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Highlights:
Naturally regenerated and planted seedlings were compared in Pinus patula stands.
Naturally regenerated seedlings had greater height (73.8 ± 12.29 cm) compared to planted seedlings (60.8 ± 12.39 cm).
Naturally regenerated seedlings had higher water potential (-0.90 MPa) compared to planted seedlings (-1.06 MPa).
Post-planting stress may have been a limiting factor in the growth of planted seedlings.
Introduction
Natural regeneration in forest stands under management is one of the most relevant silvicultural practices; to be successful it requires extensive knowledge of the factors involved in regeneration and making adequate site preparation (Nyland, Kenefic, Bohn, & Stout, 2016).
In Mexico, the seed tree regeneration method is applied in about 45 % of the forest area with a management program (Carrillo et al., 2017), while in some areas, the clear-cutting method with planting after cutting is applied. Successful works are known on natural regeneration using the parent tree method (Chacón-Sotelo, Velázquez-Martínez & Musálem, 1998; Hernández, Deras-Ávila, Deras-Ávila, & Colín, 2019); however, in many cases plantations are established after regeneration cutting and before to the growth season. This activity is not included in the rules for forest management in Mexico, because the use of forest plantations for a new stand is only considered when natural regeneration is not achieved after three years (Cámara de Diputados del H. Congreso de la Unión, 2005; Secretaría del Medio Ambiente y Recursos Naturales [SEMARNAT], 2006).
Several authors have evaluated seedling density after regeneration cutting (Castelán-Lorenzo & Arteaga-Martínez, 2009); the response of both naturally regenerated and planted seedlings after final cuts in even-aged stands (Kang, Shibuya, & Shin, 2014; Morales-González, López-Upton, Vargas-Hernández, Ramírez-Herrera, & Gil-Muñoz, 2013; Vargas & Vanegas, 2012; Yang, Yan, & Liu, 2014) and effects on different growth variables. Some studies indicate more growth and increase in biomass, height and diameter in seedlings from natural regeneration compared to planted seedlings after regeneration cutting, indicating that natural regeneration represents a productive alternative compared to planting (Fernández-Pérez, Ramírez-Marcial, & González-Espinosa, 2013; Hatzichristaki & Zagas, 2017; Otto, García-del-Rey, Méndez, & Fernández-Palacios, 2012; Pensado-Fernández, Sánchez-Velázquez, Pineda-López, & Díaz-Fleischer, 2014; Rebottaro & Cabrelli, 2007; Yang et al., 2014). On the other hand, in forested areas in Poland, a study by Dlugosiewicz, Zając, and Wysocka-Fijorek (2019) indicated that individuals established through planting on wet sites have better growth characteristics, despite the fact that natural regeneration of Pinus sylvestris L. is abundant; however, the authors consider that natural regeneration is the best option when site conditions are favorable, since the high maintenance costs that a plantation requires.
Immediate planting after harvest can be an expensive practice, especially because of nursery plant production and planting costs (Dlugosiewicz, Zając, Wysocka-Fijorek, & Sułkowska, 2019). Sometimes, field established seedlings show low survival and growth in subsequent years (Vargas & Vanegas, 2012). Post-planting stress of seedlings and low water availability are factors limiting success (Burney et al., 2015). In the ejido Carbonero Jacales located in the municipality of Huayacocotla, Veracruz, it has been observed that natural regeneration of Pinus patula Schltdl. & Cham. shows better characteristics and higher abundance compared to planted seedlings (Romo-Guzmán, Valtierra-Pacheco, González-Guillén, Valdez-Lazalde, & Vivar-Miranda, 2016). In this context, the present study evaluates both naturally regenerated and planted seedlings in P. patula stands, harvested during the period 2014-2016, with the objective of comparing the annual height and diameter growth, as well as diurnal water balance of plants.
Materials and Methods
Study site
The study was conducted in the ejido Carbonero Jacales, belonging to the Forest Management Unit (UMAFOR) 3013 "Sierra de Huayacocotla", located in the municipality of Huayacocotla, Veracruz, between the coordinates 20° 26’ 01’’ north and 98° 27’ 38’’ west (Figure 1). The region is located in the Sierra Madre Oriental. According to Köppen's climate classification, modified by García (2004), the climate in the region is temperate-humid [C(fm)] and sub-humid [C(w0)(w) and C(w2)]; the mean annual temperature is 14 °C with a mean annual precipitation of 1 333 mm (García, 2004).
According to the topographic map scale 1:50 000, the main soils are LVha+LVcr+ANmo/3 and CMcrlen+RGeulen/2, which correspond to luvisol and cambisol soils, respectively (Instituto Nacional de Estadística y Geografía [INEGI], 2009). The dominant arboreal vegetation is pine-oyamel-oak conifer forest (Romo et al., 2016).
Sampling sites
Annual growth of naturally regenerated (NR) and planted (PA) plants was compared in a paired manner through targeted sampling in three stands harvested in 2014, 2015, and 2016 using the seed tree method (Figure 1). The stands were relatively homogeneous in exposure, slope, and elevation (Table 1). A total of four sites of 100 m2 (10 m x 10 m) were selected at each stand, where NR and PA were present for paired comparison.
Plant measurements
Origin (NR or PA) and age of each P. patula seedlings was identified at each site. Natural regeneration (NR) was characterized by being randomly distributed, while planted seedlings were uniformly distributed. The age of naturally established seedlings was obtained by counting growth rings by destructive sampling at the end of the study for all individuals, and for planted seedlings, the age considered was that corresponding to the harvest year of the stand.
Annual height and diameter growth was recorded during the period June 2018 to June 2019. Values were obtained from 368 seedlings from the three stands under study: 123 in the stand harvested in 2014 (73 NR and 50 PA), 130 in the stand harvested in 2015 (76 NR and 54 PA) and 115 in the stand harvested in 2016 (66 NR and 49 PA). Total height was obtained with a stadia and diameter at the stem base using a digital Vernier (Truper® U.S.A).
At the end of the drought period in 2019 (27 to 29 May), diurnal variation in plant water balance was evaluated. For this purpose, water potential (Ψ) was determined with a pressure chamber (PMS Instruments® Model 1000) with the procedure recommended by Cleary, Zaerr, and Hamel (2003). Three sampling points (blocks nested in sites) were established at each site to reduce the effects of spatial variability, where a seedling from each origin (NR and PA) was located to allow paired comparison. Three daily measurements were made on the twigs of each individual sampled, with a total of six individuals per site (three NR and three PA): A total of 24 seedlings from the stand harvested in 2014 were measured on 27 May; 24 from the stand harvested on May 28, 2015; and 24 from the stand harvested on May 29, 2016. The first diurnal measurement was carried out before sunrise (4:00-6:30), when seedlings are more hydrated; the second measurement was at midday (12:00-14:00), when these reduce hydration level due to evapotranspiration; and the third measurement was in the afternoon (17:30-20:00) to evaluate the capacity for immediate recovery of the water deficit presented during the day.
From May to September 2019, soil samples were taken monthly to determine the moisture content using the gravimetric method (AS-05) of the NOM-021-SEMARNAT-2000 (SEMARNAT, 2002). Soil samples were taken at the center of the 12 sites located within the three stands, at a depth of 10 cm of mineral soil. Samples were collected with a Truper® garden shovel and placed in double Ziploc® brand bags to avoid water loss. The samples were transferred to the soil laboratory of the Soil Science Postgraduate Program of the Colegio de Postgraduados Campus Montecillo. Fresh weight of each sample was determined with an analytical balance to the nearest 0.01 g, dried at 105 °C for 24 hours in a drying oven and dry weight was recorded.
Statistical analysis
Hypothesis tests were performed to compare the means of the two plant origins (NR and PA) in height and diameter growth at the base of the stem, according to the age of the seedlings. Hypothesis tests were carried out with the statistical analysis package R, version 4.0.1. (R Development Core Team, 2015), by means of generalized linear mixed models (GLMM), using the Ime4 program; in addition, a comparison of means was performed using the least significant difference (LSD) with significance level α = 0.05. The analysis model included age (Xi) and origin (Oj) as fixed effect factors, and stand (Rk) and sampling site (Sl) as random effect factors. The model used was as follows:
where,
µ = overall mean
β = slope with the effect of the covariate age
Eijklm= error.
Water potential data (Ψ) was analyzed with a mixed-effects model with repeated measures, using the MIXED procedure of the SAS version V.9.4, for Windows (Statistical Analysis Systems Institute Inc., 2013). A Tukey's mean comparison test (α = 0.05) was also performed. The model included origin (Oi), time of day (Hj) and interaction (OHij) as fixed effects factors, and stand (Rk), site (Sl) and blocks (Bm) within them as random effects factors. The model used was the following:
where,
µ = overall mean
Eijklm= error.
Results and Discussion
Plant growth
The results indicate that height growth and basal stem diameter (Table 2) were significantly different (P < 0.05) between the two origins, after adjusting the data for seedling age. The average age was four years.
Table 2 Hypothesis test on the fixed effects of origin (naturally regenerated and planted seedlings) and age (4 years on average), for the variables of height and diameter growth at the base of the stem (DBS) in Pinus patula seedlings in the extension of the ejido Carbonero Jacales, Huayacocotla, Veracruz.
| Variable | Factor | Numerator DF | Denominator DF | F | P |
|---|---|---|---|---|---|
| Height | Origin | 1 | 354 | 9.99 | 0.0017 |
| Age | 1 | 354 | 46.2 | <0.0001 | |
| DBS | Origin | 1 | 354 | 23.9 | <0.0001 |
| Age | 1 | 354 | 67.16 | <0.0001 |
DF = degrees of freedom
Naturally regenerated seedlings had greater mean annual height growth (73.8 ± 12.3 cm) compared to planted seedlings (60.8 ± 12.4 cm) (Figure 2A). On the other hand, variation in height was lower for naturally regenerated seedlings than planted ones (Figure 2B), indicating greater consistency in growth of natural regeneration.
Figure 2 Comparison of annual height growth (A) and variability (B) in naturally regenerated (NR) and planted seedlings (PA) of Pinus patula in the extension of the ejido Carbonero Jacales, Huayacocotla, Veracruz. Different letters indicate significant differences (DMS; P = 0.05).
This trend has been observed by Rebottaro and Cabrelli (2007), who evaluated Pinus elliotii Engelm. seedlings and found that the annual height growth of planted seedlings (80 ± 19.2 cm) was lower compared to natural regeneration (143.2 ± 26.6 cm). On the other hand, Pensado-Fernández et al. (2014), in Perote, Veracruz, compared the annual height growth rate of Pinus seedlings and recorded higher growth for natural regeneration (1.55 ± 0.1 cm) compared to planted seedlings (1.1 ± 0.05 cm). Similar results of height growth in both origins of seedlings have been obtained by Otto et al. (2012) for Pinus canariensis C. Sm. ex DC. and by Fernández-Pérez et al. (2013) for Cupressus lusitanica Mill.
Natural regeneration also showed higher annual diameter growth (20.5 ± 3.5 mm) compared to planted seedlings (14.8 ± 3.5 mm) (Figure 3A). The trend is similar to that of height growth in terms of variability within each seedling origin (Figure 3B).
Figure 3 Comparison of annual diameter growth at the base of the stem (A) and variability (B) in naturally regenerated (NR) and planted seedlings (PA) of Pinus patula in the extension of the ejido Carbonero Jacales, Huayacocotla, Veracruz. Different letters indicate significant differences (DMS; P = 0.05).
Several authors have found a similar growth pattern in other species; that is, greater diameter growth for naturally regenerated seedlings compared to planted ones (Hatzichristaki & Zagas, 2017; Pensado-Fernández et al., 2014; Rebottaro & Cabrelli, 2007; Yang et al., 2014). The above could be explained by the fact that natural regeneration comes from the seed trees adapted to local environmental conditions and the advantage of increased taproot development from the moment seed germination occurs on site (Gómez-Cárdenas, Vargas-Hernández, Jasso-Mata, Velázquez-Martínez, & Rodríguez-Franco, 1998; Wakamiya-Noborio, Heilman, Newton, & Messina, 1999); therefore, seedlings have the same local adaptation characteristics as the parents, from a genetic and physiological point of view (Harrington, Brissette, & Carlson, 1989). In the case of the planted seedlings in the evaluated stands, it is not known if seeds comes from the same harvested stand.
In the case of natural regeneration, there is a selection process in the establishment stage, since, after germination, seedlings are exposed to various biotic and abiotic threats that limit their survival, causing only a few individuals to succeed. Moreover, competition for resources with herbaceous and shrub vegetation is high in the first years of natural regeneration (Castelán-Lorenzo & Arteaga-Martínez, 2009), which increases the intensity of natural selection (Długosiewicz et al., 2019). Seedling and sapling stages are the most critical stages in the life cycle of a woody plant (Padilla-Ruíz, 2008) and only the fittest individuals or those facing the least competition survive.
The better performance of natural regeneration can also be explained by the fact that it was established directly on the ground and, therefore, there is no post-planting stress stage, as is the case with seedlings produced in nursery and transplanted to the ground (Burney et al., 2015).
Water potential
The Ψ of seedlings from both origins showed significant differences (P ≤ 0.05) throughout the day and interaction origin*time of day (Table 3). Tukey's test confirms that differences in Ψ during the day are only apparent in the measurement at sunset (Figure 4).
Table 3 Hypothesis test on fixed effects of origin (natural regeneration and planted seedlings), time of day (5:00, 13:00 and 19:00 h) and interaction on the variable water potential of Pinus patula seedlings in the extension of the ejido Carbonero Jacales, Huayacocotla, Veracruz.
| Effect | Numerator DF | Denominator DF | F | P |
|---|---|---|---|---|
| Origin | 1 | 70 | 1.87 | 0.1758 |
| Time of day (h) | 2 | 140 | 282.36 | <0.0001 |
| Origin*time of day | 2 | 140 | 3.44 | 0.0347 |
DF = degrees of freedom.
The minimum values of Ψ at midday (-1.45 MPa) in the seedlings of the two origins are due to the effect of transpiration during the morning. The two types of seedlings recovered their water potential during the afternoon, according to the measurement made at sunset, which is a physiological response that has been widely documented, associated with a partial closure of stomata to reduce transpiration and increased water conduction within the plant (Agudelo-Castañeda, Cadena-Torres, Almanza-Merchán, & Pinzón-Sandoval, 2018; Moreno, 2009); however, naturally regenerated seedlings had higher efficiency in their evening recovery with average Ψ of -0. 90 MPa, while planted seedlings had an average Ψ of -1.06 MPa (Figure 4).
Figure 4 Water potential at different times of the day for naturally regenerated (NR) and planted seedlings (PA) of Pinus patula in the extension of the ejido Carbonero Jacales, Huayacocotla, Veracruz.
The greater recovery capacity of Ψ for the natural regeneration of P. patula may be associated with a more developed and efficient root system on soil water absorption (Aguilar-Muniz, Cruz-Medrano, Velázquez-Martínez, & Vargas-Hernández, 1992). The greatest efficiency could be due to a significant interaction with mycorrhizal fungi that increase the contact surface with soil matrix and water absorption capacity and nutrients from deeper layers (Demelash, Dejene, Oria de Rueda, Geml, & Martin-Pinto, 2020; South & Zwolinski, 1997).
Some studies have evaluated the repercussions on plant development and growth associated with reduced Ψ values (Luna-Flores, Estrada-Medina, Jiménez-Osornio, & Pinzón-López, 2012; Singh & Singh, 2006). Those studies conclude that when Ψ values close to -1.5 MPa are reached, light stress occurs, but as Ψ decreases, physiological stress in the plant gradually increases, resulting in stomata closure, reduced photosynthetic rate and, consequently, decreased growth.
On the other hand, several studies have analyzed the impact on seedling and sapling growth under different soil moisture conditions (Martiñón-Martínez, Vargas-Hernández, Gómez-Guerrero, & López-Upton, 2011; Martiñón-Martínez, Vargas-Hernández, López-Upton, Gómez-Guerrero, & Vaquera-Huerta, 2010; May-Lara, Pérez-Gutiérrez, Ruiz-Sánchez, Ic-Caamal, & García-Ramírez, 2011). Studies reveal there are conditions that favor seedling growth when moisture content is higher and acceptable levels of usable water are maintained.
In the present study, the lowest values of Ψ at midday (-1.45 MPa) were obtained during the period of greatest drought (May), when the average moisture content at a depth of 10 cm in the mineral soil was 31 % (Figure 5). In the following months, the average soil moisture gradually increased to 70 % in September.
Figure 5 Gravimetric soil moisture content, from the end of the dry season (May) to the first part of the summer rainy season (September), for Pinus patula stands sampled in the extension of the ejido Carbonero Jacales, Huayacocotla, Veracruz.
Variation in soil moisture content reflects the rainfall and climate pattern of the region. In September, moisture content in some sites almost tripled with respect to the values at the beginning of the sampling period in May. During the rainy period, the water potential of the seedlings was not evaluated, which limited the possibility of establishing seasonal differences in the water response. This allows us to assume that the greatest differences between the two origins of seedlings occur during the drought period. Studies by Moreno (2009) and Martiñón-Martínez et al. (2010, 2011) show that differences in water potential are more likely to be detected in woody plants during the drought period.
Conclusions
The natural regeneration of Pinus patula had greater annual height and diameter growth at the base of the stem compared to planted seedlings. This could be attributed to the fact that there was probably no plant selection during the nursery propagation process or adequate management in the plantation, which could have affected growth. Results suggest that natural regeneration has better physiological performance in root that allows faster recovery of diurnal water deficit in foliage, with respect to planted seedlings. Measuring water potential is the best way to indicate that planted seedlings had growth problems associated with post-planting stress because recovery was slower throughout the day.
