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Introduction
One of the most important aspects of successful regeneration of plant populations is seedling growth, which is key to community dynamics (Kitajima & Fenner, 2000). The establishment of plants in contrasting environments can lead to a better understanding of the ability of threatened endemic species to adapt to different environments and contribute to population restoration (Li & Pritchard, 2009; Mendoza et al., 2009).
The establishment of plants in areas different from their natural habitat can be a limitation for their survival, growth, and development (Quintana-Ascencio et al., 2004; Restrepo & Cardona, 2011). For example, García-Castro et al. (2017), evaluated in Magnolia pugana seedlings the effect of light, fertility, and seed origin on the relative growth rate and its components, reporting diverse morphological and physiological differences, making it possible to adapt to diverse environments.
Chlorophyll fluorescence is a useful tool to assess the tolerance of plants in different environments (Ashraf & Harris, 2013). Plants of the same species could show different photosynthetic responses to environmental variables, for example, Navarro et al. (2010) found differences in the response of chlorophyll fluorescence to water stress in Pinus halepensis. Likewise, research on adults of Quercus mongolica Fisch. ex Ledeb, from two different populations, showed differences when analyzing PSII quantum efficiency (фPSII) and electron transfer rate (Zhang et al., 2005).
The Sierra Madre Occidental is a mountainous complex that extends almost from the border with the United States to northern Jalisco (González-Elizondo et al., 2012), besides one of the most important regions in terms of floristic richness (Rzedowski, 1978). This is a transitional zone between the Nearctic and Neotropical kingdoms with a high diversity of species and endemism, including the Magnoliaceae family (Vázquez-García et al., 2002).
Magnolia pugana (H. H. Iltis & A. Vázquez) A. Vázquez & Carvajal, known regionally as "almacasusco", is an evergreen tree between 10 and 20 m tall that grows along the banks of streams tributary to the Santiago River, forms part of the vegetation community of gallery forests (Vázquez-García et al., 2002), and is endemic to central Jalisco and southern Zacatecas. The fragmentation of its habitat due to extensive cattle ranching and forest use for furniture manufacturing has caused a decline in its populations, therefore, the population is at serious risk of extinction (Cicuzza et al., 2007). Due to its restricted distribution and populations with few individuals, factors such as inbreeding and genetic drift could promote extinction scenarios (Vázquez-García et al., 2002; Muñiz-Castro et al., 2021). In addition, Jacobo-Pereira et al. (2016) found restrictions in seed dispersal due to low viability and dormancy mechanisms.
Repopulation of endangered species is crucial for the rescue and conservation of vulnerable populations (Dawson et al., 2013). The restoration of M. pugana populations is important due to the critical state of its populations caused by habitat loss and low numbers of individuals (Muñiz-Castro et al., 2021). The comparison of the growth and physiological performance of this species in areas outside its range and in its original habitat could provide new knowledge for its conservation. There are no studies of the growth of M. pugana in situ and ex situ conditions, which would provide essential information for the development of programs and activities for the restoration of its populations. This work aimed to evaluate the growth and chlorophyll fluorescence of Magnolia pugana seedlings in two contrasting habitats: in situ (original habitat) and ex situ (urban park).
Methodology
Study area
The in situ site was located in San Lorenzo (SL) in the municipality of Zapopan, Jalisco, located 8 kilometers from the community of Santa Lucia between 103°33'13.82" W, 20°49'12.28" N, at an altitude of 1467 meters. Most of the soils come from the Tertiary and Quaternary periods, rich in compounds such as volcanic rocks, basalt, and tuff. The dominant soils belong to the Eutrous Regosol and Haplic Feozem type, which are characterized by a sandy texture, and poor in organic matter. (INEGI, 1981). Soil use is agricultural and forestry. Most of the land is owned by smallholders, followed by ejido and communal land (INEGI, 1981). The average annual temperature is 20.6°C. The average minimum and maximum temperatures are 8.2°C and 33.4°C in January and May, respectively. The average annual precipitation is 999.3 millimeters (Ruiz et al., 2012). The riparian forest is the natural habitat of M. pugana, which is accompanied by tree species: Litsea glaucescens Kunth, Taxodium mucronatum Ten, Piper hispidum Kunth, Piper jaliscanum S. Watson, Ficus insipida Willd., and Aphananthe monoica (Hemsl.) J.-F. Leroy (Acevedo-Rosas et al., 2008), which on average have heights between 18 and 25 m in height, shrubs of 2 to 4 m in height are also found.
The ex situ site was established in an urban area with the category of Municipal Hydrological Protection Area called "Bosque Los Colomos" (BLC), located northeast of the city of Guadalajara, Jalisco, Mexico (González-Hernández et al., 2015). It has an area of approximately 90 hectares and its coordinates are 20°42'38" N, 103°24'12" W and 20°42'07" N, 103°23'26" W; the altitude is 1556 meters. The soil is Regosol Eutric with little development with a coarse texture and poor in organic matter. The climate is semi-warm sub-humid [(A)C(w1) (w)] with rainfall in summer, with annual precipitation of 976.5 millimeters and a mean annual temperature of 19.5 °C (Loza-Ramírez & González-Salazar, 2009). The vegetation structure is mainly composed of trees 15 to 20 m tall and shrubs 2 to 5 m tall. The main established native species are: Pinus ayacahuite C. Ehrenb. ex Schltdl., P. devoniana Lindl., P. douglasiana Martínez, P. maximartinezii Rzed., P. oocarpa Schiede ex Schltdl., P. patula Schltdl. & Cham., P. tenuifolia Salisb. However, secondary vegetation and introduced species are also found: Casuarina cunnighamiana Miq., C. equisetifolia L., Eucalyptus camaldulensis Dehnh., E. citrinoides Benth., E. globulosus St.-Lag., and E. robusta Sm. (Jara-Arce & Orendain-Díaz, 2009).
Seed collection and seedling growth in the greenhouse
In April 2015, seeds of at least 10 adult individuals of Magnolia pugana were collected at the San Nicolas locality (20ᵒ 48'53.2" N and 103ᵒ 34'49. 8" W), germination and seedling growth were carried out in a greenhouse located at the Centro Universitario de Ciencias Biológicas y Agropecuarias (20ᵒ 44'53.6" N and 103ᵒ 30'52.2" W) following the methodology applied by García-Castro et al. (2018).
In July 2015, 60 twelve-month-old M. pugana seedlings, ranging from 15 to 25 centimeters in height, were established approximately three meters apart between individuals and 1.5 meters from the margin of each stream. Thirty seedlings were transplanted in La Virgen stream in San Lorenzo (in situ) and 30 seedlings were transplanted in Bosque Los Colomos (ex situ) on La Culebra stream (Fig. 1a). Both sites are devoid of tree and shrub vegetation, the vegetation was removed approximately 20 years ago for agricultural activities in SL and the BLC for recreational activities. During the recording of the variables, herbaceous vegetation was kept free around the seedlings.
To assess environmental conditions at the beginning and end of the work in both sites; temperature, and water vapor pressure deficit were measured, using with HOBO electronic devices (H08-004-002, Onset Computer Corporation, Massachusetts, USA), and photosynthesis photon flux density (DFFF) with a Quantum LI-COR LI-250; at the SL site (in situ) the temperature was 26. 1 ± 0.6 ᵒC, vapor pressure deficit 2.3 ± 0.13 MPa; and at the BLC site (ex situ) the temperature was 29.7 ± 1.1 ᵒC, vapor pressure deficit 2.4 ± 0.3 MPa.
Response variables
From October 2016 through March 2017, each month in both study sites (SL and BLC), survival was assessed by counting live and dead seedlings. Stem length (cm), stem base diameter (mm) (with a Mitutoyo Absolute digital vernier), and canopy cover (recorded with the length of the two perpendicular axes to estimate the horizontal projection of cover) were also measured according to the ellipse area formula (Mueller-Dombois & Ellenberg, 1974).
Chlorophyll fluorescence was assessed in the last month (January 2017) with a portable fluorescence analyzer (Mini-PAM, Photosynthesis Yield Analyzer, Walz, Effeltrich, Germany). Every two hours from 08:00 to 17:00 hours in seven seedlings per site (SL and BLC), the effective quantum yield of photosystem II (ΦPSII) was estimated in a light-adapted sample with the following formula: фPSII = (F'm - Ft)/ F'm, where F'm which is the maximum fluorescence emitted by chlorophyll when a pulse of actinic light is superimposed on light levels and Ft is the chlorophyll fluorescence emitted by plants in a stable phase of illumination (e.g., field light conditions) (Genty et al., 1989). Values for ΦPSII range from 0.8 to 0.83 when unstressed plants; these values decrease with increasing environmental stress (Maxwell & Johnson, 2000).
Also, in seven seedlings per site at 5:00 h (pre-dawn), the maximum quantum efficiency of photosystem II (Fv/Fm) was measured with the following formula Fv/Fm = (Fm -F0)/Fm, where Fv is the variation of chlorophyll fluorescence of a dark-adapted leaf (Fv = Fm - F0) and Fm is the maximum fluorescence of a dark-adapted leaf (Maxwell and Johnson, 2000). The rate of electron transfer (ETR) was estimated with the following formula: ETR= ΦPSII × RFA × 0.05 × 0.084, expressed in μmol m-2 s-1, where 0.5 is the energy distribution factor between photosystem I and photosystem II, and 0.84 is a standard factor of light absorbed by photosynthetic tissue (Ehleringer, 1981).
Experimental design and statistical analysis
The experimental design was completely randomized with two treatments: in situ (SL) and ex situ (BLC) with 30 seedlings (replicates) for each site. Survival was recorded and analyzed with the X 2 test, considering the number of dead and live seedlings as a column factor and the site as a row factor. Stem basal area (mm) (n = 60) was analyzed with repeated measures ANOVA to evaluate the effect of site and time (month of sampling). The assumptions of normality and homogeneity of variance were tested prior to the analyses. Tukey's multiple comparison test (α = 0.05) was used to identify differences between sites. Canopy cover and stem length variables were analyzed using Friedman's test with repeated measures due to the lack of normality and homoscedasticity (n = 60).
Photosystem II effective quantum yield ΦPSII (µmol m-2 s-1), photosystem II maximum quantum efficiency (Fv/Fm) (µmol m-2 s-1) and electron transfer rate (ETR, µmol m-2 s-1) were evaluated by repeated measures ANOVA (n = 14) with seven seedlings per site to assess the effect of site and time (sampling time). All analyses were performed with the statistical package Statistica version 7.0 (StatSoft Inc., 2004).
Results
Growth
During the first three months after transplanting, it was observed that 100 % of the seedlings survived at both sites. At the end of the evaluation (six months after transplanting), survival analysis showed significant differences between sites (X 2 = 1784.5, p = ˂ 0.001). In the BLC (ex situ) 73 % of seedlings survived, in contrast to those in SL (in situ) where 97 % of seedlings survived.
Repeated measures ANOVA for seedling basal area growth revealed significant differences between locations (F = 341, p = ˂ 0.01). At the SL site, the basal area of seedlings increased on average 68.8 % compared to that of seedlings at the BLC site. The time × site interaction showed no statistical differences (F = 1.75, p = ˃ 0.05 and F = 0.17, p = ˃ 0.05) (Table 1).
The variable cover also showed differences between sites (X2 = 143.56, p = ˂ 0.001), at the SL site seedlings increased canopy cover by 61.1 %, in contrast to the BLC site (Table 1). The variable stem length also revealed significant differences (X 2 = 108.58, p = ˂ 0.000), seedlings at SL showed 18.7 % greater height compared to seedlings at the BLC site (Table 1).
Table 1 Average (± SE) of the growth variables (cover, stem length and basal area of the stem) of Magnolia pugana seedlings in situ and ex situ.
| Site | Coverage (cm-2) | Stem length (cm) | Stem basal area (mm-2) |
|---|---|---|---|
| San Lorenzo (in situ) | 815.1a ± 39.3 | 28.54a ± 0.6 | 7.44a ± 0.18 |
| Bosque Los Colomos (ex situ) | 498.2b ± 22.1 | 20.2b ± 0.5 | 5.26b ± 0.15 |
Different letters indicate significant differences for each variable according to Tukey's test (p ˂ 0.05).
Chlorophyll fluorescence
The maximum quantum yield of photosystem II ΦPSII showed statistical differences (F = 61.1, p = ˂ 0.0001). In Magnolia pugana seedlings from the BLC site, it was lower (0.626b ± 0.01) than in the SL site (0.778a ± 0.01). Repeated measures analysis of variance of the effective photosynthetic efficiency of ΦPSII revealed significant differences by site effect (F = 17.77, p = ˂ 0.001). The ΦPSII in seedlings from the SL site showed 20.7 % more quantum yield than those from the BLC site (Fig. 1). Differences by sampling time were also revealed; the lowest photosynthetic efficiency occurred at 16:00 h (0.4788 µmol m-2 s-1). The site × sampling time interaction revealed no statistical differences (F = 0.59, p = ˃ 0.5).
Different letters indicate significant differences according to Tukey's test (p ˂ 0.05)
Figure 1 Average (± SE) of the effective photosynthetic efficiency of photosystem II ΦPSII (µmol m-2 s-1) in Magnolia pugana seedlings transplanted in two sites: San Lorenzo (in situ) and Bosque Los Colomos (ex situ).
In electron transfer rate (ETR) we also found significant differences (F = 17.62, p ˂ 0.01) by site effect. Seedlings from the SL site showed 82.4 % more ETR (20.8a ± 2.6) in contrast to those from the BLC site (17.3b ± 1.9). There were also differences by sampling time (F = 92.54, p ˂ 0.0001). Between 12:00 and 16:00 hours, the highest electron transfer rate was recorded. We found differences by site × sampling time interaction (F = 16.47, p ˂ 0.001), ETR increased in the hours with the highest solar radiation from 12:00 hours and up to 16:00 hours, but at the BLC site seedlings decreased ETR in the last two sampling hours, in contrast to those in SL (Fig. 2).
Different letters indicate significant differences for each variable according to Tukey's test (p ˂ 0.05).
Figure 2 Average (± SE) of the electron transfer rate (µmol m-2 s-1) in Magnolia pugana seedlings transplanted in two sites: San Lorenzo (in situ) dotted line and Bosque Los Colomos (ex situ) continuous line.
Discussion
Both in situ and ex situ conservation of endangered species require knowledge of the survival and growth of the species under study to obtain basic biological information as a preliminary step in protection actions (IUCN, 2012). Survival is one of the main factors affecting the regeneration of plant populations (Elzinga et al., 2001), and also represents an important measure to evaluate the success of conservation programs for endangered populations (Ramírez-Herrera et al., 2005). One of the main objectives of ex situ conservation is to avoid the extinction of endangered populations as an effort to improve and increase conservation programs (Maunder & Byers, 2005). In this work, we found that in situ conditions (San Lorenzo) had higher survival than ex situ (Bosque Los Colomos). These results are consistent with those reported by Restrepo & Cardona (2011), who carried out plantations with juveniles of five endemic species of the Magnolia genus with contrasting environmental site conditions, with greater survival and growth in conditions similar to their natural habitat.
Plant growth depends on its ability to capture resources such as light and nutrients (Tilman, 1985). The growth of the basal area and stem height is considered as an indicator of the morpho-physiological quality of seedlings (Restrepo & Cardona, 2011). In this work, seedlings established in situ conditions showed greater growth in basal area and stem length and therefore a greater competitive ability than those grown in ex situ conditions. These results agree with those obtained by García-Castro et al. (2018) who studied under greenhouse conditions, the relative growth rate of Magnolia pugana seedlings obtained from seeds with in situ and ex situ provenance and found that seedlings from in situ populations had higher growth in contrast to seedlings with ex situ provenance.
The capture of solar radiation by the canopy affects plant productivity (Lambers & Poorter, 1992). This measure can also predict the direction that the plant community may follow (Tilman, 1987), where competition for resources determines the abundance of species (Mouquet et al., 2002). In this work, in situ seedlings showed greater canopy cover than those in ex situ conditions, which implies greater solar radiation capture area and therefore better photosynthetic performance in seedlings established in their original distribution area.
Chlorophyll fluorescence can be used as a tool to evaluate the adaptive capacity of plants in different environmental conditions (Cavender-Bares & Bazzaz, 2004). The maximum photosynthetic efficiency of photosystem II (Fv/Fm) in a healthy plant presents values between 0.8 and 0.83, the decrease of this value indicates that there are processes of inactivation of photosystem II by some type of stress, also called photoinhibition (Ribeiro et al., 2005). In this work in neither of the two populations of Magnolia pugana established values of 0.8 were reached, however, seedlings established in SL showed 19.5 % more photosynthetic efficiency (0.778 µmol m-2 s-1), in contrast to that recorded in BLC (0.626 µmol m-2 s-1), and therefore SL seedlings showed better photochemical performance than those established in BLC.
Techniques such as chlorophyll fluorescence provide basic insights into the fundamental mechanisms of photosynthesis and the effect of stress factors on plants that impact the decrease in photosynthetic efficiency of PSII (ΦPSII) (Force et al., 2003; Murchie & Lawson, 2013). Plants of the same species in different habitats show morphological and physiological changes to acclimate (Zhang et al., 2005). ΦPSII, could decrease due to variation in environmental factors (Adams & Demming-Adams, 2004). In this work, the lower quantum yield was observed in Magnolia pugana seedlings established in ex situ conditions.
The electron transport rate (ETR) is a protective mechanism of the photosynthetic apparatus against a decrease in quantum efficiency (Flexas & Medrano 2002). High ETR values occur in response to increased quantum efficiency (Hernández-González et al., 2020). In this work, the electron transport rate in SL seedlings (in situ) was significantly higher in the 16:00 h sampling (Fig. 2), in contrast to those in the BLC (ex situ); this means that M. pugana seedlings in SL showed a recovery of PSII, which could suggest that in the latter site they had greater tolerance to light.
The study of the growth of endangered species is crucial for the conservation of populations of endemic species. The conservation of populations of endangered native species is crucial to alleviate the decline of populations and requires knowledge of the ecophysiological attributes, so studies such as this one contribute to the knowledge and search for actions for the restoration of endangered riparian species.
Conclusions
Magnolia pugana seedlings transplanted at the San Lorenzo site (in situ) showed higher survival and better performance in growth and photosynthetic efficiency compared to seedlings transplanted at Bosque Los Colomos (ex situ). It is important to continue these studies because the information generated contributes to knowledge for decision making regarding the establishment of Magnolia pugana plantations for conservation and restoration purposes.
