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Highlights:
Prosopis laevigata and Cordia boissieri showed acclimation to heterogeneous light conditions.
Growth in diameter and biomass production of both species was greater in the outdoor light conditions.
Leaf area and chlorophyll content increased at higher shading only for C. boissieri.
This study confirms that P. laevigata is a light-demanding species.
C. boissieri shows acclimation strategies suggesting intermediate shade tolerance.
Introduction
It is essential to conserve plant communities because they are an extensive source of ecosystem services and timber and non-timber products. The Tamaulipan Thornscrub (TT) is a characteristic ecosystem of the northeast of Mexico that has played a relevant role in the economy and rural development of the region (Domínguez-Gómez et al., 2013). However, the woody vegetation of the TT faces strong degradation and fragmentation processes, due to silvo-agricultural activities (Pequeño-Ledezma et al., 2012). Therefore, it is necessary to implement propagation and planting activities of native tree species to support the ecological restoration of this ecosystem (Alanís-Rodríguez et al., 2013).
TT is constituted by a wide diversity of trees and shrubs with different growth dynamics, where about half of the species belong to spiny species, mainly from the Fabaceae family (Mora-Donjuán et al., 2013). In this functional group, mesquite (Prosopis laevigata Humb. et Bonpl. ex Willd) plays a significant role in the ecology of the TT (Alanís-Rodríguez et al., 2017; Rodríguez-Sauceda et al., 2014), along with the extensive economic value of the species for the rural population (Ríos-Saucedo et al., 2012). There are other species such as anacahuita (Cordia boissieri A. DC.) belonging to the Boraginaceae family that, in addition to the ecological importance in the TT, has a high sociocultural value (Graciano-Ávila et al., 2018). The anacahuita is the most representative species of Nuevo León and has been considered a priority in reforestation programs in the northeast of Mexico for over two decades (Mata-Balderas et al., 2022).
The success of reforestation programs depends, mostly, on the ability of plants to survive and establish under stress conditions (Riikonen & Luoranen, 2018). Therefore, at nursery level, cultural production practices focused on achieving the best morphological and physiological attributes should be implemented in order to achieve adequate plant performance in the field (Grossnickle & MacDonald, 2018).
Sunlight is one of the most determinant environmental factors in plant growth. The ecological relevance of the main features of radiation, such as intensity, quality or spectrum, directionality and spatial-temporal distribution, has been widely recognized in diverse natural systems (Valladares et al., 2004). These aspects are also relevant for their effect on growth and development of the species of interest in plant production spaces such as greenhouses and nurseries. Therefore, light management has become relevant in forest plant production of a larger number of taxa with the purpose of generating research approaches to develop strategies that promote satisfactory performance of plants in nurseries and fields (Basave-Villalobos et al., 2022a).
Growth characterization and morphophysiological changes of acclimation to light conditions has been the main approach addressed (Endres et al., 2010), with greater emphasis on variations in the intensity or amount of radiation. This experimental approach is consistent with the operational and infrastructural conditions of forest nurseries, where the use of shade nets is the most employed practice for the modification of light environments (Stamps, 2009). For example, Basave-Villalobos et al. (2022, 2022a) recently analyzed the morphological and physiological changes of Pithecellobium dulce (Roxb.) Benth, Enterolobium cyclocarpum (Jacq.) Griseb. and Crescentia alata Kunth, three species from the tropical dry forest, in response to variations in light availability. These authors noted, first, the importance of providing the light environments that each species requires for adequate growth and, second, the possibility of modifying the morphological and physiological attributes of the species according to certain plant quality standards.
The ecophysiological responses of acclimation to light have crucial practical implications for improving plant production processes and field establishment of forest species. This fact justifies the need to study morphological and functional changes under variations in light availability in a wider number of taxa, for two main reasons: a) there is still a knowledge gap regarding the behavior of each species in heterogeneous light environments, which could help to understand the acclimation mechanisms of each species according to its own ecology and, b) many taxa still lack nursery propagation protocols due to their limited ecological and silvicultural knowledge (Basave-Villalobos et al., 2022a; Bonfil & Trejo, 2010), this being particularly the case for TT species.
Therefore, the objective of this study was to evaluate growth and changes in some morphological attributes and chlorophyll concentration in P. laevigata and C. boissieri plants grown under different light environments under nursery conditions. The starting hypothesis was that these characteristics differ in response to heterogeneous light environments in both species. Understanding the morpho-physiological responses of these species to the light environment has important implications that will contribute to the improvement of propagation and cultivation protocols of TT native tree species during the nursery stage and field establishment in restoration projects.
Materials and methods
Plant material and experimental design
The study species are among the most representative of the TT. Prosopis laevigata has a predominantly arboreal growth, reaching up to 15 m in height and has a wider distribution in the arid and semi-arid regions of Mexico. On the other hand, C. boissieri has a generally shrubby growth habit of 5 to 8 m in height with a distribution more restricted to the northeast of Mexico and, occasionally, in the center of the country.
The study was carried out at the GEMA S. C. forest nursery in the municipality of Linares, Nuevo León (northeastern Mexico; 24° 51.0’ N, 99° 33.8’ W; 361 m elevation). Prosopis laevigata and C. boissieri seeds from natural distribution areas surrounding the city of Linares, Nuevo León, were used in the year prior to sowing (2018). Seeds were sown in 10 x 23 cm black polyethylene bags (650 cm3) with a substrate mixture composed of 70 % black bush soil, 30 % perlite, and 10 % organic compost (humus). Due to their physical dormancy, P. laevigata seeds received a scarification treatment by immersion in drinking water at 95 °C for 1.5 min (Quiñones Gutiérrez et al., 2013). Cordia boissieri seeds received no pre-germinative treatment.
A total of 600 plants were grown for each species, which were arranged in 1.30 x 4.30 m planting beds. Once seedling emergence was completed, two weeks after sowing, the beds were divided into three sections which were assigned to an environmental light condition: 1) outdoors (OD), 2) 40 % shade (N40) and 3) 60 % shade (N60). Each light environmental condition had four replications of 50 plants (200 plants in total per treatment and species), which were arranged in a completely randomized experimental design.
Plant growing lasted 17 weeks, from mid-June to the end of October 2019. During this period, an average global radiation of 440.0 ± 5.7 W∙m-2 was recorded, while the photosynthetic photon flux density (PPFD) was 1 012 ± 13 µmol∙m-2∙s-1. The average ambient temperature was 29.5 ± 1.0 °C and relative moisture of 70.1 ± 3.3 %. Plants were watered twice a week and occasionally three times when the temperature exceeded 35 °C. At four and eight weeks after planting, a commercial water-soluble fertilize (24-8-16 NPK; Miracle-Grow® Lawn Products, Marysville, OH, EE. UU.) was applied at the rate of 0.8 g∙L-1 water, based on the fertilization traditionally used by the nurseryman.
Evaluation of growth and biomass distribution
Six weeks after planting, 24 plants per treatment (six per replication) were selected to monitor height (cm) and diameter (mm) growth every two weeks during the growing season. At 17 weeks after planting, 12 plants per treatment (three per replication) were harvested to evaluate aboveground and root biomass. For this purpose, after carefully washing the root system, the plants were separated into aboveground and root parts and dried in a forced-air oven (FE-133, Felisa, Mexico) at 65 °C for 72 h. The dry weight of each component was determined with a digital analytical balance (Ohaus Adventurer, Ohaus, Mexico). The fraction of aboveground biomass and root biomass to total plant biomass was calculated from the biomass data.
Analysis of leaf area and chlorophyll concentration
Leaf area was determined on 12 randomly selected plants per treatment (three per replication). Leaves were separated and scanned. Individual leaf area was measured using ImageJ software (Schneider et al., 2012). Chlorophyll a (C a ) and b (C b ) concentration was determined by colorimetry following the methodology described by Barnes et al. (1992). A uniform sample of fresh leaves (about 1 g) cut into small pieces was taken and liquefied in an 80 % acetone solution. The extract was then filtered using Whatman No. 1 paper and the absorbance was measured at 663 and 645 nm in a spectrophotometer (UV-1601B, Shimadzu Scientific Instruments Inc., USA). The concentrations (mg∙g-1) of C a and C b were estimated by the following equations (Wellburn, 1994): C a = 12.21A 663 - 2.81A 645 and C b = 20.13A 645 - 5.03A 663.
Statistical analysis
Statistical analyses were carried out using SPSS software, separated by species. The effect of light environment on height and diameter variables during the growing season was evaluated by repeated measures ANOVA, which was expressed as a mixed effects model in which time (days after planting, discrete variable) and light environment were included as fixed effects and plant as a random effect. Biomass, leaf area and chlorophyll concentration variables were analyzed by one-way ANOVA. For each variable, the assumptions of normality and homogeneity of variances were tested using the Shapiro Wilk and Levene tests, respectively. For height and diameter growth over time, the residuals of the model were checked for normality and homoscedasticity. In required cases, when the data showed a non-normal distribution, the transformation was made to natural logarithm. When the ANOVA showed a significant effect, a multiple comparison of means was made using Tukey's test (P = 0.05).
Results
Height and diameter growth
During the growing period, light environment significantly affected both species' growth. In the case of P. laevigata, the time*environment interaction was significant (F = 3.15, P < 0.001) on height growth, showing the greatest effect in the first two months of growth (Figure 1a). The greatest increase in height was recorded with the most shaded treatment (N60) with a difference of almost 10 % compared to plants grown in the outdoor conditions. On the other hand, diameter growth was favored in the outdoor conditions (Figure 1c), which was almost twice higher than that recorded in the N60 plants, which had the lowest values (F = 6.55, P < 0.001).
Figure 1 Height and diameter growth throughout the nursery period of Prosopis laevigata and Cordia boissieri in different light environments: outdoors (OD), 40 % shade net (N40) and 60 % shade net (N60). Each point represents the mean ± standard error (n = 24).
C. boissieri plants grown in both shade levels showed greater height growth compared to the outdoor condition, although the difference was more marked towards the end of the growing period (time*environment interaction, F = 5.09, P < 0.001; Figure 1b). On the other hand, plants grown both in outdoors and in intermediate shade (M40) had greater diameter growth with significant differences over those grown under the highest shade intensity (M60); like height growth, these differences became more evident over time (time*environment interaction, F = 1.91, P = 0.013; Figure 1d).
Biomass production
In both species, light environment significantly (P < 0.001) affected biomass production, both aboveground and root. For P. laevigata plants grown under the outdoor condition induced superior formation of both aboveground and root biomass with highly significant differences over plants at the highest shading level (N60; Table 1). Cordia boissieri plant biomass increased at higher light intensity; however, aboveground and root biomass production was not significantly different between plants in outdoors and those at N40.
Table 1 Aboveground biomass (AGB) and root biomass (RB) in Prosopis laevigata and Cordia boissieri plants grown under three light environments: outdoors (OD), 40 % shade net (N40) and 60 % shade net (N60).
| Light environment | Prosopis laevigata | Cordia boissieri | ||
|---|---|---|---|---|
| AGB (g) | RB (g) | AGB (g) | RB (g) | |
| OD | 2.38 ± 0.29 a | 2.04 ± 0.20 a | 1.54 ± 0.11 a | 2.17 ± 0.12 a |
| N40 | 0.87 ± 0.06 b | 0.55 ± 0.06 b | 1.39 ± 0.06 a | 1.75 ± 0.16 a |
| N60 | 0.51 ± 0.07 c | 0.23 ± 0.04 c | 0.89 ± 0.06 b | 0.76 ± 0.07 b |
| P-value | <0.001 | <0.001 | <0.001 | <0.001 |
At the species level, means with different letters indicate significant differences between light environments.
On the other hand, biomass allocation patterns were also modified as an effect of light condition. Prosopis laevigata showed a higher allocation to the aboveground part as the amount of light decreased (Figure 2a), with values ranging from 54 % to 69 %. Cordia boissieri biomass allocation was similar between the N40 and outdoors treatments (Figure 2b); however, these treatments had a higher proportion of biomass allocated to roots than to the aboveground area.
Figura 2 Aboveground and root biomass fractions in Prosopis laevigata (a) and Cordia boissieri (b) plants grown in three nursery light environments: outdoors (OD), 40 % shade net (N40) and 60 % shade net (N60). At the species level, means with different letters indicate significant differences between light environments according to Tukey's test (P < 0.05).
Leaf area and chlorophyll concentration
Under both shade conditions (N40 and N60), P. laevigata plants showed lower leaf area (P < 0.05) compared to the outdoor condition (Table 2). On the other hand, in this same species, chlorophyll a and b concentrations increased at higher shade intensity, although without significant difference (P > 0.05) compared to the outdoor condition.
Table 2 Leaf area (LA) and chlorophyll concentration (Ca and Cb) in Prosopis laevigata and Cordia boissieri plants grown under three light environments: outdoors (OD), 40 % shade (N40) and 60 % shade (N60).
| Light environment | Prosopis laevigata | Cordia boissieri | ||||
|---|---|---|---|---|---|---|
| LA (cm2) | Ca (mg∙g-1) | Cb (mg∙g-1) | LA (cm2) | Ca (mg∙g-1) | Cb (mg∙g-1) | |
| OD | 76.6 ± 16.7 a | 0.98 ± 0.16 | 0.22 ± 0.03 | 97.7 ± 22.4 b | 0.48 ± 0.05 c | 0.14 ± 0.02 b |
| N40 | 45.2 ± 13.2 b | 1.27 ± 0.21 | 0.33 ± 0.08 | 167.6 ± 28.1 a | 0.60 ± 0.05 b | 0.16 ± 0.01 b |
| N60 | 42.8 ± 14.2 b | 1.05 ± 0.17 | 0.33 ± 0.13 | 159.9 ± 30.8 a | 0.76 ± 0.07 a | 0.20 ± 0.01 a |
| P value | 0.004 | 0.061 | 0.820 | 0.001 | 0.001 | 0.003 |
At the species level, means with different letters indicate significant differences between light environments according to Tukey's test (P < 0.05).
Unlike the response of P. laevigata, C. boissieri plants grown in outdoor conditions had less leaf area than those grown in shaded conditions. For C. boissieri, chlorophyll a and b concentrations increased significantly (P < 0.05) at higher shade intensity, and of these, C a concentration showed a linear increase as shade intensity increased (N60 > N40 > OD; Table 2).
Discussion
The results indicate that growth, biomass production, and chlorophyll concentration for P. laevigata and C. boissieri plants are affected by the light environment during nursery culture. In general, this response suggests a plastic adjustment of the species to thrive in heterogeneous light environments (Valladares et al., 2004). According to diameter growth and biomass production, both P. laevigata and C. boissieri improved in the environment with the highest light availability (outdoors). This behavior can be explained by the ecology of the species, due to the habitat where they predominate. However, it is interesting to analyze the differences in attributes as a function of light, because acclimation responses are usually species-specific (Wyka et al., 2007) and vary according to the trait examined (Valladares et al., 2004), as was observed in the present study.
On the one hand, P. laevigata plants tended to grow higher from the beginning of the experiment under the light restriction imposed by the nets, showing a shade escape syndrome by stem elongation (Valladares & Niinemets, 2008). This result shows the preference of P. laevigata plants for a higher radiation environment, which is usually characteristic of pioneer species (Firmino et al., 2021). Shoot elongation is an important strategy to maximize light capture in competitive environments (Masarovičová et al., 2016), as has been observed in the tropical species Crescentia cujete L. (Piña & Arboleda, 2010); however, it involves spending reserves for cell elongation sacrificing resources for secondary growth (Nagashima & Hikosaka, 2011). This explains the lower diameter growth found in the shade treatments during most of the production cycle. Also, light restriction reduced biomass production in both components (aboveground and root), reflecting suboptimal growth. Light is an indispensable resource for growth, so when availability is reduced, the effect is greater on the performance of light-demanding species (Basave-Villalobos et al., 2022).
Shading using nets induced alterations in the biomass distribution patterns, favoring the allocation to the aboveground component. Bignoniaceae, Tabebuia chrysotricha (Mart. Ex DC.) Standl (Endres et al., 2010) and in Meliaceae, Cedrela fissilis Vell. (Sanches et al., 2017). This behavior, apparently common in several species, ratifies that the alteration of biomass allocation patterns is one of the acclimation strategies at the morphological level, to maintain a positive carbon balance under light-limiting conditions (Kitajima, 2007), although with a lower growth rate than would be the case under optimal conditions, as reflected by the results of this study.
Growth was also affected by the limited availability of light in the leaf area of P. laevigata, with higher values (almost 2-fold) in the outdoor environment compared to the environment with lower light availability (N60). Thus, a lower leaf area affects the photosynthetic capacity of plants because the surface area for light capture is reduced, which has an impact on growth; although, at the leaf level, there are other functional traits that have a greater impact on photosynthesis (dosAnjos et al., 2015). These changes in leaf area, in response to the light environment, have also been recorded in plants of Araucaria angustifolia (Bertol.) Kuntze (Olguin et al., 2020) and C. fissilis (Sanches et al., 2017).
Other studies with P. laevigata also report the impact of light restriction on morphology and growth (Basave-Villalobos et al., 2017). Similarly, in plants such as C. alata, a light-demanding species, low levels of this factor also significantly reduced their growth rates (Basave-Villalobos et al., 2022). Finally, although the effect of the light environment on the chlorophyll concentration of P. leavigata was marginal, the lower presence of this pigment in plants grown in outdoors suggests possible damage by photoxidation. This anomaly induces the degradation of chlorophylls and other photosynthetic pigments (Tang et al., 2015).
On the other hand, the response of C. boissieri to the light environment was similar to P. laevigata regarding height and diameter growth, since plants elongated in shaded environments because of the growth in diameter. This behavior is not favorable because it can lead to slender phenotypes that, based on plant quality, are more vulnerable to mechanical damage at the planting site (Basave Villalobos et al., 2020). Also, in this species, biomass allocation to aboveground tissues was higher when shading intensity was higher, as reported for its congener Cordia trichotoma (Vell.) Arráb. ex Steud. (Firmino et al., 2021) and T. chrysotricha (Endres et al., 2010); however, biomass allocation contrasted only at the highest level of shade (N60). This suggests that, for C. boissieri, the intermediate shade condition (N40) was not a significant light restriction that would require alterations in its biomass allocation patterns.
The absence of differences in growth or other functional attributes may be associated with a lower degree of plasticity to the light environment. For example, in plants of Machaerium brasiliense Vogel, even a shading level of 80 % had no effect on growth or other morphological variables, compared to plants growing in outdoor conditions (Firmino et al., 2021). Low plasticity in morphological characters is attributed to tolerant species; although, in the case of C. boissieri, the lack of differences only between plants grown in outdoors and those with intermediate shading (N40) could suggest an intermediate tolerance to shade. Similar trends have been found in other species such as E. cyclocarpum, which show the ability to acclimate to heterogeneous light conditions in several traits, including some physiological attributes (Basave-Villalobos et al., 2022).
Some degree of shade tolerance of heliophyte species is a trait that is usually exhibited in the natural environment, due to vegetation dynamics in the developmental stages of a stand; that is, there are species that in early stages usually modulate morphophysiological changes to acclimate to heterogeneous light environments, which are often present in the understory (Endres et al., 2010; Sanches et al., 2017). Leaf area results also evidenced acclimation capacity of C. boissieri to the heterogeneous light environment, as leaf area increased as light availability decreased, in contrast to the situation in P. laevigata.
A similar behavior to C. boissieri has been found in other intermediate successional species such as Cabralea canjerana (Vell.) Mart (Moretti et al., 2019) or Torreya grandis Fortune ex Lindl (Tang et al., 2015), but they show tolerance to shade during their juvenile phase. However, there are other species with this same succession dynamics such as C. trichotoma, M. brasiliense and Triplaris americana L. (Firmino et al., 2021), in which leaf area modulation is not always observed, as they produce the same area in different light environments or, on the contrary, leaf area decreases with shading as occurs in P. dulce (Basave-Villalobos et al., 2022).
The increase in leaf area is considered a typical acclimation response that plants exhibit to optimize light interception, absorption and processing in shaded environments (Masarovičová et al., 2016), but also, the effectiveness in light absorption is optimized with the increase in photosynthetic pigment concentration. A marked trend of chlorophyll a and b increase in C. boissieri plants at higher shading was found in this study. This effect suggests greater investment to light-capturing antenna complexes, as reported for C. canjerana and Carpotroche brasiliensis (Raddi) A. Gray (Cerqueira et al., 2018). This increase in the amount of chlorophylls is mainly due to the increase in the amount of chlorophyll b, which is a component of the antenna complex, although chlorophyll a is also a key component involved in the electron transport chain (dosAnjos et al., 2015).
Conclusions
Prosopis laevigata and Cordia boissieri modify their morphology, growth and chlorophyll concentration depending on the light environment in which they grow, which shows acclimatization capacity to heterogeneous light conditions. Although both species perform better in high light levels, C. boissieri shows acclimation strategies that suggest an intermediate tolerance to shade, in contrast to P. laevigata which confirms to be a light-demanding species. These responses have important implications in the management of the species for reforestation programs because they allow defining the adequate light conditions in the nursery to optimize their growth.
