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Revista Facultad Nacional de Agronomía Medellín

Print version ISSN 0304-2847On-line version ISSN 2248-7026

Rev. Fac. Nac. Agron. Medellín vol.72 no.1 Medellín Jan./Apr. 2019

https://doi.org/10.15446/rfnam.v72n1.69575 

Artículos

Survival, growth and photosynthesis analysis of native forest species established in the tropical dry forest in Antioquia, Colombia

Análisis de supervivencia, crecimiento y fotosíntesis de especies forestales nativas en el bosque seco tropical en Antioquia, Colombia

Nora Isabel Bravo Baeza1 

Luis Fernando Osorio Vélez1 

Felipe Bravo Oviedo2 

Enrique Martínez Bustamante1 

1 Facultad de Ciencias Agrarias. Universidad Nacional de Colombia. AA 1779, Medellín, Colombia. <noraisabelbb@gmail.com>

2 Universidad de Valladolid. C/Plaza de Santa Cruz, 8, 47002 Valladolid, España.


ABSTRACT

The tropical dry forest (TDF) is one of the most affected ecosystems by anthropic activities in the world; so, it is necessary to study the dynamics of its ecosystem in order to restore it. With the aim of determining the survival, development, and photosynthetic behaviors of forest species at a young age, a field study was performed using three species Cedrela odorata L. (Spanish cedar), Pachira quinata (Jacq.) W.S. Alverson (red ceiba) and Ochroma pyramidale (Cav. ex Lam.) Urb. (balsa) species. Field data were collected in different periods whose climatic conditions were: dry period (S.0), first rainy period (Ll.1), first dry period (S.1), second rainy period (Ll. 2), and second dry period (S.2). The total height (H) and the root collar diameter (RCD) were measured repeatedly, and two harvests were made to measure dry weight. Besides, photosynthetic performance and its effect on the species development species during three contrasting rainfall periods was evaluated by measuring photosynthetically active radiation (PAR), stomatal conductance (gs), intercellular carbon (Cint), net photosynthesis (NP), transpiration (trans), efficient water use (EWU) and efficient light use (ELU) from 8:00 and 17:00 h during the day. Analysis of variance was performed obtaining significant differences (P<0.05) in the interaction time×species regarding variables H and RCD, and the photosynthetic variable NP. The gs and trans variables showed statistical significance with the species and rainfall periods; Cint was significant only for the rainfall periods. The species O. pyramidale presented the best survival and tolerance to weather by adapting physiological mechanisms, while C. odorata was the most affected species by climatic conditions concerning overall survival.

Keywords: Cedrella odorata L; Efficient light use; Efficient water use; Ochroma pyramidale (Cav. Ex Lam.); Pachira quinata Jacq

RESUMEN

El Bosque seco tropical es uno de los ecosistemas más afectados en el mundo por el desarrollo de actividades antrópicas, por lo que es necesario estudiar las dinámicas de su ecosistema con el fin de restaurarlo. Con el objetivo de determinar la supervivencia, desarrollo y comportamiento fotosintético de las especies forestales en edades tempranas, se realizó un estudio de campo con tres especies: Cedrela odorata L. (cedro rojo), Pachira quinata (Jacq.) W.S. Alverson (ceiba tolúa) y Ochroma pyramidale (Cav. ex Lam.) Urb. (balso). Los datos de campo fueron recolectados en diferentes períodos, cuyas condiciones climáticas fueron: período seco (S.0), primer período lluvioso (Ll.1), primer período seco (S.1), segundo período lluvioso (Ll.2) y segundo período seco (S.2). Se midió la altura total (H) y el diámetro en la base (RCD), y se realizó dos cosechas para medir el peso seco. Además, se evaluó el funcionamiento fotosintético y su efecto en el desarrollo de las especies en tres periodos pluviométricos contrastantes midiendo la radiación fotosintéticamente activa (PAR), conductancia estomática (gs), carbono intercelular (Cint), fotosíntesis neta (PN), transpiración (trans), uso eficiente del agua (EWU) y uso eficiente de la luz (ELU) entre las 8:00 y 17:00 h del día. Así mismo, se realizaron dos cosechas, para la medición del peso seco. Se realizó un análisis de varianza, encontrando diferencias significativas (P<0.05) en la interacción en H y RCD, y en la variable fotosintética PN. Las variables gs y trans mostraron significancia estadística con las especies y los periodos pluviométricos; Cint fue significativa sólo en los periodos pluviométricos. O. pyramidale fue la especies que mayor supervivencia presentó y toleró las condiciones climáticas desarrollando mecanismos fisiológicos, mientras que C. odorata fue la especies más afectada en términos de supervivencia por las condiciones climáticas.

Palabras clave: Cedrella odorata L; Uso eficiente de la luz; Uso eficiente del agua; Ochroma pyramidale (Cav. Ex Lam.); Pachira quinata Jacq

The dry tropical forest (TDF) consists of continuous forest cover and is found in regions with an average annual temperature higher than 27 °C and average annual precipitation of 1058 mm (Stoner and Sánchez-Azofeifa, 2009). The dry tropical forest is one of the ecosystems most threatened by anthropic activities because its soils are fertile and well-suited for agriculture (Calvo-Alvarado et al., 2009; Quesada et al., 2009). It is estimated that 48.5% of the world’s TDF have been used for different purposes than its conservation (Portillo-Quintero and Sánchez-Azofeifa, 2010). These disturbances have given rise to plant distinct covers from those naturally found in TDF because natural regeneration processes do not ensure a return to the original state (Griscom and Ashtom, 2011). Nearly 1,000,000 km2 of the world’s remaining TDF is threatened by the expansion of human populations, habitat fragmentation, and climate change, and just 30% of TDFs are protected under conservation regimes (Fajardo et al., 2013). Besides, 350 million ha have been deforested, and another 500 million ha of primary and secondary forest has been degraded (Lamb et al., 2005). Restoration and replanting native species are strategies that can guarantee the continued provision of environmental goods and services, in addition to protecting and recovering native flora (Bastien-Henri et al., 2010). These strategies have produced positive results, including the recovery of soils and nutrients and the establishment of plant cover and water balance in degraded areas (dos Santos et al., 2006).

Nevertheless, one of the metrics governing whether a plantation or reforestation program is successful is the survival of plants species and its growth and development time because these characteristics depend mainly on the source of seeds, the environmental requirements, and microclimatic conditions (Allen et al., 2010). The establishment of species and provenance trials has become a forestry tool that enables the development of programs aimed at genetic improvement for the propagation of species at determined sites, ensuring the quality of the conservation effort. At the same time, these trials provide information about species potential for use in the plant recovery of degraded areas.

Various experiments involving native species in tropical countries have been performed, and interest in this subject has grown due to the lack of information about which species will contribute most to the success of reforestation and restoration programs (Niinemets and Valladares, 2006). Despite the wide diversity of species found in tropical forests, commercial reforestation programs most commonly utilize exotic species. The most frequently used genera in the tropical Americas are Tectona, Eucalyptus, Pinus, and Acacia (Bastien-Henri et al., 2010; van Breugel et al., 2011). This common practice is because there is a risk to utilize new species when little is known about its management or its growth and survival rate under natural conditions (dos Santos et al., 2006).

Species such as Cedrela odorata, Pachira quinata, and Ochroma pyramidale, which are native to the tropical Americas, are known for their high commercial value. However, little information is available regarding their development and adaptation to the climatic conditions of TDF, where seasonal variations are marked by intense dry periods alternated with rainy periods, the latter of which is decisive for the growth, phenology and photosynthetic response of the plants in TDF (Eamus, 1999).

Microclimatic factors such as temperature, water availability, and relative humidity can generate stress for plants that directly impacts their physiological and photosynthetic development (Marenco et al., 2003; Briceño, 2017). For this reason, plants have developed diverse adaptation strategies; the results of which are manifested in growth, reproduction, survival, abundance, and geographical distribution (Cai et al., 2009; Araque et al., 2009; Esmail and Oelbermann, 2011).

With the progressive disappearance of TDF at a global level, it is necessary to obtain a better understanding of the effects of extreme climatic factors on the early establishment of native forest species and to identify the ecological requirements of these plants (Stoner and Sánchez-Azofeifa, 2009). The objective of the study was to advance the monitoring of three species in their survival, dasometric parameters, and gaseous exchange of foliage in TDF conditions in contrasting rainfall periods.

MATERIALS AND METHODS

Study area

This research was performed as part of the forest species test carried out in the project “Study of the recovery of degraded areas in the dry tropical forest, Olaya municipality.” Founded by the Inter-administrative Agreement 8787 of 2010, which included the Universidad Nacional de Colombia-Sede Medellín and the Corporación Autónoma Regional de Antioquia (Corantioquia). The study was developed at the Tribio Mamey ranch located in the Sucre township, Olaya municipality, Antioquia department (6°35´33.72”N, 75°47´33.70”W) (Colombian Andean region), between 540 and 680 m of altitude. The Sucre township registers an average annual rainfall of 1058 mm and an average temperature of 27.1 °C (registering minimum temperatures of 21 °C and maximum temperatures of 40.5 °C) which places it in the dry tropical forest life zone.

During the first half of the year, rainfall occurs in April and May, with the highest amount registered in April, and temperatures reaching 37 °C. The second rainy period occurs in September and October, with the highest levels of precipitation in October. The periods with dry tendencies in the first half of the year occur during January and February, which register the highest temperatures of the year (38 °C); in the second half of the year, the dry periods occur in June and July, with temperatures between 37 and 38 °C. In December, rainfall decreases, and the temperature begins to rise (IDEAM, 2013).

Species, characteristics of the plots and evaluated variables

Between March 2011 and February 2013, the inter-administrative study was carried out with 11 native species of the TDF (Table 1), in an area of 23.66 ha. From this species, P. quinata, C. odorata, and O. pyramidale were selected because they have a high potential to be used in reforestation and restoration processes, which were followed up on their gas exchange and dasometric characteristics. Each species was planted over an area of one hectare distributed randomly in four complete blocks of 2,500 m2 at a planting density of 3×3 m (i.e., 1,100 tree ha-1). At the beginning of the study, the land was cleared manually with a machete, and the trees and shrubs growing as a part of natural regeneration processes were left intact. A maintenance procedure consisting of clearing one-meter radius around each plant with a machete was performed every six months. A circular plot of 250 m2 was established in the center of each block with an average of 28 specimens per plot; each specimen was identified and labeled. C. odorata seeds were provided by Corantioquia and were originally obtained in the Andean region of Colombia, while Balsur and Monterrey Forestal Ltda. companies provided the O. pyramidale and P. quinata seeds, respectively. Both came from Colombia’s Atlantic region. Seed handling and the chosen pretreatments for optimal germination were based on standard recommendations for these species.

Table 1 Species used in the study Inter-Administrative Agreement 8787 of 20101

Data were collected in the following periods, whose climatic conditions were: dry period S.0 (Marzo 2011), rainy period Ll.1 (Apri-May 2012), dry period S.1 (June-September 2012), rainy period Ll.2 (October-November 2012) and dry period S.2 (January-February 2013). The last period was not considered in the analysis of photosynthesis data due to the defoliation of the C. odorata and P. quinata species. During each of these periods, the species was 13 (Ll.1), 17 (S.1), 21 (Ll.2) and 23 (S.2) months old; where the total height (H) and the root collar diameter (RCD) were measured, repeatedly. A count of standing specimens was taken during each round of data collection to perform a survival analysis, and the percentage of survival for each rainfall period was determined (Ll.1, S.1, Ll.2, and S.2).

The following photosynthetic variables: photosynthetically active radiation, PAR (µmol m-2 s-1), stomatal conductance, gs (mmol m-2 s-1), intercellular carbon, Cint, net photosynthesis, NP (µmol m-2 s-1), and transpiration, trans (mmol m-2 s-1), were measured simultaneously between 8:00 and 17:00 h (Ellis et al., 2000; Krause et al., 2001; Marenco et al., 2003; Juhrbandt et al., 2004; Araque et al., 2009). A healthy mature leaf in the upper third of the canopy was selected for each using an infrared gas analyzer (IRGA, TPS - 2 PPSYSTEMS). Efficient water use (EWU) and efficient light use (ELU) (Larcher, 1995; Lambers et al., 2008) were calculated using the equations:

The total height (H) of each specimen was measured with a tape, measuring from the base of the tree to the terminal bud (in the cases for which this was not possible, height was measured up to the highest leaf) and the root collar diameter (RCD) was measured at the height of 5 cm from the ground.

For the collection of biomass data, two specimens were harvested manually from each plot: one at the beginning of data collection (April-May 2012) and the other at the end (January-February 2013). In the field, the specimens were divided into the stem, leaves, and roots (primary and secondary). The samples were incubated at 60 °C until they reached a constant weight to determine their dry weight (g) in the Ecology Laboratory - Biogeochemical Area of the Faculty of Agricultural Sciences of the Universidad Nacional de Colombia - Sede Medellín.

Statistical design

To determine the behavior of the dasometric and photosynthetic variables between rainfall periods (Ll.1, S.1, and Ll.2) and species, an analysis of variance was performed, adjusting the first-order autoregressive covariance structure (type=arh(1)) through the use of mixed models. In the factorial structure (Time×Treatment). Time represents each of the stages of the bimodal regime in which the measurements were taken, and Treatment represents each of the three species. Significant differences (P<0.05) were determined using the Fisher test (Least Significant Difference). The assumption of normality was confirmed using the Kolmogorov-Smirnov test (Pr>D). The statistical program SAS® 9.2 (SAS Institute Inc. 2004) was used.

RESULTS AND DISCUSSION

Survival and growth of the species in TDF climate conditions

During the first rainy period (Ll.1, 13 months old), the three species presented similar averages of survival (94 and 99%), C. odorata species registered the lowest values. During the final period, C. odorata registered the lowest survival rate (15%), P. quinata registered 42%, and O. pyramidale registered 55% (Figure 1). After thirteen months, the three species showed similar behaviors in Ll.1 with high levels of survival. O. pyramidale was the species that shows the highest percentage of survival during periods S.1 and Ll.2, identical to the findings of Craven et al. (2007) with the same species in a dry tropical forest. These results also confirm that O. pyramidale is species that easily acclimate to weather variation (Oberbauer and Strain, 1984; Kitajima, 1994; Krause et al., 2001). Besides, many perennial species growing in dry climates avoid the effects of drought conditions by developing a deep root system that allows them to capture water in soil zones that are sometimes close to the phreatic stratum (Castellanos and Newton, 2015). Moreover, water deficiency is an important environmental limit that is related to the physiological processes involved in the growth and development of plants. It influences a set of responses to the sequence that mainly affects the mechanism of gas exchange (Centritto et al., 2009).

Figure 1 Survival (%) for three species during rainy period (Ll.1, April-May 2012), dry period (S.1, June-September 2012), rainy period (Ll.2, October-November 2012) and dry period (S.2, January-February 2013). 

There were significant differences in the interaction time×species in height (P<0.0002) and diameter (P<0.0003). The species that registered the greatest height was O. pyramidale, which reached 180 cm during the final period (S.2), followed by P. quinata at 68.55 cm and C. odorata at 50.74 cm. Regarding diameter, at 23 months after planting (S.2), O. pyramidale had the greatest diameter of 3.43 cm, while P. quinata registered a diameter of 1.43 cm and C. odorata of 1.01 cm.

The accumulation of total biomass of the species under study was 1,787.87 g in O. pyramidale, 795.61 g for P. quinata, while C. odorata had a biomass of 222.60 g (Table 2).

Table 2 Height, diameter and biomass of the three species during S.0 dry period (March 2011), rainy period (Ll.1, April-May 2012), dry period (S.1, June-September 2012), rainy period (Ll.2, October-November 2012) and dry period (S.2, January-February 2013). 

O. pyramidale also presented greater growth both in diameter and in height, supporting the findings of Wishnie et al. (2007) in the dry zones of Panama, where they reported higher annual growth in height and diameter for O. pyramidale than for C. odorata and P. quinata. Similarly, during the Ll.1 rainy period, this species registered greater leaf production, which agrees with the findings of dos Santos et al. (2006), who reported that in conditions of high solar radiation, some species make optimal use of light energy, transforming it into ATP to increase their biomass.

Site conditions had a greater influence on the survival of C. odorata, and confirm the reported by Gerhardt (1998) because, under dry conditions with a controlled supply of water, this species increases its survival in the field. C. odorata also displayed low levels of survival in plantation trials performed on Ecuadorian pastureland, Davidson et al. (1998) reported low survival rates for C. odorata (less than 50%) in the dry zones; however, with water supply, the death of the species notably decreased. Similarly, Esmail and Oelberman (2011) reported that C. odorata seedlings that were constantly irrigated when exposed to high-temperature conditions (34 °C) exhibited an improvement in growth response regarding height and biomass.

Between the three species, it was observed that C. odorata showed total defoliation during the dry periods, in addition to low foliar mass production during the rainy periods. As a result, their accumulated total biomass was low during the study period. This behavior happens because the decrease in the foliar area is one of the strategies employed by plants to counteract the stress caused by a lack of water (Lambers et al., 2008). Along these lines, in Panama, Craven et al. (2007) found that species such as C. odorata maintained low leaf area and growth levels, leading to the conclusion that these plants invested more energy into withstanding stressful conditions than into accumulating biomass.

P. quinata species has been adapted to weather conditions, and it is resistant to low rainfall rates, which facilitated its establishment in this degraded area. In the dry regions, low mortality values have been reported for P. quinata (Hall et al., 2011). At the same time, Kane et al. (1993) noted that this species maintains considerable reserves of starch in its root system, which allow it to have a rapid initial growth at the beginning of the rainy season. Consistently, an increase in growth rate was observed during the Ll.1 period. The strategy employed by the plant was the reduction of its leaf biomass during the dry periods to combat hydric stress. According to Eamus (1999), stomatal sensibility in caducipholic plants increases with soil dryness, and a result attributed to the decrease in elasticity of their cell walls that in turn results in a high propensity to the loss of turgidity. P. quinata specimens exhibited the greatest diameter, coinciding with the findings of Wishnie et al. (2007) in a study of 24 species with restoration potential and commercial value. P. quinata is a species that acclimate to conditions of high solar radiation and low humidity (Kane et al., 1993). Although soil fertility was not evaluated in the present research, it could be a factor that impacts its growth (Hall et al., 2011). O. pyramidale performed the best in terms of height due to the ease with which it acclimates (Krause et al., 2001). The results obtained are consistent with the findings of Wishnie et al. (2007) in Panama in a study of TDF species that also included C. odorata and P. quinata. These findings also confirm that O. pyramidale is a fast-growing species that acclimate well to dry areas.

Photosynthetic behavior of the species studied

It must be considered the importance of the leaves does not exclusively lie in carrying out the photosynthetic process. They are involved in nutrient storage and photoassimilate process, and as sources of nutrients in the processes of metabolic remodeling during organ senescence (Severino and Auld, 2013). In their early stages, the seedlings developed physiological mechanisms that allowed them to increase CO2 assimilation during the dry period. Water deficiency is an important environmental limitation that affects all the physiological processes involved in the growth and development of plants. It influences a set of responses to the drought that mainly affects the mechanism of gas exchange (Centritto et al., 2009). The stomatal regulation of transpiration and intercellular carbon concentration during dry periods did not decrease the CO2 assimilation rate; for optimal control of stomata to manage hydraulic risk is likely to have significant consequences for ecosystem fluxes during drought, which is critical given projected intensification of the global hydrological cycle (Anderegg et al., 2018).

The foliage response of these three species had a relationship with the climate. In such a way that stomatal regulation was identified as the rainfall was presented with stomata partially open until almost closed depending on the species. Thus, during the rainy periods, O. pyramidale and C.odorata showed partially open stomata, regardless of whether they were, although in a different degree of openness. On the contrary, P.quinata remained with the stomata partly or almost closed in the two climatic seasons (Table 3).

Table 3 Foliage response to the gaseous exchange of the three species during dry period (S.0, March 2011), rainy period (Ll.1, April-May 2012), dry period (S.1, June-September 2012), rainy period (Ll.2, October-November 2012) and dry period (S.2, January-February 2013). 

According to Berry et al. (2010), plants with better control of stomatal function are more efficient in the use of water and have more tolerance to the drought. It is indicative that stomatal control is an important adaptive mechanism of tolerance to the drought in this species (dos Santos et al., 2017). The partial closure of the stomata is a known strategy of plant tolerance to water stress since it decreases the rate of transpiration, conserves the water content of the leaves, and reduces the risk of dehydration avoiding death by desiccation (Peak et al., 2004).

The vapor pressure deficit (VPD) is one of the most important environmental factors of stomatal regulation since plants from semi-arid regions showed an inverse correlation between leaf with stomatal conductance, transpiration, and photosynthesis (dos Santos et al., 2017). Likewise, the castor has a high stomatal regulation under field conditions, which can reduce the loss of water by transpiration and maintain the hydric state of the plant (Pinheiro and Chaves, 2011).

The previous response of the species under study represented that O. pyramidale exhibited the highest NP in the dry period (24.31 μmol CO2 m-2 s-1), with the lowest average NP in the rainy period (9.81 μmol CO2 m-2 s-1). C. odorata expressed the highest average photosynthetic rate (16.43 μmol CO2 m-2 s-1) in rainy periods and intermediate in dry periods (11.02 μmol CO2 m-2 s-1), and P. quinata the lowest NP in the two climatic conditions. It can be affirmed that these species are from the group of C3 plants by considering the photosynthetic rates. According to Ocheltree et al. (2014), C3 plants reduce stomatal conductance to minimize water loss; however, the rate of CO2 diffusion also decreases, which reduces the internal concentration of CO2 and the efficiency in carbon fixation by plants (Table 3).

Stomatal regulation of the transpiratory process was observed in these species that are adapted to arid and semi-arid regions, with average rates of 2.96 mmol m-2 s-1 in the rainy period and 0.98 mmol m-2 s-1 in the dry period for C. odorata; 1.33 and 0.94 mmol m-2 s-1 in O. pyramidale and in P. quinata 1.03 and 0.09 mmol m-2 s-1 during the same climatic periods. It led to divergences between the species studied since P. quinata expressed average EWU values of 12.64 µmol CO2 mmol-1 H2O in the rainy season, but in the dry period, it was 10.94 µmol CO2 mmol-1 H2O. On the other hand, both O. pyramidale and C. odorata were around 3.00 and 14.00 µmol CO2 mmol-1 H2O in the rainy and dry periods respectively.

In different species, including soybean, it has been found that the reduction in gs increases the intrinsic efficiency of water use, especially with little availability of water in the soil (Gilbert et al., 2011). Barros Junior et al. (2008) found that the castor, under drought stress, showed a high efficiency in the use of water, which helped maintain the production of biomass.

The reduction in stomatal conductance has been correlated with an increase in the intrinsic efficiency of water use, which indicates that the closure of stomata contributes to optimizing the efficiency of water use in plants under stress. It allows plants to absorb carbon by decreasing the loss of water in the hottest part of the day, contributing to the maintenance of photosynthesis (Broeckx et al., 2014). It can be considered that EWU is a preventive mechanism, as an immediate effect of water deficiency. Besides, from the physiological point of view, the high value of EWU is traditionally considered as a mechanism that provides greater productivity and survival in dry environments (Centritto et al., 2009; Gilbert et al., 2011).

Under conditions of water stress, the castor plant maintains an effective stomatal regulation with a high net CO2 fixation (Severino et al., 2012); with a decrease in perspiration due to rapid stomatal closure, without damage to the photosynthetic apparatus because the deficiencies in the fixation and capture of C are due to the diffusive resistances (Sausen and Rosa, 2010). For this property, they can partially recover the functioning of the photosynthetic apparatus, while remaining in stress; but, when this is eliminated, the plants recover their photosynthetic function in 24 h (Severino et al., 2012). Consequently, they tolerate drought stress quite well; they become a viable crop for arid and semi-arid regions where there are few effective agricultural alternatives (Sausen and Rosa, 2010).

However, this research information is scarce in field conditions to better understand the physiological mechanisms and their interactions with climatic factors under drought (dos Santos et al., 2017). Finally, Anderegg et al. (2018) found that the stomatal response to environmental conditions forms the backbone of all ecosystem models and carbon cycles; but relies heavily on empirical relationships. Evolutionary theories of stomatal behavior are critical to protecting against prediction errors of empirical models in future climates. A longstanding theory holds that stomata maximize the ability to maintain a constant marginal efficient water use over a given time horizon. However, a recent evolutionary theory proposes that stomata instead of maximizing carbon gain reduce carbon costs/risk of hydraulic damage. Anderegg’s et al. (2018) findings focus on the constant known as “marginal efficiency of water use” when it is not the quantity of water that governs the evolution of stomatal regulation, but the stomatal regulation is maximized with the carbon gain while maintaining the hydraulic function.

CONCLUSIONS

There were significant differences in the interaction time×species regarding height (P<0.0002) and diameter (P<0.0003), the highest was O. pyramidale, followed by P. quinata and C. odorata. In regard to diameter, O. pyramidale had the greatest diameter after 23 months (S.2) and biomass accumulation, followed by P. quinata and C. odorata.

Foliage response of these three species had a relationship with weather conditions, during the rainy periods O. pyramidale and C.odorata showed partially open stomata regardless of whether they were. Besides, P.quinata remained with the stomata partly or almost closed in the two climatic seasons.

The behavior of the stomatal regulation was detected in species adapted to arid and semi-arid conditions, in such a way, the intensity of the photosynthetic and transpiratory rates and the efficient water use were expressed according to the genotype×environment interaction. However, it would be interesting to auscultate and use the EWU to identify the stomatal regulation with the carbon cost/risk of hydraulic damage.

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Received: March 06, 2018; Accepted: November 15, 2018

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