574853). To Mr. Noé Beltran, for the facilities and access to the study sites.

References

Alba-López, M. P., González-Espinosa, M., Ramírez-Marcial N. & Castillo-Santiago, M. Á. (2003). Determinantes de la distribución de Pinus spp. en la Altiplanicie Central de Chiapas, México. Boletín de la Sociedad Botánica de México, 73(2), 7-15. Retrieved from http://www.redalyc.org/pdf/577/57707301.pdf

Alvarez-Aquino, C., & Williams-Linera, G. (2012). Seedling survival and growth of tree species: site condition and seasonality in tropical dry forest restoration. Botanical Sciences, 90(3), 341-351.doi: 10.17129/botsci.395

Arosa, M. L., Ceia, R. S., Costa, S. R., & Freitas, H. (2015). Factors affecting cork oak (Quercus suber) regeneration: Acorn sowing success and seedling survival under field conditions. Plant Ecology and Diversity, 1(4), 1−12. doi: 10.1080/17550874.2015.1051154

Avendaño-Yáñez, M. L., Sánchez-Velásquez, L. R., Meave, J. A. & Pineda-López, M. R. (2014). Is facilitation a promising strategy for cloud forest restoration? Forest Ecology & Management, 329(8), 328-333. doi: 10.1016/j.foreco.2014.01.051

Bonfil, C., & Soberón, J. (1999). Quercus rugosa seedling dynamics in relation to its re-introduction in a disturbed Mexican landscape. Applied Vegetation Science, 2(2), 189-200. doi: 10.2307/1478982

Bonfil, C., Rodríguez de la Vega, H., & Peña, R. V. (2000). Evaluación del efecto de las plantas nodriza sobre el establecimiento de una plantación de Quercus L. Revista Ciencia Forestal en México, 25(1), 59-73. Retrieved from http://cienciasforestales.inifap.gob.mx/editorial/index.php/Forestales/article/view/18

Bustamante, R. O., Badano, E. I., & Pickett, S. T. A. (2012). Impacts of land use change on seed removal patterns of native and exotic species in a forest landscape. Community Ecology, 13(2), 171-177. doi: 10.1556/ComEc.13.2012.2.6

Camacho-Cruz, A., González-Espinosa, M., Wolf, J. H. D., & de Jong, B. H. J. (2000). Germination and survival of tree species in disturbed forests of the highlands of Chiapas, Mexico. Canadian Journal of Botany, 78(10), 1309-1318. doi: 10.1139/b00-103

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(1-3), 296-301. doi: 10.1016/j.foreco.2005.10.026

Castro, J., Zamora, R., & Hódar, J. A. (2006). Restoring Quercus pyrenaica forests using pioneer shrubs as nurse plants. Applied Vegetation Science, 9(1), 137-142. doi: 10.1658/1402-2001(2006)9[137:RQPFUP]2.0.CO;2

Cayuela, L., Rey-Benayas, J. M., & Echeverría, C. (2006). Clearance and fragmentation of tropical montane forests in the highlands of Chiapas, Mexico (1975-2000). Forest Ecology and Management, 226(1-3), 208-218. doi: 10.1016/j.foreco.2006.01.047

Comisión Nacional del Agua (CONAGUA). (2017). Normales climatológicas: Chiapas. Retrieved April 10, 2017 from http://smn1.conagua.gob.mx/index.php?option=com_content&view=article&id=174&tmpl=component

Crawley, M. J. (2013). The R Book (Second edition). West Sussex, United Kingdom: John Wiley & Sons.

De la Mora-Estrada, L. F., Ruiz-Montoya, L., Ramírez-Marcial, N., Morón-Ríos, A., & Mayorga-Martínez, M. C. (2017). Diversidad de chinches (Hemiptera: Heteroptera) en bosques secundarios de pino-encino de San Cristóbal de Las Casas, Chiapas, México. Revista Mexicana de Biodiversidad, 88(1), 86−105. doi: 10.1016/j.rmb.2017.01.016

Dickson, R. E. (1990). Assimilate distribution and storage. En A. S. Raghavendra (Ed.), Physiology of trees (pp. 51-85). New York, USA: Wiley and Sons.

Espelta, J. M., Riba, M., & Retana, J. (1995). Patterns of seedling recruitment in West-Mediterranean Quercus ilex forests influenced by canopy development. Journal of Vegetation Science, 6(4), 465-472. doi: 10.2307/3236344

Feltrin, R. P., Will, R. E., Meek, C. R., Masters, R. E., Waymire, J., & Wilson, D. S. (2016). Relationship between photosynthetically active radiation and understory productivity across a forest-savanna continuum. Forest Ecology and Management, 374(1), 51-60. doi: 10.1016/j.foreco.2016.04.049

Flores-Cano, J., Badano, E. I., & Flores, J. (2012). Effects of burial depth on seed germination and seedling emergence of Mexican oaks: A glasshouse experiment. Archives of Biological Sciences, 64(2), 1543-1554. doi: 10.2298/ABS1204543C

Galindo-Jaimes, L., González-Espinosa, M., Quintana-Ascencio, P., & García-Barrios, L. (2002). Tree composition and structure in disturbed stands with varying dominance by Pinus spp. in the highlands of Chiapas, México. Plant Ecology, 162(2), 259-272. doi: 10.1023/A:1020309004233

González-Espinosa, M., Meave, J. A., Lorea-Hernández, F. G., Ibarra-Manríquez, G., & Newton, A. C. (2011). The red list of Mexican cloud forest trees. Cambridge: Fauna & Flora International.

González-Espinosa, M., Meave, J. A., Ramírez-Marcial, N., Toledo-Aceves, T., Lorea-Hernández, F. G., & Ibarra-Manríquez, G. (2012). Los bosques de niebla de México: conservación y restauración de su componente arbóreo. Ecosistemas, 21(1), 36-52. Retrieved from http://www.revistaecosistemas.net/index.php/ecosistemas/article/viewFile/26/20

Guo, H., Wang, X. A., Zhu, Z. H., Wang, S. X., & Guo, J. C. (2011). Seed and microsite limitation for seedling recruitment of Quercus wutaishanica on Mt. Ziwuling, Loess Plateau, China. New Forests, 41(1), 127-137.

Gutiérrez, E., & Trejo, I. (2014). Efecto del cambio climático en la distribución potencial de cinco especies arbóreas de bosque templado en México. Revista Mexicana de Biodiversidad, 85(1), 179-188. doi: 10.7550/rmb.37737

Hunt, R., Causton, D. R., Shipley, B., & Askew, A. P. (2002). A modern tool for classical plant analysis. Annals of Botany, 90(4), 485-488. doi: 10.1093/aob/mcf214

Kabeya, D., & Sakai, S. (2003). The role of roots and cotyledons as storage organs in early stages of establishment in Quercus crispula: A quantitative analysis of the nonstructural carbohydrate in cotyledons and roots. Annals of Botany, 92(4), 537-45. doi: 10.1093/aob/mcg165

Lamb, D., Stanturf, J., & Madsen, P. (2012). What is forest landscape restoration? En J. Stanturf, D. Lamb, & M. Palle (Eds.), Forest landscape restoration (pp 3-24). Athens, Georgia, USA: Springer.

Lei, J. P., Xiao, W., Liu, J. F., Xiong, D., Wang, P., Pan L., Jiang Y., & Li, M. H. (2013). Responses of nutrients and mobile carbohydrates in Quercus variabilis seedlings to environmental variations using in situ and ex situ experiments. PLOS ONE, 8(4), e61192. doi: 10.1371/journal.pone.0061192

Neufeld, H. S. (1983). Effects of light on growth, morphology, and photosynthesis in Bald cypress (Taxodium distichum (L.) Rich.) and Pond cypress (T. ascendens Brongn.) seedlings. Bulletin of the Torrey Botanical Club, 110(1), 43-54. Retrieved from http://www.appstate.edu/~neufeldhs/publications/neuf1983.pdf

Padilla, F. M., & Pugnaire, F. I. (2006). The role of nurse plants in the restoration of degraded environments. Frontiers in Ecology and the Environment, 4(4), 196-202. doi: 10.1890/1540-9295(2006)004[0196:TRONPI]2.0.CO;2

Pulsford, S. A., Lindenmayer, D. B., & Driscoll, D. A. (2016). A succession of theories: Purging redundancy from disturbance theory. Biological Reviews, 91(1), 148-167. doi: 10.1111/brv.12163

R Development Core Team. (2015). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from http://www.R-project.org

Ramírez-Contreras, A., & Rodríguez-Trejo, D. A. (2004). Effect of seedling quality, aspect and microsite on a Quercus rugosa plantation. Revista Chapingo Serie Ciencias Forestales y del Ambiente, 10(1), 5-11. Retrieved from https://chapingo.mx/revistas/forestales/contenido.php?id_articulo=403&doi=&id_revista=3

Ramírez-Contreras, A., & Rodríguez-Trejo, D. A. (2009). Nurse plants in the reforestation with Pinus hartwegii Lindl. Revista Chapingo Serie Ciencias Forestales y del Ambiente, 15(1), 43-48. Retrieved from https://chapingo.mx/revistas/forestales/contenido.php?id_articulo=511&doi=&id_revista=3

Ramírez-Marcial, N., Camacho-Cruz, A., & González-Espinosa, M. (2008). Clasificación de grupos funcionales vegetales para la restauración del bosque mesófilo de montaña. En L. R. Sánchez-Velásquez, J. Galindo-González, & F. Díaz-Fleischer (Eds.), Ecología, manejo y conservación de los ecosistemas de montaña en México (pp. 51-72). México: Mundi Prensa.

Ramírez-Marcial, N., Camacho-Cruz, A., González-Espinosa, M., & López-Barrera, F. (2006). Establishment, survival and growth of tree seedlings under successional montane oak forests in Chiapas, Mexico. In M. Kappelle (Ed.), Ecology and conservation of neotropical montane oak forests (pp. 177-189). Berlin: Springer. doi: 10.1007/3-540-28909-7_14

Ramírez-Marcial, N., Camacho-Cruz, A., Martínez-Icó, M., Luna-Gómez, A., Golicher, D., & González-Espinosa, M. (2010). Árboles y arbustos de los bosques de montaña en Chiapas. San Cristóbal de Las Casas, Chiapas, México: El Colegio de la Frontera Sur.

Ramírez-Marcial, N., González-Espinosa, M., García-Moya, E. (1996). Establecimiento de Pinus spp. y Quercus spp. en matorrales y pastizales de Los Altos de Chiapas, México. Agrociencia, 30(2), 249-257.

Ramos-Palacios, C. R., & Badano, E. I. (2014). The relevance of burial to evade acorn predation in an oak forest affected by habitat loss and landscape use changes. Botanical Sciences, 92(2), 299-308. doi: 10.17129/botsci.101

Rich, P. M., Wood, J., Vieglais, D. A., Burek, K., & Webb, N. (1999). HemiView user manual. Retrieved from ftp://ftp.dynamax.com/manuals/HemiView_Manual.pdf

Sánchez-Velásquez, L. R., Domínguez-Hernández, D., Pineda-López, M. R., & Lara-González, R. (2011). Does Baccharis conferta shrub act as a nurse plant to the Abies religiosa seedling? The Open Forest Science Journal, 4(1), 67-70. doi: 10.2174/1874398601104010067

Sánchez-Velásquez, L. R., Ramírez-Bamonde, E. S., Andrade-Torres, A., & Rodríguez-Torres, P. (2008). Ecología florística y restauración del bosque mesófilo de montaña. En L. R. Sánchez-Velásquez, J. Galindo-González, & F. Díaz-Fleischer (Eds.), Ecología, manejo y conservación de los ecosistemas de montaña en México (pp. 9-50). México: Mundi Prensa .

Stanturf, J. A., Palik, B. J., Williams, M. I., Dumroese, R. K., & Madsen, P. (2014). Forest restoration paradigms. Journal of Sustainable Forestry, 33, S161−S194. doi: 10.1080/10549811.2014.884004

Torres-Miranda, A., Luna-Vega, I., & Oyama, K. (2011). Conservation biogeography of red oaks (Quercus, Section Lobatae) in Mexico and Central America. American Journal of Botany, 98(2), 290-305. doi: 10.3732/ajb.1000218

Vázquez de Castro, A., Oliet, J. A., Puértolas, J., & Jacobs, D. F. (2014). Light transmissivity of tube shelters affects root growth and biomass allocation of Quercus ilex L. and Pinus halepensis Mill. Annals of Forest Science, 71(1), 91-99. doi: 10.1007/s13595-013-0335-3

Figures:

Figure 1. Air temperature recorded at 1 m above ground level (October 2015-September 2016) in San Cristóbal de Las Casas, Chiapas. Each point corresponds to the average monthly value (± standard error). Different letters denote significant differences among coverages by means of the Wilcoxon test (P < 0.05), after the Kruskal-Wallis analysis.
Figure 2. Profile of the monthly distribution of photosynthetically active radiation under three conditions of coverage (January 2016-December 2016) in San Cristóbal de Las Casas, Chiapas. Different letters denote significant differences among coverage by means of the Wilcoxon test (P < 0.05). ± standard error of the mean.
Figure 3. Survival curves of three Quercus species during a 14-month period from transplanting under forest, shrubland and grassland conditions in San Cristóbal de Las Casas, Chiapas. Different letters indicate significant differences among survival curves using the nonparametric Kaplan-Meier log rank test (P < 0.05).
Figure 4. Relative growth rate (RGR) in height and diameter of Quercus species after 14 months of field growth in San Cristóbal de Las Casas, Chiapas. Different letters indicate significant differences among sites using the Tukey test (P < 0.05). ± standard error of the mean.
Figure 5. Biomass accumulated of three Quercus species grown under three coverage conditions (forest, shrubland and grassland) in San Cristóbal de Las Casas, Chiapas. Different letters indicate significant differences among sites, according to the Tukey test (P < 0.05). ± standard error of the mean (n = 45).

Tables:

Table 1. Temperature and percentage of soil moisture under three coverage conditions in San Cristóbal de Las Casas, Chiapas.
Microclimatic variable Period Coverage Kruskal-Wallis X 2 P Value
Forest Shrubland Grassland
Soil temperature (°C) October 2015 15.9 ± 0.05 a 16.6 ± 0.12 b 18.8 ± 0.08 c 122.03 P < 0.001
April 2016 18.2 ± 0.18 a 20.2 ± 0.20 b 22 ± 0.24 c 94.53 P < 0.001
Soil moisture (%) October 2015 64 ± 1.59 a 61 ± 1.83 a 65 ± 1.63 a 2.24 P = 0.32
April 2016 31 ± 1.43 a 23 ± 1.03 b 28 ± 1.47 a 12.93 P < 0.001
Different letters denote significant differences among coverage sites for each evaluation period (P < 0.001). ± standard error of the mean.
Table 2. Analysis of variance of the relative growth rate (RGR) of height and diameter and biomass accumulated of three Quercus species (Q. ocoteifolia, Q. crispipilis and Q. segoviensis) established in three sites with different microenvironmental conditions (forest, shrubland and grassland) in San Cristóbal de Las Casas, Chiapas.
Factor Degrees of freedom RGR height RGR diameter Biomass
F P F P F P
Species 2 15.52 <0.001 13.82 <0.001 19.22 <0.001
Site 2 11.09 <0.001 71.53 < 0.001 17.85 <0.001
Species*Site 4 1.59 0.17 4.45 < 0.01 1.88 0.11