Introduction
The central Argentina ecotone, characterized by an arid-to-subhumid temperate transition climate, encompassing more than 10 M hectares, has been seriously degraded by deforestation, overgrazing and some unsustainable agriculture (González and Pérez, Reference González and Pérez2017; Zeberio and Peréz, Reference Zeberio and Pérez2020). These high levels of disturbance removed vegetation and exposed areas to erosion, severe processes of desertification and loss of agricultural productivity in arid and semiarid regions (Gabella and Strijker, Reference Gabella and Strijker2018; Winschel and Pezzola, Reference Winschel and Pezzola2018). In semiarid-to-subhumid environments, continuous grazing contributes to an increased abundance of woody species that may interfere with livestock management and reduce the production of desirable grasses (Villalobos and Peláez, Reference Villalobos and Peláez2001).
Plant species are locally adapted to the environmental conditions in which they occur (Lascoux et al., Reference Lascoux, Glémin and Savolainen2016). Neltuma (ex Prosopis) caldenia Burk. and Neltuma flexuosa var depressa F.A. Roig (Fabaceae; subfam: Mimosoideae) are two species that occur within the central ecotone region. They are valued as a forage source for ruminants and bees and are suitable candidates for the restoration of degraded areas (Alvarez and Villagra, Reference Alvarez and Villagra2009; Villagra et al., Reference Villagra, Vilela, Giordano, Álvarez and Ramawat2010; Farinaccio et al., Reference Farinaccio, Ceccon and Pérez2021; Hughes et al., Reference Hughes, Ringelberg, Lewis and Catalano2022). These species could play an important role in restoration and erosion control, as well as in increasing soil fertility due to their capacity to fix atmospheric nitrogen (Cony, Reference Cony1996). The tree N. caldenia is distributed between 31 and 41°S latitude in a temperate semiarid environment and can form forests where they are dominant or form communities with greater diversity, consisting of other species including N. flexuosa DC, Geoffroea decorticans Gill. ex. H. et A. Burkart and Jodina rhombifolia (Hook. & Arn.) Reissek. The shrub- (N. f. var depressa) occurs predominantly between latitudes 30 and 43°S and has been found to show tolerance to drought, cold, salinity and alkalinity in a temperate arid environment (Roig, Reference Roig1993; Alvarez and Villagra, Reference Alvarez and Villagra2009; Villagra et al., Reference Villagra, Vilela, Giordano, Álvarez and Ramawat2010). Both species are predominantly cross-pollinated and are known to have physical dormancy, caused by water-impermeable palisade cells in the seed coat, a trait which could favour its dispersal via endozoochory (Peinetti et al., Reference Peinetti, Pereyra, Kin and Sosa1993; Villagra et al., Reference Villagra, Marone and Cony2002; Campos et al., Reference Campos, Campos, Mongeaud, Borghi, De Los Rios and Giannoni2011; Aguilar et al., Reference Aguilar, Cristóbal-Pérez, Balvino-Olvera, Aguilar-Aguilar, Aguirre-Acosta, Ashworth, Lobo, Martén-Rodríguez, Fuchs, Sanchez-Montoya, Bernardello and Quesada2019). From an economic point of view, Neltuma species represent the most important plant community in Central Argentina. Unlike other woody legumes, the foliage and pods (~18% of protein) are a good source of forage for domestic herbivores (Somlo et al., Reference Somlo, Cohen, Giorgetti, Montenegro and Rodriguez1997). Good adaptation to the extreme environmental conditions, and their ecological and economic importance, give them high potential as candidates for rehabilitating degraded areas.
The study of local adaptation mediated by genotype and environment is relevant to understanding responses to climate change, and for informing conservation and restoration programmes. Seed persistence is one of the key stages in the life history of plants and can be associated with the dormancy strategy. Variation in seed persistence may support bet-hedging strategies, facilitating drought avoidance at xeric sites or those with variable precipitation and temperature regimes (Christie et al., Reference Christie, Pierson, Lowry and Holeski2022). A bet-hedging strategy acts to reduce establishment risk for the seed produced by an individual plant by spreading germination over the growing season or over several years. This reduces short-term reproductive success in favour of longer-term risk reduction. In contrast, short-term seed persistence occurs in species that may depend on other life-history stages for persistence (Saatkamp et al., Reference Saatkamp, Poschlod, Venable, Gallagher and Gallagher2014) and can make a species more vulnerable for in situ conservation in a climate change context (Ooi, Reference Ooi2012; Chen et al., Reference Chen, Hu, Baskin and Baskin2023). Species with a long plant lifespan, or high seed fecundity and dispersal, rely comparatively less on persistent soil seed banks (Chen et al., Reference Chen, Poschlod, Antonelli, Liu and Dickie2020). Arid-semiarid environments seem to evolutionarily select for higher seed persistence in the soil seed bank, and high variability in germination, growth and reproduction as a bet-hedging strategy (Rubio de Casas et al., Reference Rubio de Casas, Willis, Pearse, Baskin, Baskin and Cavender-Bares2017; Klein and Mitchell, Reference Klein and Mitchell2024). In Neltuma species, there are few studies of seed persistence in the soil bank and seedling traits associated with the environment of origin. In general, past studies have been oriented towards the breaking of physical seed dormancy and germination under controlled laboratory conditions (Villagra, Reference Villagra1997; Vilela and Ravetta, Reference Vilela and Ravetta2001; Villalobos and Peláez, Reference Villalobos and Peláez2001; Galindez et al., Reference Galindez, Ceccato, Malagrina, Pidal, Chilo, Bach, Fortunato and Ortega-Baes2016; Boeri et al., Reference Boeri, Cedrés Gazo, Failla, Barrio, Dalzotto and Sharry2019).
The ecological study of native species is crucial for their informed use in the ecological rehabilitation of degraded areas and the management of grasslands to prevent bush encroachment. The transition from seed to seedling is the most critical stage for survival in a Neltuma community (Villalobos and Peláez, Reference Villalobos and Peláez2001). Thus, our objectives were to (i) study the intraspecific variations in persistence in the soil seed bank and early seedling traits in different populations in N. caldenia and N. f. var. depressa collected in the central region of Argentina; and (ii) assess the relationships between the observed variations and environmental conditions and population size of origin as potential drivers of adaptation.
Materials and methods
Seed collections
The study area comprised the central region of Argentina, including the ecoregions of the central Monte Desert, south Espinal and northern Patagonian steppe (Fig. 1). Ripe pods were collected in bulk (>80 pods) from at least 8 specimens from 8 N. caldenia and 12 N. flexuosa var. depressa native populations separated from each other by ~40 m, during 1 month in the summer of 2020 (Supplementary Table S1). Populations were separated by >30 km, to ensure they represented independent genetic structure (Bessega et al., Reference Bessega, Pometti, Campos, Saidman and Vilardi2017). At this period of the season, N. f. var. depressa and N. caldenia individuals have reached fruit maturity and show active vegetative growth (Roig, Reference Roig1993; Steibel and Troiani, Reference Steibel and Troiani1999; Hughes et al., Reference Hughes, Ringelberg, Lewis and Catalano2022).
Figure 1. Seed persistence in the soil seed bank during 6, 12 and 36 months (Mo), and asymptotic exponential nonlinear regression in Neltuma caldenia Burk. (A, B), and N. flexuosa var. depressa F.A. Roig populations (D, E). Different letters indicate significant differences between populations for each burial time (Fisher's least significant difference, LSD, P < 0.05).
The global positioning system (GPS) coordinates were recorded for each population detected (Supplementary Table S1). The descriptive parameters of the populations were (i) latitude and longitude, (ii) altitude, (iii) environmental factors (soil and climate) and (iv) population size, visually by observation of the distribution of the specimens in the field as ‘isolated’, ‘small’ or ‘large’ population size (>~100 specimens per ha) (Leimu and Fischer, Reference Leimu and Fischer2008). In addition, landscape conditions were assessed through the vegetation cover using satellite image analysis. Forest/shrub cover (0-to-100%) was estimated on cloud-free days, in visually homogeneous zones, with EOS Land Viewer services (https://eos.com/landviewer) during the sampling growing period (January-to-February). The images were stored in optical natural colour, and the visual vegetation cover (percent of bare soil) was estimated.
For environmental classification, the WorldClim (http://worldclim.org) version 2.0 database was used. Data were extracted by means of DIVA-GIS software from ESRI grids, with a spatial resolution of 30 arc-seconds (~1 km) in the WGS-84 (EPSG: 4326). Nineteen bioclimatic variables were derived from monthly temperature and rainfall values (Fick and Hijmans, Reference Fick and Hijmans2017). To avoid over-parameterization among the bioclimatic variables, we used Pearson correlation coefficients to measure pairwise correlations between the variables (R, Version 3.5.1), and one of the two paired variables correlated above 0.8 was eliminated. Nine bioclimatic, non-redundant variables used were: annual mean temperature (BIO1), mean diurnal range (mean of monthly (max temp - min temp)) (BIO2), isothermality (BIO3), mean temperature of warmest quarter (BIO10), mean temperature of coldest quarter (BIO11), annual precipitation (BIO12), precipitation seasonality (BIO15), precipitation of warmest quarter (BIO18) and precipitation of coldest quarter (BIO19) (Hijmans et al., Reference Hijmans, Cameron, Parra, Jones and Jarvis2005). The soil parameters of the populations, such as soil texture, pH and bulk density, were obtained from soil databases (FAO/IIASA/ISSCAS/JRC, 2012) using WGS84 and spatial resolution of 30 arc-seconds. For the details, including basic descriptive statistics of each Neltuma population, see Supplementary Table S1.
Seed persistence
After harvest, the pods were incubated under laboratory conditions for 50 days (~22°C) to allow the development of insects throughout the life cycle (from egg to adult) that were potentially infecting the seeds at sampling time (Velez et al., Reference Velez, Chacoff and Campos2018), mainly bruchids (Coleoptera) (Alvarez and Villagra, Reference Alvarez and Villagra2009). Populations were formed from seeds, removed and cleaned by hand from different intact pods. Seed weight was estimated for a sample of 25 seeds (n = 3) for each population (Supplementary Table S2).
The soil seed bank persistence for 3 years was evaluated in all the populations. The seeds used were those without any sign of predation (no exit holes, or depressions) and regular in colour and shape (Velez et al., Reference Velez, Chacoff and Campos2018). To determine initial viability, 30 previously scarified seeds per population were incubated in a germination chamber for 7 days (20°C ± 2; 8 h light/16 h dark) and were considered viable with a visible protrusion of the radicle from the seed coat (≥1 mm). Batches of random samples of 25 seeds (n = 3 for each population and exhumation time) were prepared inside permeable nylon mesh bags (10 × 10 cm), in order to simulate natural soil conditions of air and water diffusion and micro-organism activity. The batches were buried in mid-autumn (23 April 2020) at a depth of 5 cm in sandy loam soil (pH = 7.5, soil organic matter = 1.2%) without any vegetation or leaf litter. The burial site was in the experimental field of INTA EEA Ascasubi (Buenos Aires, Argentina; 39°22′S, 62°39′W). Weather data were recorded at the nearby meteorological station (less than 200 m away) (Supplementary Fig. S1). Seeds were exhumed after 6, 12 and 36 months of burial.
The proportion of PY seeds was assessed. PY seeds (i.e. ‘hard’ or impermeable) were determined by an imbibition test performed at 20 ± 2°C for 2 days (Baskin and Baskin, Reference Baskin and Baskin2014), after which swollen and germinating seeds were recorded and removed. After the exhumation, seed viability was assessed for the remaining non-germinated seeds by scarifying the opposite end of the embryo and placing them in germination chambers for 4 days (20°C ± 2; 8 h’ light/16 h’ dark). The total number of viable seeds consisted of germinated seeds.
Seedling traits evaluation
Seedling elongation tests in the laboratory were conducted in Petri dishes with two layers of Whatman No. 1 filter paper moistened with 10 ml of water. Seeds were previously scarified to avoid a lack of germination imposed by physical dormancy. The seed populations were incubated in a germination chamber (20°C ± 2; 8 h light/16 h dark). To obtain the necessary seedlings, 30 seeds per dish were incubated. Once seedlings with a radicle length of 1 mm were obtained, six representative seedlings were selected per dish and transferred to new Petri dishes (n = 6). The length of seedlings (root + shoot) was measured using a digital calliper following a non-destructive sampling method. The length of each seedling was measured every 24 h for 7 days. The mean seedling elongation rate (mm day−1) was estimated.
Seedling phenotypic traits were evaluated in each population collected (n = 20). The randomly chosen seeds were individually sown in plastic pots (6.5 × 8.0 cm) filled with 35 g of a sterilized substrate mix (Growmix Multipro, Terrafertil). All seedlings were watered three to four times per week until the time of measurement. Forty days after planting, the leaf number per plant, seedling height (cm), aerial (shoot), subterranean (root) and total dry biomass of each seedling were evaluated (n = 10). Then a dry-down experiment to assess seedling survival was conducted in the rest of the replicas (n = 10), imposing a severe drought by completely halting daily watering. No additional watering was added during the survival experiment. Seedlings were monitored on a daily basis. Individuals were scored according to the criteria of Engelbrecht and Kursar (Reference Engelbrecht and Kursar2003) and considered dead when all above-ground parts lost colour and showed no elasticity. To verify seedling death, we subsequently watered each pot to saturation and monitored it for revival (Larson et al., Reference Larson, Anacker, Wanous and Funk2020). Thus, seedling survival was measured daily as a function of days without irrigation. The experiments were conducted in a greenhouse, under a completely randomized design. The temperature was controlled at 20/25°C, photoperiod was a 14-h light:10-h dark cycle.
Statistical analysis
For each population, the percentages of PY (i.e. PY seeds = 100 – (germinated (%) + imbibed seeds (%)) at 6, 12, and 36 months were analysed by Generalized Linear Model (GLM) performed with R version 3.6.1) in Infostat. Population means were compared by Fisher's least significant difference test for seed persistence (Di Rienzo et al., Reference Di Rienzo, Casanoves, Balzarini, Gonzalez, Tablada and Robledo2013). For analyses, the PY data were arcsine -square root transformed, and the untransformed data are presented in the Figures for clarity.
Seed persistence in soil, taking the percentage of initial viability as a starting point, was plotted as a function of burial time (months) with nonlinear models, relating PY seeds remaining over time to an exponential model. The decay function was expressed as:
where Y = persistent seeds (%), Y 0 = Y value when X (time) is zero, k = rate constant, and X = burial time in months. We estimated the half-lives of seed persistence in the soil seedbank (t 0.5) for each population. The exponential growth equation was calculated using GraphPad Prism Software version 8.0 (GraphPad).
Correlations between seed persistence at 6, 12, 36 months, and half-lives for seed persistence, and seedling traits and environment conditions of origin were calculated using Pearson's correlation coefficient, with P < 0.05 set as the significance level. In addition, a principal component analysis (PCA) was performed with seedling traits and selected bioclimatic variables (BIO1, 2, 3, 10, 11, 12, 15, 18 and 19) in relation to seed persistence using InfoStat software.
Linear regression analysis between vegetation cover and seed persistence (t 0.5) was performed by species using GraphPad Prism Software version 8.0 (GraphPad).
Results
Seed persistence
Initial seed viability was over 87% in all cases (Supplementary Table S2). The seed persistence in the soil ranged between 0-to-72% in N. caldenia and 0-to-64% in N. f. var depressa at the third year of burial, with differences found between populations in both species (Fig. 1). The persistence in the soil seedbank obtained at 6 and 12 months correlated with those of the third year in both species (r > 0.71**), and with the seed half-life in the soil (t 0.5) (r > 0.91**) (Supplementary Tables S3 and S4).
In both species, we observed a geographical gradient in seed persistence associated with latitude, longitude, and altitude (Fig. 2). Seed persistence increased in the east-to-west (latitude; r = 0.75*, and r = 0.79**) and south-to-north (longitude; r = 0.83** and r = 0.79**) directions, correlated with higher altitude (r = 0.72* and r = 0.80**) within the range of 11 to 1512 m above sea level.
Figure 2. Geographic localization of Neltuma caldenia Burk. (grey) and N. flexuosa var. depressa F.A. Roig populations (black). The size of the circle in each population is related to the seed persistence in the soil bank after 3 years of burial.
Seed persistence and seedling traits
In N. caldenia, seed persistence was positively associated with seedling elongation rate (r = 0.73*). Higher initial seedling growth was correlated with seedling height (r = 0.77*). Conversely, in N. f. var. depressa, we observed a negative association between seed persistence and seedling height (r = −0.64*). Seedling heights were directly associated with shoot, root, and total seedling weight in both species. We did not find a relationship between seed weight and seedling elongation rate for either species (P > 0.05) (Fig. 3).
Figure 3. Biplot of Neltuma caldenia Burk. (A), and N. flexuosa var. depressa F.A. Roig (B) seed persistence ranges on the first two principal components (80.9 and 74.4%) based on seedling traits in early growth stage. In bold letters the trait that shows a significant correlation with seed persistence (P < 0.05).
Relationship between seed persistence and environment
Populations of N. f. var depressa were located in arid environments (281 ± 77 mm year−1) in contrast to those of N. caldenia which were found in semiarid environments (445 ± 98 mm year−1) (Fig. 2). The populations with the highest seed persistence originated in the environment with a highest mean diurnal range (r = 0.84**), isothermality (r = 0.85**) and mean temperature of the warmest quarter (summer) (r = 0.70*) in N. caldenia (Fig. 4A). In N. f. var depressa, a higher seed persistence was associated with a higher mean diurnal range (r = 0.74**), isothermality (r = 0.89**), precipitation seasonality (r = 0.76**), precipitation of the coldest quarter (r = 0.67*), lower annual mean temperature (r = −0.64*) and mean temperature of the coldest quarter (r = −0.71*) (Fig. 4B, and Supplementary Table S3).
Figure 4. Biplot of Neltuma caldenia Burk. (A), and N. flexuosa DC. var. depressa F.A. Roig (B) seed persistence ranges on the first two principal components (80.9 and 74.4%) based on bioclimatic variables (BIOs 1, 2, 3, 10, 11, 12, 15, 18 and 19). In bold letters the BIO that shows a significant correlation with seed persistence (P < 0.05).
We observed that the plants of N. f. var depressa populations located in the northwest (Bar, Cha, E.Ma, and E.So) showed an isolated distribution, associated with a lower vegetation cover (≤25%). Higher seed persistence was associated with a lower vegetation cover (Fig. 5).
Figure 5. Relationship between half-lives for seed persistence in the soil seedbank (t 0.5) in Neltuma caldenia Burk. (grey), and N. flexuosa var. depressa F.A. Roig populations (black) and vegetation cover estimated in a hectare area (circle).
Discussion
The climate of the sites varies from subhumid to arid conditions, the latter with only 150 mm of rainfall per year. Seed persistence in both species showed clinal trends increasing in a north-westerly (NW) direction (Fig. 2). This was associated with the natural plant community that also showed an ecological cline between grass steppe with woody species and xerophytic trees (Larrea spp. Cav., Bulnesia spp. C. Gay, Neltuma spp. L., Cercidium spp. Tul and Geoffroea spp. Jacq.) in the east and arid steppe in the west (Anderson et al., Reference Anderson, Bonvissuto, Brizuela, Chiossone, Cibils, Cid, Feldman, Fernández Grecco, Kunst, Oesterheld, Oliva, Paruelo, Peinetti and Villagra2011; Torres Robles et al., Reference Torres Robles, Arturi, Contreras, Peter and Zebedio2022). The higher seed persistence for north-western populations of N. caldenia was found to be associated with strong seasonality with large temperature swings and hot summers, showing a more extreme and less stable environment. In N. f. var depressa, we observed that the populations located in the northwest showed greater seed persistence (Fig. 2), associated with cold climates with variable and extreme thermal conditions, and also a marked variability in precipitation, with higher records during the winter. This result is consistent with findings in legume species adapted to aridity, which is likely to be an advantage in unpredictable environments (Villagra et al., Reference Villagra, Vilela, Giordano, Álvarez and Ramawat2010; Rubio de Casas et al., Reference Rubio de Casas, Willis, Pearse, Baskin, Baskin and Cavender-Bares2017; Renzi et al., Reference Renzi, Brus, Duchoslav, Pirintsos, Erdős and Smýkal2020). We cannot separate the genetic and environmental factors of seed persistence in both species, which involve either local genetic adaptation or phenotypic plasticity associated with maternal effects. However, seed persistence variation underscores the ecological strategies adopted for adapting to diverse environmental constraints. Maternal effects in transgenerational studies in perennial species would probably be smaller in magnitude than in annual species (Yin et al., Reference Yin, Zhou, Lin, Li and Zhang2019).
The persistent soil seed bank, with more than 30% of seeds intact and viable after 3 years of burial, was observed in the 37% of N. caldenia and in 42% of N. f. var depressa populations (Fig. 1). Only one N. caldenia population and two N. f. var depressa populations showed <10% intact seeds after 1 year, forming short-term seed banks (Baskin and Baskin, Reference Baskin and Baskin2014). Seed bank persistence in Neltuma taxa would be species and population-dependent (Lerner and Peinetti, Reference Lerner and Peinetti1996; Villagra et al., Reference Villagra, Marone and Cony2002; Renzi et al., Reference Renzi, Reinoso, Quintana and Cantamutto2023). Spontaneous regeneration from the soil seed banks will be higher in the northern populations. When the soil seed bank is exhausted, seed-based rehabilitation programmes constitute one of the more promising and economic models for dryland restoration (Golos et al., Reference Golos, Dixon and Erickson2016; Busso and Pérez, Reference Busso and Pérez2018; Pérez et al., Reference Pérez, Pilustrelli, Farinaccio, Sabino and Aronson2019, Reference Pérez, Ceballos and Oneto2022). Within the framework of these rehabilitation objectives, candidate taxa should preferably be selected from species of the natural flora of the surrounding non-degraded environment, which would ensure their adaptation to the conditions in which they will be released (Cortina et al., Reference Cortina, Bellot, Vilagrosa, Caturla, Maestre, Rubio, de Urbina JM, Bonet, Vallejo and Alloza2004). However, it is important to consider the ecological adaptation of a native species to help define the propagule collection strategy (Woolridge et al., Reference Woolridge, Fant, Flores, Schultz and Kramer2022).
We observed a divergent trade-off between soil seed bank persistence and seedling traits in Neltuma species, related to the environmental conditions and population size, estimated by vegetation cover. Seed persistence was not associated with seed weight (P > 0.05) for the range evaluated in N. caldenia (15–39 mg seed−1) and N. f. var depressa (18–44 mg seed−1). However, this should be corroborated in future analyses with a larger number of replicates and seeds per replicate in each population and in different years. These results are consistent with the analysis conducted by Chen et al. (Reference Chen, Hu, Baskin and Baskin2023), who studied 349 species, many of which were legumes (~14%). Although we did not find a relationship between seed weight and persistence or initial seedling growth, it is well established that seed weight plays a significant role in various ecological processes, benefiting early life stage fitness and enhancing seedling survival (Christie et al., Reference Christie, Pierson, Lowry and Holeski2022). Nonetheless, it is important to note that these relationships are highly context-dependent (Chen et al., Reference Chen, Hu, Baskin and Baskin2023).
All the N. caldenia surveyed were found at sites with a large population size and high vegetation cover (Fig. 4). Higher persistence in an unpredictable environment observed in N. caldenia may require greater vigour at emergence to ensure reproductive success. It is during seedling establishment that most mortality occurs, and this could be an adaptive mechanism (Villalobos and Peláez, Reference Villalobos and Peláez2001; Lewandrowski et al., Reference Lewandrowski, Stevens, Webber, Dalziell, Trudgen, Bateman and Erickson2021). Rapid seedling growth may help escape drought by enabling a greater depth of soil moisture to be reached and would confer a high relative competitive ability, especially if thermal conditions for initial growth are limited. In arid environments with Plantago patagonica, it was also observed that higher seedling height was a significant predictor of survival under early-season drought (Christie et al., Reference Christie, Pierson, Lowry and Holeski2022). Studies under natural conditions should be performed on Neltuma species in the future.
The northwest populations of N. f. var depressa, situated at the ecological niche boundary (Renzi et al., Reference Renzi, Reinoso, Quintana and Cantamutto2023), exhibited higher seed persistence associated with lower seedling height (−18.5%; Fig. 3B). In sites with low vegetation cover (isolated habitat), seedlings are likely to face relatively little competition during establishment and will therefore require less height in the early stages of life (Christie et al., Reference Christie, Pierson, Lowry and Holeski2022). However, a more plausible explanation could be that animal-pollinated trees or shrubs in small populations or isolated conditions tend to decrease outcrossing rates, thereby increasing the inbreeding coefficients of the generated offspring (Angeloni et al., Reference Angeloni, Ouborg and Leimu2011). This did not occur in our study of N. caldenia because the populations collected were in a continuous forest in the middle of its ecological niche distribution of species (Dussart et al., Reference Dussart, Medina and Bogino2015). Consistent with our results, Aguilar et al. (Reference Aguilar, Cristóbal-Pérez, Balvino-Olvera, Aguilar-Aguilar, Aguirre-Acosta, Ashworth, Lobo, Martén-Rodríguez, Fuchs, Sanchez-Montoya, Bernardello and Quesada2019) observed that the progeny of fragmented and isolated populations of N. caldenia showed lower seedling growth compared to continuous forest areas due to inbreeding depression. The extent of progeny vigour decrease may depend on landscape fragmentation, mating system, presence of potential pollinators in outcrossing species (obligate > facultative), and the number of generations post-fragmentation (Rocha and Aguilar, Reference Rocha and Aguilar2001; Broadhurst et al., Reference Broadhurst, Young and Forrester2008; Aguilar et al., Reference Aguilar, Cristóbal-Pérez, Balvino-Olvera, Aguilar-Aguilar, Aguirre-Acosta, Ashworth, Lobo, Martén-Rodríguez, Fuchs, Sanchez-Montoya, Bernardello and Quesada2019; Doyle et al., Reference Doyle, Yap, Bragg, Rossetto, Orme and Ooi2023). The effect on population size would not be evident in seed germination (Baskin and Baskin, Reference Baskin and Baskin2024) and seed dormancy, which could be attributed to maternal inheritance and environmental control (Bewley and Black, Reference Bewley and Black1994; Iwasaki et al., Reference Iwasaki, Penfield and Lopez-Molina2022).
The rehabilitation of degraded or small populations of Neltuma specimens will usually require the collection of seeds from similar environmental settings (Cortina et al., Reference Cortina, Bellot, Vilagrosa, Caturla, Maestre, Rubio, de Urbina JM, Bonet, Vallejo and Alloza2004). The seed-collection environment has strong effects on seedling performance (Klein and Mitchell, Reference Klein and Mitchell2024). More arid and unstable environments will have seeds with greater persistence in the soil seed bank and with the suitable seedling traits for establishment in the face of environmental variability. In addition to the environment, population size must be considered during collection, ensuring it corresponds to a large population to avoid the effects of inbreeding depression in the progeny fitness and the possibility of maladaptation effects (Leimu and Fischer, Reference Leimu and Fischer2008; Alves et al., Reference Alves, Sartori, Zucchi, Azevedo-Tozzi, Tambarussi and de Souza2018).
Conclusions
Neltuma populations in central Argentina are expected to continue to face severe precipitation and thermal variability associated with global climate change (Soliani et al., Reference Soliani, Ceccarelli, Lantschner, Thomas and Marchelli2024). Our results show a different response depending on the species and populations associated with environmental conditions and population size. In arid and unstable environments, it is expected that the seed bank will be more persistent. Natural regeneration could form small plant patches that would improve the microenvironment and facilitate the establishment of a ring of pasture around the trees or shrubs (Busso and Pérez, Reference Busso and Pérez2018). However, when complete exhaustion of the soil seed bank occurs, it will require seed-based rehabilitation programmes. In this scenario, seed collection would have to be undertaken in large populations close to the rehabilitation area, to avoid collection of seeds from isolated specimens (Alves et al., Reference Alves, Sartori, Zucchi, Azevedo-Tozzi, Tambarussi and de Souza2018). Regeneration mediated by the seed bank could vary depending on the environment and seed persistence. The collection of isolated plants or small populations of Neltuma adapted to an arid environment and used as germplasm may have undesirable implications in the progeny performance, due to inbreeding depressions (Bessega et al., Reference Bessega, Pometti, Campos, Saidman and Vilardi2017). Further studies on seed persistence and associated plant traits under natural conditions are needed with a holistic approach considering the interactions between genotype, environment, and landscape conditions. A finer description of population size and habitat heterogeneity would be desirable in subsequent studies.
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S0960258524000205.
Data availability statement
The data that support the findings of this study are openly available in the supplementary material.
Acknowledgements
The study reported in this manuscript was supported by the Instituto Nacional de Tecnología Agropecuaria (PD I100 and PD I98) and Universidad Nacional del Sur of Argentina (PGI 24/A271). The authors would like to thank Rosemary Scoffield for the English language review.
Competing interests
None.
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