Influence of storage and temperature on the germination of a macrophyte seed bank from a temporary pond in the Brazilian semiaridAbstract
Seed bank (SB) formation in temporary ponds is key to the local resilience of macrophyte species after drought disturbance. Studying seed germinability and its response to temperature is crucial to understanding regeneration strategies in wetlands, where seed banks play a central role. The objective of this work was to evaluate, through two experiments, the effect of storage period and temperature on the germination of the macrophyte seed bank from a temporary pond in the Brazilian semiarid region. In the first experiment, germinability was compared between fresh samples and samples stored in a cold chamber. In the second experiment, the effect of temperature on germination was evaluated using stored sediment. The fresh SB showed higher richness and lower seedling density than the stored sample. The higher temperature treatment (37 °C) led to higher richness and seedling density. Lemna sp. and Heteranthera limosa were the only species that germinated and emerged from the SB under all tested temperature conditions. The study concluded that cold storage can aid the conservation of temporary pond seed banks and that, within the temperature range, seed bank germinability was maintained under elevated temperatures representative of projected climate scenarios.
Keywords:
Caatinga; ex situ conservation; resilience seeds; seed germinability; temporary wetlands
Introduction
Aquatic habitats subjected to cycles of flooding and drought are defined as temporary ecosystems and are often classified as biodiversity hotspots due to their unique ecological dynamics (Lukács et al., 2013; Calhoun et al., 2017; Parra et al., 2021). Temporary habitats are distributed globally, and are especially numerous in regions with highly seasonal climates, such as semiarid drylands (Lumbreras et al., 2016; Albuquerque et al., 2020). The temporary ponds in drylands formed during rainy seasons are shallow and isolated from any terrestrial water source, and usually evaporate completely during the dry season (Tabosa et al., 2012; Carta, 2016). Despite their ecological importance, temporary ponds are increasingly threatened by human pressures such as land-use change, agricultural intensification, water extraction, and pollution (Bagella et al., 2016).
In Brazil, temporary ponds are common in the semiarid northeastern region, where the soil is typically shallow, and rainfall is low, with a long dry season, spanning from 8 to 10 months of the year (Maltchik, 2000). The plants in these ponds are mainly macrophytes, which are aquatic plants visible to the naked eye that grow fully or partially submerged in aquatic environments (Esteves, 2011). These species rely on rapid life cycles to develop and release seeds/propagules before the end of the rainy season (Esteves, 2011; Tabosa et al., 2012). The accumulation of desiccation-resistant propagules, such as seeds and spores of macrophytes, in the dried sediment of temporary ponds contributes to the formation of a soil seed bank (Ferreira & Catian, 2016).
Propagule banks are natural reserves of viable reproductive units found in the soil, including seeds and spores, capable of germinating and forming new plants when environmental conditions are favorable for germination (Douh et al., 2018). These propagules play an essential role in vegetation regeneration, allowing species persistence during adverse periods until conditions permit germination and reestablishment of aquatic vegetation (Fernández-Zamudio et al., 2018). Thus, they contribute to the maintenance of biodiversity, facilitate the recolonization of disturbed habitats, and support the functional stability of aquatic ecosystems (Bonis et al., 1995; Duarte et al., 2020).
Seed banks consist of transient seeds, which remain viable in the soil for up to one year, and persistent seeds, which survive for many years by enduring multiple wet-dry cycles, allowing germination to occur over extended periods (Vandvik et al., 2016; Baskin et al., 2019; Wang et al., 2020). Certain macrophyte species produce orthodox seeds, characterized by their ability to tolerate desiccation and low temperatures, thereby facilitating their storage and long-term viability in ex situ conservation (Hay et al., 2000; Tuckett et al., 2010; Carta et al., 2013). In the case of temporary pond sediment in drylands, these seed banks are predominantly formed by persistent seeds, and storing sediment samples dry at room temperature is often sufficient to preserve their viability (Brock, 2011).
Semiarid regions are expected to be disproportionately affected by climate change, characterized by rising temperatures, reduced rainfall, and decreased soil moisture (Scholes, 2020). These changes intensify evaporation and accelerate the desiccation of aquatic environments, including temporary ponds (Marengo et al., 2017; Ouhamdouch & Bahir, 2017; Xia et al., 2017). Such alterations threaten the persistence of macrophyte populations and their associated soil seed banks, which are essential for long-term ecosystem resilience. The reduction in seed bank density not only compromises the regenerative capacity of these systems but also heightens the extinction risk for species dependent on temporary aquatic habitats (Faist & Collinge, 2015; Calhoun et al., 2017; Grillas et al., 2021).
In addition to reductions in seed bank density, climate change may also impact seed viability and germination behavior. Extreme temperatures, both high and low, can inhibit germination of various species (Tuckett et al., 2010). Exposure to low temperatures can reduce enzymatic activity and metabolism in seeds, which may result in the inhibition of the germination process (Liu et al., 2022). Subsequently, rising global temperatures may drastically alter seed behavior within soil seed banks, disrupting the balance between quiescent and dormant states, or between germination and seedling survival following rainfall events (Walck et al., 2011; Ooi, 2012). For example, seeds may germinate in response to brief rainfall, but insufficient soil moisture may lead to high seedling mortality. (Ooi et al., 2009; Akinyemi et al., 2019). Investigating the composition and ecological dynamics of seed banks in temporary ponds is therefore essential for understanding the ecological history and resilience of these unique habitats. Furthermore, the evaluation of the seeds contained in seed banks provides insights into their long-term viability and supports the development of ex situ conservation strategies.
Therefore, this study aimed to evaluate the germination capacity of aquatic macrophyte seed banks after three and four years of cold storage and their ecological response to varying temperatures. Specifically, the objectives were: i) to evaluate whether seed banks composed of macrophyte propagules germinate after storage for three years in a cold chamber; and ii) to evaluate the ecological response of these seed banks after four years of storage when subjected to different temperatures (17 °C and 37 °C). Our hypotheses are: i) the macrophyte seed bank maintains germinability after at least three years of storage under cold-chamber conditions (10 ± 2 °C and 20% RH); and ii) seedling emergence responses differ among the temperature regimes tested.
Materials and Methods
Study Area
The study was carried out in a temporary pond undergoing eutrophication, located in the municipality of Sobradinho (9°27'29" S, 40°48'29" W, elevation 371 m), state of Bahia, Brazil. The pond has an area of 0.175 ha, a perimeter of 239 m, a maximum water depth of 0.6 m, and a volume of 370 m³. This temporary pond was chosen for the study, among other accessible ponds, because it showed a seed bank with high density and species richness of macrophytes (Pereira, 2017). The local biome is classified as a seasonally dry tropical forest in the Caatinga phytogeographic domain (Pennington et al., 2000). According to the Köppen scale, the climate in the region is BSh (hot semiarid), with high temperatures, long dry periods, and irregular rainfall, concentrated from December to March. Average annual temperature and rainfall are 27 °C and 800 mm, respectively (Alvares et al., 2013; Pinheiro et al., 2020).
Seed bank (SB) sampling
In September 2014, during the dry phase of the temporary pond, when the substrate was completely dry under natural conditions, we collected 20 sediment samples from the bed of the dried temporary pond within a 250 m² sampling plot located in the undisturbed deepest region of the lagoon, avoiding the margins that had been traversed by animals and people. The samples were randomly collected within this plot using a post hole digger (0.11 m diameter) at a depth of up to 0.1 m, resulting in a sampled volume of approximately 9.51 × 10⁻⁴ m³ per core (corresponding to an area of 0.044404 m²). Each one of the sediment samples was then sieved and homogenized after removal of pebbles and rhizomes. Immediately after collection, part of the samples was used to evaluate seedling emergence from the fresh seed bank (FSB). The remaining samples were stored in sealed plastic bags under controlled cold conditions (10 ± 2 °C and 20% relative humidity) and later used in two independent experiments: one conducted after three years of cold storage, in September 2017 (Experiment 1), and another conducted after four years of storage under cold conditions (10 ± 2 °C and 20% relative humidity), in September 2018 (Experiment 2). Each experiment addressed distinct objectives and was analyzed independently.
Evaluation of the seed banks
Fresh and/or stored samples were assessed in two independent experiments, as described below. In both experiments, germination was defined as seedling emergence, and seed bank composition was assessed based on all seedlings that emerged during a six-week monitoring period, following the criteria of Gross (1990) . Each of the 20 samples was considered an experimental unit (∼replicate). Each experimental unit consisted of 150 mL of pond sediment, measured using a graduated beaker, mixed with 150 mL of expanded low-density vermiculite. The mixture was placed in individual rectangular aluminum trays (203 × 133 mm, 4.2 cm depth), evenly distributed to form a 3 cm-deep layer, and covered with a 1 cm layer of tap water.
Vermiculite was mixed with the sediment to improve substrate aeration, prevent compaction during flooding, and facilitate uniform seedling emergence. Control trays containing only vermiculite and the same water layer were randomly distributed among the experimental units to confirm that all emerged seedlings originated from the sediment samples. Each experiment lasted 42 days (six weeks). Seedling emergence was monitored weekly, and to prevent feedback sowing, all emerged seedlings were removed every 15 days, resulting in three removal events during the experimental period.
The emerged plants were identified at the genus or species level, following Bueno et al. (2011) , Souza & Lorenzi (2012) , and Flora and Funga of Brasil (2022). When diagnostic morphological characters were insufficient for species-level identification at early developmental stages, individuals were recorded at the genus level (e.g., Ludwigia sp.). The density was estimated using the seedling emergence method proposed by Van Der Valk & Davis (1978) , in which viable propagules are quantified through seedling emergence under controlled conditions. Values were standardized and expressed as seedlings per square meter (seedlings m⁻²) based on the sampled sediment surface area. The species richness (S) was determined according to the number of species germinated.
Experiment 1. Effect of seed bank storage on the emergence of seedlings
In Experiment 1, seedling emergence from the fresh seed bank (FSB) was evaluated shortly after sample collection in September 2014. The same sediment samples were then stored for three years in the dark in a cold chamber (Model RLC-050-B, MC Quay, São José dos Campos, Brazil) at 10 ± 2 °C and 20% relative humidity, yielding the stored seed bank (SSB). Seedling emergence from FSB (2014) and SSB (2017) was assessed under comparable environmental conditions in a polyethylene-covered greenhouse with 50% shading, during the same season, at an average temperature of 27 ± 2 °C and a 12-hour photoperiod. These assessments were compared in terms of seedling density and species composition.
Experiment 2. Effect of temperature on the emergence of seedlings
In Experiment 2, seed bank samples stored for four years in a cold chamber at 10 ± 2 °C and 20% relative humidity (from September 2014 to September 2018) were assessed under contrasting temperature conditions representing the minimum and maximum average temperatures recorded at the collection site (Embrapa, 2025). Seedling emergence and seed bank composition were evaluated either in a controlled germination room at a constant temperature of 17 °C (SB17) or in a glass greenhouse under natural light and naturally fluctuating temperatures, with a mean ambient temperature of approximately 37 °C (SB37).
Statistical analysis
Before analysis, data from Experiment 1 were evaluated for normality using the Shapiro-Wilk test at a 5% significance level. The residuals met the assumptions of normality (p > 0.05), allowing the use of parametric statistics. Therefore, differences in mean seedling density between the fresh seed bank (FSB) and the stored seed bank (SSB) were assessed using an independent-samples t-test.
To analyze the effect of temperature on seedling emergence from the SB17 and SB37 samples, we applied generalized linear modeling (GLM) to fit the data, after confirming data residuals with non-normal distribution (W = 0.764; p < 0.001) and non-homogeneous variances (L = 27.855; p < 0.001) (Shapiro & Wilk, 1965; Levene, 1960). Therefore, we chose not to use the angular transformation for the response variable. (Silva et al., 2022a). The distribution and link function were the quasibinomial distribution with the logit link function. After the GLM, the significant differences between temperatures were evaluated by pairwise comparison of the means by the post-hoc Tukey test at 5% significance. The means followed by the standard errors of the mean were fitted by theŠidák method (Šidák, 1967). All the statistical procedures were carried out with the R software (R Core Team, 2022). The following R packages were used to carry out the analyses: car (Fox & Weisberg, 2019), fBasics (Wuertz et al., 2023), nortest (Gross & Ligges, 2015), boot (Canty, 2002), emmeans (Lenth, 2024), multcomp (Hothorn et al., 2008), and multcompView (Graves et al., 2023).
Results
Experiment 1. Effect of seed bank storage on the emergence of seedlings
A total of 15 taxa were recorded in the fresh seed bank (FSB), whereas seven taxa emerged from the stored seed bank (SSB) after three years of cold storage (Table 1). The species identified belonged to ten families, with Onagraceae and Poaceae showing the highest richness in FSB, while Araceae was the most representative family in SSB.
List of species of aquatic plants, biological forms (BF), density (seedlings/ m2) by species and richness (S) of Fresh seed bank (FSB) and stored seed bank (SSB). Biological forms (Fb): fixed submerged (SF); free submerged (SL); fixed floating (FF); free floating (FL); amphibious (A); emergent (E). Fresh seed bank samples (FSB), stored seed bank (SSB).
The FSB comprised a wide range of biological forms, including emergent, amphibious, free-floating, fixed-floating, and submerged species. In contrast, the SSB was mainly composed of free-floating and emergent species, indicating a shift in seed bank composition after storage (Table 1).
In terms of density, the most abundant taxa in the FSB were Azolla sp. and Heteranthera limosa, whereas in the SSB, Azolla sp. and Lemna sp. showed the highest emergence values (Table 1). These results indicate changes not only in species richness but also in the dominance structure of the seed bank after storage.
Mean total seedling density did not differ significantly between the stored seed bank (SSB) and the fresh seed bank (FSB) (t-test, t(19) = −0.99, p > 0.05), although higher values were observed in the SSB (3076.9 seedlings m⁻²) than in the FSB (1558.6 seedlings m⁻²) (Fig. 1). Several species showed contrasting responses to storage, with Lemna sp., Heteranthera limosa, and Azolla sp. presenting higher densities in SSB, while other taxa emerged exclusively in FSB (Table 1).
Total seedling density (mean ± standard error) according to treatments in Experiments 1 (Effect of seed bank storage on the emergence of seedlings) and 2 (Effect of temperature on the emergence of seedlings). FSB: fresh seed bank; SSB: stored seed bank; SB17: seed bank germinated in a growth room at a constant temperature of 17°C; SB37: seed bank germinated at an average temperature of 37°C.
Experiment 2. Effect of temperature on the emergence of seedlings
Seed bank samples exposed to contrasting temperature regimes exhibited pronounced differences in species richness, taxonomic composition, and biological forms (Table 2). Germination at 37°C (SB37) resulted in the emergence of nine taxa distributed among five families, whereas only three taxa belonging to three families emerged at 17 °C (SB17). Free-floating and emergent life forms predominated under SB37 conditions, while germination at SB17 was restricted mainly to emergent and amphibious forms.
List of species of aquatic plants, biological forms (BF), density (seedlings/ m2) by species and richness (S) of the seed bank placed to germinate at 17°C (SB17) and 37°C (SB37). Biological forms (BF): fixed submerged (SF); free submerged (SL); fixed floating (FF); free floating (FL); amphibious (A); emergent. Germination room at constant temperature of 17 °C (SB17), germination with average temperature of 37 °C (SB37).
At 37°C, Lemna sp. and Azolla sp. were the most abundant taxa, with densities of 2082.69 and 746.15 seedlings m⁻², respectively, followed by Heteranthera limosa (355.77 seedlings m⁻²). In contrast, seedling emergence at 17 °C was extremely limited, with only Lemna sp., H. limosa, and one morphospecies recorded, all presenting very low densities (≤ 7.69 seedlings m⁻²) (Table 2).
Temperature had a significant effect on total seedling density (GLM, p < 0.001). The average density observed under SB37 conditions (3305.77 seedlings m⁻²) was more than 200 times higher than that recorded at SB17 (11.53 seedlings m⁻²) (Fig. 1). Pairwise comparisons confirmed significant differences between the two temperature treatments.
Discussion
Effect of seed bank storage on the emergence of seedlings
Seed banks in pond sediments represent a natural strategy for preserving plant biodiversity, especially in dynamic or disturbed habitats (Wakshum et al., 2018). These banks act as a genetic reservoir for vegetation regeneration in subsequent hydrological cycles or in degraded areas (Wang et al., 2015; Carta, 2016). Our findings demonstrate that the seed bank preserved its germination capacity both after three years and after four years of cold storage, under favorable conditions. This long-term persistence highlights the potential use of sediment seed banks for the restoration of aquatic environments and for the ex situ conservation of native aquatic plants.
The storage conditions adopted, sediment samples collected during the natural dry phase of the pond, and sealed in plastic bags, likely helped preserve seed germinability by preventing moisture fluctuation and limiting gas exchange (Mbofung et al., 2013). Additionally, low temperatures reduce seeds’ metabolic activity, preventing aging by oxidation and degradation of membranes (Silva et al., 2022b). This conservation strategy is particularly suitable for orthodox seeds, which are characterized by their ability to tolerate desiccation and remain viable under low-moisture, low-temperature conditions (Mayrinck et al., 2019). According to available reports, a substantial proportion of macrophyte species exhibit orthodox seed behavior (Hay et al., 2000), which may partially explain the potential for long-term cold storage observed in our study. The comparable emergence patterns of FSB and SSB (Table 1) suggest that seeds in this temporary seed bank are resilient to long-term storage under cold conditions, corroborating previous findings on aquatic plant species stored at low temperatures (Zhao et al., 2017). Interestingly, the density of Lemna sp. markedly increased after storage (Table 1), rising from 198.77 individuals in the fresh seed bank to 1000.00 in the stored seed bank. This pattern may indicate a possible dormancy release promoted by prolonged exposure to low temperatures, resembling cold stratification effects reported for some aquatic species. However, since dormancy mechanisms were not directly evaluated in this study, this interpretation should be considered with caution.
Despite the maintenance of germination capacity, a decline in species richness was observed after storage. It is important to emphasize that the evaluation of the seed bank was based exclusively on seedling emergence. We did not perform direct viability tests on the remaining sediment after the experiment; therefore, it was not possible to determine whether non-emerging propagules were dead or remained dormant under the tested conditions. The absence of germination in certain species may be related to factors such as the death of vegetative propagules, as described for seeds of Ocotea puberula (Rich.) (Vicente et al., 2016), or to the presence of secondary dormancy, as observed in species of Beta vulgaris L. (Hourston et al., 2022). For some species, such as Alternanthera philoxeroides, Ludwigia octovalvis, L. peploides, Eleocharis elegans, and E. minima, the low seedling emergence recorded in the FSB suggests that these species were already present at low densities in the sediment bank. Species with initially low emergence may be more susceptible to local disappearance after prolonged storage due to reduced propagule persistence or viability loss over time. Additionally, sensitivity to cold temperatures (Pistia stratiotes, Chara sp.) and intrinsically low seed longevity (Nymphaea sp.) may have contributed to species loss (Kan & Song, 2008; Sederias & Colman, 2007; Dalziell et al., 2019).
Ecological significance and conservation under environmental change
Beyond their ecological value for biodiversity maintenance, temporary ponds also offer essential ecosystem services, such as water provision for human use, livestock, and agriculture (Lumbreras et al., 2016). However, anthropogenic pressures, such as water extraction and agriculture in nearby areas, can eutrophicate these habitats and reduce their hydroperiods, affecting plant reproductive success and seed production (Bouahim et al., 2014). Climate change further intensifies these challenges, with increased temperatures and prolonged droughts leading to shorter inundation periods and greater desiccation risk (Bagella et al., 2016; Grillas et al., 2021). Under these scenarios, ex situ storage of seed banks emerges as a vital conservation strategy, enabling the preservation of viable propagules that might otherwise be lost during extreme climate events. Our findings support the feasibility of storing sediment-derived seed banks for at least three to four years, providing a reservoir for future restoration efforts in ephemeral wetlands.
Germination under elevated temperature scenarios
In the most optimistic climate change scenario for Brazil’s semi-arid region, average annual air temperature is expected to increase by at least 1.5 °C, and in the worst scenario, by up to 5 °C, reaching 32 °C by 2040 (IPCC, 2021). In this context, our results (Fig. 1, Table 2) revealed that seeds remained viable and germinated at both tested temperatures (17 °C and 37 °C); however, since only two temperature points were evaluated, no inference about thermal limits (Tb or Tmax) can be drawn. This aligns with evidence that aquatic macrophytes exhibit broad thermal tolerance, occupying habitats ranging from extreme deserts (~58 °C) to subpolar zones (Murph et al., 2019). It is worth noting that fewer than 2% of macrophyte species have a global distribution, indicating that thermal tolerance is often linked to local adaptation (Murph et al., 2019).
Previous studies have reported that germination in aquatic macrophytes generally occurs within a temperature range of approximately 15 to 40 °C, with an optimum near 24 °C (Baskin & Baskin, 2014), although these thresholds may vary considerably among species. Our results indicate that several species present in the studied pond are likely adapted to the local tropical semi-arid climate, where daily temperatures frequently exceed 30 °C (Lucena et al., 2021). This may have led to the high germination density observed under SB37 conditions (Fig. 1, Table 2). Temperature effects on seed germination reflect species-specific physiological adaptations to local environmental conditions and ecological niches (Oliveira et al., 2014). In the Caatinga, for example, native dry forest species often exhibit optimal germination near 35 °C (Dantas et al., 2020). The combined effects of seasonality, hydrological variation, and alternating drought/flooding cycles likely promote the selection and development of physiologically resilient seed banks in these regions.
Species-specific responses and implications for management
In all experimental conditions (FSB, SSB, SB17, and SB37), both H. limosa and Lemna sp. successfully germinated. While H. limosa is known to produce dormant and persistent seeds, species within the genus Lemna often rely on vegetative reproduction and a short life cycle (Rejmánková, 1976; Baskin et al., 2003). Nonetheless, both species have global distributions and appear to exhibit broad thermal germination windows, as confirmed by their performance at 17 °C (Table 2). Among them, Lemna sp. showed significantly higher germination at 37 °C, which may also indicate thermotolerance or ecological plasticity (Ziegler et al., 2023).
The considerable density of Azolla in both experiments also deserves attention. As an aquatic fern, Azolla reproduces through resistant sporocarps that can persist in sediments during dry phases (Dyer, 1994). Its consistent emergence in both fresh and stored seed banks suggests effective survival of these propagules under cold storage conditions. This resilience may contribute to rapid recolonization following rewetting events, reinforcing the ecological importance of sediment banks for maintaining functional diversity in temporary ponds.
Interestingly, the difference in seedling density between SSB (27 °C) and SB37 was relatively small (~229 seedlings/m²), reinforcing the notion that seed banks from temporary ponds in semi-arid regions can retain germinability for at least four years when stored under cold conditions (Fig. 1).
Practical applications for conservation and restoration
The successful germination of seed banks after prolonged cold storage reinforces the potential use of sediment seed banks as an accessible and cost-effective source of native plant material for ecological restoration. In semi-arid regions, where hydrological variability and habitat degradation increasingly threaten aquatic biodiversity, sediment-based seed banks may serve as natural repositories of local genetic diversity (Brock, 2011; Faist et al., 2013; Fernández-Zamudio et al., 2018). These banks can be integrated into regional germplasm collections to support the conservation of aquatic macrophytes adapted to temporary water bodies. Moreover, their use in restoration initiatives, such as the rewetting of degraded wetlands or the recovery of seasonal ponds, could enhance the resilience and ecological integrity of these systems by ensuring the reestablishment of native species.
Our findings indicate that the seed bank as a functional unit retained overall germinability after prolonged cold storage and maintained its capacity for regeneration under elevated germination temperatures, provided water availability persisted for at least six weeks. Although a reduction in species richness was observed, the persistence of multiple taxa suggests that the seed bank remained ecologically viable. Cold storage thus represents a practical and scalable tool for the conservation and restoration of aquatic plant communities in semi-arid environments. Nevertheless, further research in establishing protocols for the collection, storage, and germination of sediment seed banks, while considering temperature thresholds and species-specific responses, may significantly contribute to long-term conservation planning, particularly in regions like the Brazilian semi-arid, where aquatic habitats are highly dynamic and understudied. Additionally, we recommend conducting similar studies across a larger number of temporary ponds throughout different semiarid regions to further validate our findings regarding seed banks in these environments.
Acknowledgments
We thank Embrapa Semiárido for providing the physical structure to carry out the experiment.
References
-
Akinyemi DS, Oseni SR, Oke SO. 2019. Effect of heat on soil seed bank of three contrasting physiognomies in Shasha forest reserve, Southwestern Nigeria. Acta Oecologica 94: 22-30. doi: 10.1016/j.actao.2018.03.009
» https://doi.org/10.1016/j.actao.2018.03.009 -
Albuquerque AC, Rodrigues- CAS Filho, Matias LQ. 2020. Influence of climatic variables on CSR strategies of aquatic plants in a semiarid region. Hydrobiologia 847: 61-74. doi: 10.1007/s10750-019-04072-5
» https://doi.org/10.1007/s10750-019-04072-5 -
Alvares CA, Stape JL, Sentelhas PC, Gonçalves JDM, Sparovek G. 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728. doi: 10.1127/0941-2948/2013/0507
» https://doi.org/10.1127/0941-2948/2013/0507 -
Bagella S, Gascón S, Filigheddu R, Cogoni A, Boix D. 2016. Mediterranean temporary ponds: New challenges from a neglected habitat. Hydrobiologia 782: 1-10. doi: 10.1007/s10750-016-2962-9
» https://doi.org/10.1007/s10750-016-2962-9 -
Baskin CC, Baskin JM, Chester EW. 2003. Ecological aspects of seed dormancy-break and germination in Heteranthera limosa (Pontederiaceae), a summer annual weed of rice fields. Weed Research 43: 103-107. doi: 10.1046/j.1365-3180.2003.00321.x
» https://doi.org/10.1046/j.1365-3180.2003.00321.x - Baskin CC, Baskin JM. 2014. Seeds: Ecology, biogeography, and evolution of dormancy and germination. 2nd. edn. San Diego, Academic Press.
-
Baskin CC, Baskin JM, Chester EW. 2019. Long-term persistence of summer annuals in soil seed banks of seasonally dewatered mudflats. Plant Ecology 220: 731-740. doi: 10.1007/s11258-019-00948-7
» https://doi.org/10.1007/s11258-019-00948-7 -
Bonis A, Lepart J, Grillas P. 1995. Seed bank dynamics and coexistence of annual macrophytes in a temporary and variable habitat. Oikos 74: 81-92. doi: 10.2307/3545677
» https://doi.org/10.2307/3545677 -
Bouahim S, Rhazi L, Amami B, et al. 2014. Unravelling the impact of anthropogenic pressure on plant communities in Mediterranean temporary ponds. Marine and Freshwater Research 65: 918-929. doi: 10.1071/MF13194
» https://doi.org/10.1071/MF13194 -
Brock MA. 2011. Persistence of seed banks in Australian temporary wetlands. Freshwater Biology 56: 1312-1327. doi: 10.1111/j.1365-2427.2010.02570.x
» https://doi.org/10.1111/j.1365-2427.2010.02570.x -
Bueno NC, Prado JF, Meurer T, Bicudo CEM. 2011. New records of Chara (Chlorophyta, Characeae) for subtropical southern Brazil. Systematic Botany 36: 523-541. doi: 10.1600/036364411X583510
» https://doi.org/10.1600/036364411X583510 -
Calhoun AJ, Mushet DM, Bell KP, Boix D, Fitzsimons JA, Isselin-Nondedeu F. 2017. Temporary wetlands: Challenges and solutions to conserving a ‘disappearing’ ecosystem. Biological Conservation 211: 3-11. doi: 10.1016/j.biocon.2016.11.024
» https://doi.org/10.1016/j.biocon.2016.11.024 - Canty AJ. 2002. Resampling methods in R: the boot package. The Newsletter of the R Project 2: 2-7.
-
Carta A. 2016. Seed regeneration in Mediterranean temporary ponds: Germination ecophysiology and vegetation processes. Hydrobiologia 782: 23-35. doi: 10.1007/s10750-016-2808-5
» https://doi.org/10.1007/s10750-016-2808-5 -
Carta A, Bedini G, Müller JV, Probert RJ. 2013. Comparative seed dormancy and germination of eight annual species of ephemeral wetland vegetation in a Mediterranean climate. Plant Ecology 214: 339-349. doi: 10.1007/s11258-013-0174-1
» https://doi.org/10.1007/s11258-013-0174-1 -
Dalziell EL, Funnekotter B, Mancera RL, Merritt DJ. 2019. Seed storage behaviour of tropical members of the aquatic basal angiosperm genus Nymphaea L. (Nymphaeaceae). Conservation Physiology 7: coz021. doi: 10.1093/conphys/coz021
» https://doi.org/10.1093/conphys/coz021 -
Dantas BF, Moura MS, Pelacani CR, et al. 2020. Rainfall, not soil temperature, will limit the seed germination of dry forest species with climate change. Oecologia 192: 529-541. doi: 10.1007/s00442-019-04575-x
» https://doi.org/10.1007/s00442-019-04575-x -
Douh C, Daïnou K, Loumeto JJ, et al. 2018. Soil seed bank characteristics in two central African forest types and implications for forest restoration. Forest Ecology and Management 409: 766-776. doi: 10.1016/j.foreco.2017.12.012
» https://doi.org/10.1016/j.foreco.2017.12.012 -
Duarte TH, Almeida TS, Albertoni EF, Palma-Silva C. 2020. Role of the propagule bank in reestablishing submerged macrophytes after removal of free-floating plants for recovery of a shallow lake in Southern Brazil. Ecología Austral 30: 239-250. doi: 10.25260/EA.20.30.2.0.1014
» https://doi.org/10.25260/EA.20.30.2.0.1014 -
Dyer AF. 1994. Natural soil spore banks-can they be used to retrieve lost ferns? Biodiversity & Conservation 3: 160-175. doi: 10.1007/BF02291886
» https://doi.org/10.1007/BF02291886 -
Embrapa. 2025. Registros meteorológicos. Looker Studio. https://lookerstudio.google.com/reporting/83744b6f-698e-488f-8ccb-8d1a9e2f6b8a/page/p_tszgmfdbvc 20 Jun 2025.
» https://lookerstudio.google.com/reporting/83744b6f-698e-488f-8ccb-8d1a9e2f6b8a/page/p_tszgmfdbvc - Esteves FA. 2011. Fundamentos de limnologia. 3 nd. edn. Rio de Janeiro, Interciência.
-
Faist AM, Ferrenberg S, Collinge SK. 2013. Banking on the past: seed banks as a reservoir for rare and native species in restored vernal pools. AoB Plants 5: plt043. doi: 10.1093/aobpla/plt043
» https://doi.org/10.1093/aobpla/plt043 -
Faist AM, Collinge SK. 2015. Seed bank composition varies along invasion and inundation gradients in vernal pool wetlands. Plant Ecology 216: 553-564. doi: 10.1007/s11258-015-0458-8
» https://doi.org/10.1007/s11258-015-0458-8 -
Fernández-Zamudio R, García-Murillo P, Díaz-Paniagua C. 2018. Effect of the filling season on aquatic plants in Mediterranean temporary ponds. Journal of Plant Ecology 11: 502-510. doi: 10.1093/jpe/rtx026
» https://doi.org/10.1093/jpe/rtx026 - Ferreira FA, Catian G. 2016. Diaspore bank of aquatic macrophytes maintaining species diversity in a Neotropical pond. Acta Scientiarum. Biological Sciences 38: 419-427.
-
Flora e Funga do Brasil. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ 10 April 2022.
» http://floradobrasil.jbrj.gov.br/ -
Fox J, Weisberg S. 2019. An R Companion to Applied Regression. 3. ed. Thousand Oaks, Sage. Available at: https://www.john-fox.ca/Companion/
» https://www.john-fox.ca/Companion/ -
Grillas P, Rhazi L, Lefebvre G, Madihi ME, Poulin B. 2021. Foreseen impact of climate change on temporary ponds located along a latitudinal gradient in Morocco. Inland Waters 11: 492-507. doi: 10.1080/20442041.2021.1962688
» https://doi.org/10.1080/20442041.2021.1962688 -
Graves S, Piepho HP, Dorai-Raj S. 2023. multcompView: Visualizations of Paired Comparisons. R package version 0.1-9. https://CRAN.R-project.org/package=multcompView 16 Oct 2023
» https://CRAN.R-project.org/package=multcompView -
Gross KL. 1990. A comparison of methods for estimating seed numbers in the soil. Journal of Ecology 78: 1079-1093. doi: 10.2307/2260953
» https://doi.org/10.2307/2260953 -
Gross J, Ligges U. 2015. nortest: Tests for Normality. R package version 1.0-4. https://CRAN.R-project.org/package=nortest 16 Oct 2023.
» https://CRAN.R-project.org/package=nortest - Hay F, Probert R, Marro J, Dawson M. 2000. Towards the ex situ conservation of aquatic angiosperms: A review of seed storage behaviour. In: Proceedings of the Sixth International Workshop on Seeds, 2000, Merida. p. 161-177.
- Hothorn T, Bretz F, Westfall P. 2008. Simultaneous inference in general parametric models. Biometrical Journal 50: 346-363.
-
Hourston JE, Steinbrecher T, Chandler JO, et al. 2022. Cold-induced secondary dormancy and its regulatory mechanisms in Beta vulgaris. Plant, Cell & Environment 45: 1315-1332. doi: 10.1111/pce.14264
» https://doi.org/10.1111/pce.14264 -
IPCC. 2021. Climate change 2021: The physical science basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, Cambridge University Press. https://www.ipcc.ch/report/ar6/wg1/ 20 Apr 2022
» https://www.ipcc.ch/report/ar6/wg1/ -
Kan J, Song S. 2008. Effects of dehydration, chilling, light, phytohormones and nitric oxide on germination of Pistia stratiotes seeds. Seed Science and Technology 36: 38-45. doi: 10.15258/sst.2008.36.1.04
» https://doi.org/10.15258/sst.2008.36.1.04 -
Lenth R. 2024. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.10.0. https://CRAN.R-project.org/package=emmeans 21 May 2021
» https://CRAN.R-project.org/package=emmeans - Levene H. 1960. Contributions to probability and statistics: Essays in honor of Harold Hotelling. In: Olkin I, Churyes SG, Hoeffding W, Madow WG, Mann HB. (eds.) Stanford studies in mathematics and statistics. Stanford, Stanford University Press. p. 278-292.
-
Liu M, Qiao N, Zhang B, et al. 2022. Differential responses of the seed germination of three functional groups to low temperature and darkness in a typical steppe, Northern China. PeerJ 10: e14485. doi: 10.7717/peerj.14485
» https://doi.org/10.7717/peerj.14485 -
Lucena RL, Faria RM, Lima RKA, Aprígio TRM, Silva ADG, Souza SFF. 2021. Temperatura e sensação térmica na depressão sertaneja: análise da região do Seridó no semiárido brasileiro. Revista Ibero-Americana de Ciências Ambientais 12: 85-97. doi: 10.6008/CBPC2179-6858.2021.011.0009
» https://doi.org/10.6008/CBPC2179-6858.2021.011.0009 -
Lukács BA, Sramkó G, Molnár A. 2013. Plant diversity and conservation value of continental temporary pools. Biological Conservation 158: 393-400. doi: 10.1016/j.biocon.2012.08.024
» https://doi.org/10.1016/j.biocon.2012.08.024 -
Lumbreras A, Marques JT, Belo AF, et al. 2016. Assessing the conservation status of Mediterranean temporary ponds using biodiversity: A new tool for practitioners. Hydrobiologia 782: 187-199. doi: 10.1007/s10750-016-2697-7
» https://doi.org/10.1007/s10750-016-2697-7 -
Maltchik L. 2000. As lagoas temporárias do semiárido. Ciência Hoje 28: 67-70. doi: 10.17648/heringeriana.v16i1.918009
» https://doi.org/10.17648/heringeriana.v16i1.918009 -
Marengo JA, Torres RR, Alves LM. 2017. Drought in Northeast Brazil-Past, present, and future. Theoretical and Applied Climatology 129: 1189-1200. doi: 10.1007/s00704-016-1840-8
» https://doi.org/10.1007/s00704-016-1840-8 -
Mayrinck RC, Vilela LC, Pereira TM, et al. 2019. Seed desiccation tolerance/sensitivity of tree species from Brazilian biodiversity hotspots: considerations for conservation. Trees 33: 777-785. doi: 10.1007/s00468-019-01815-8
» https://doi.org/10.1007/s00468-019-01815-8 -
Mbofung GC, Goggi AS, Leandro LF, Mullen RE. 2013. Effects of storage temperature and relative humidity on viability and vigor of treated soybean seeds. Crop Science 53: 1086-1095. doi: 10.2135/cropsci2012.09.0530
» https://doi.org/10.2135/cropsci2012.09.0530 -
Murph K, Efremov A, Davidson TA, et al. 2019. World distribution, diversity and endemism of aquatic macrophytes. Aquatic Botany 158: 103127. doi: 10.1016/j.aquabot.2019.06.006
» https://doi.org/10.1016/j.aquabot.2019.06.006 -
Oliveira GM, Matias JR, Dantas BF. 2014. Temperatura ótima para germinação de sementes nativas da Caatinga. Informativo ABRATES 24: 44-47. http://www.alice.cnptia.embrapa.br/alice/handle/doc/997939 11 Jun 2018
» http://www.alice.cnptia.embrapa.br/alice/handle/doc/997939 -
Ooi MK, Auld TD, Denham AJ. 2009. Climate change and bet-hedging: Interactions between increased soil temperatures and seed bank persistence. Global Change Biology 15: 2375-2386. doi: 10.1111/j.1365-2486.2009.01887.x
» https://doi.org/10.1111/j.1365-2486.2009.01887.x -
Ooi MK. 2012. Seed bank persistence and climate change. Seed Science Research 22: S53-S60. doi: 10.1017/S0960258511000407
» https://doi.org/10.1017/S0960258511000407 -
Ouhamdouch S, Bahir M. 2017. Climate change impact on future rainfall and temperature in semi-arid areas (Essaouira Basin, Morocco). Environmental Processes 4: 975-990. doi: 10.1007/s40710-017-0265-4
» https://doi.org/10.1007/s40710-017-0265-4 -
Parra G, Guerrero F, Armengol J, et al. 2021. The future of temporary wetlands in drylands under global change. Inland Waters 11: 445-456. doi: 10.1080/20442041.2021.1936865
» https://doi.org/10.1080/20442041.2021.1936865 -
Pennington RT, Prado DE, Pendry CA. 2000. Neotropical seasonally dry forests and Quaternary vegetation changes. Journal of Biogeography 27: 261-273. doi: 10.1046/j.1365-2699.2000.00397.x
» https://doi.org/10.1046/j.1365-2699.2000.00397.x - Pereira MCT. 2017. Plantas aquáticas em lagoas temporárias do semiárido, nordeste do Brasil. Ph.D. Thesis, Universidade Federal Rural de Pernambuco, Brazil. 2017.
-
Pinheiro KR, Alves ER, Alves MV, Galvíncio JD. 2020. Impacto da precipitação e do uso e ocupação do solo na cobertura vegetal na Caatinga. Journal of Environmental Analysis and Progress 5: 221-231. doi: 10.24221/jeap.5.2.2020.3058.221-231
» https://doi.org/10.24221/jeap.5.2.2020.3058.221-231 -
R Core Team. 2022. R: A language and environment for statistical computing. Vienna, R Foundation for Statistical Computing. https://www.R-project.org/ 16 Oct 2023.
» https://www.R-project.org/ -
Rejmánková E. 1976. Germination of seeds of Lemna gibba. Folia Geobotanica et Phytotaxonomica 11: 261-267. doi: 10.1007/BF02909473
» https://doi.org/10.1007/BF02909473 -
Scholes RJ. 2020. The future of semi-arid regions: A weak fabric unravels. Climate 8: 43. doi: 10.3390/cli8030043
» https://doi.org/10.3390/cli8030043 -
Sederias J, Colman B. 2007. The interaction of light and low temperature on breaking the dormancy of Chara vulgaris oospores. Aquatic Botany 87: 229-234. doi: 10.1016/j.aquabot.2007.06.008
» https://doi.org/10.1016/j.aquabot.2007.06.008 -
Shapiro SS, Wilk MB. 1965. An analysis of variance test for normality. Biometrika 52: 591-611. doi: 10.2307/2333709
» https://doi.org/10.2307/2333709 -
Šidák Z. 1967. Rectangular confidence region for the means of multivariate normal distributions. Journal of the American Statistical Association 62: 626-633. doi: 10.2307/2283989
» https://doi.org/10.2307/2283989 -
Silva JCD, Silva JDJ, Silva SSD, Gomes RA, Dantas BF. 2022a. Effect of long-term storage on viability of buffel grass (Cenchrus ciliaris L.) seeds. Journal of Seed Science 44. doi: 10.1590/2317-1545v44259954
» https://doi.org/10.1590/2317-1545v44259954 -
Silva JDJ, Alencar SDS, Gomes RA, Matias JR, Pelacani CR, Dantas BF. 2022b. Conservation and physiological quality of Handroanthus spongiosus (Rizzini) S. Grose (Bignoniaceae) seeds. Journal of Seed Science 44. doi: 10.1590/2317-1545v44257812
» https://doi.org/10.1590/2317-1545v44257812 - Souza VC, Lorenzi H. 2012. Botânica sistemática: Guia ilustrado para identificação das famílias de fanerógamas nativas e exóticas no Brasil baseado em APG III. 3nd edn. Nova Odessa, Instituto Plantarum de Estudos da Flora.
-
Tabosa AB, Matias LQ, Martins FR. 2012. Live fast and die young: The aquatic macrophyte dynamics in a temporary pool in the Brazilian semiarid region. Aquatic Botany 102: 71-78. doi: 10.1016/j.aquabot.2012.05.004
» https://doi.org/10.1016/j.aquabot.2012.05.004 -
Tuckett RE, Merritt DJ, Hay FR, Hopper SD, Dixon KW. 2010. Dormancy, germination and seed bank storage: A study in support of ex situ conservation of macrophytes of southwest Australian temporary pools. Freshwater Biology 55: 1118-1129. doi: 10.1111/j.1365-2427.2010.02386.x
» https://doi.org/10.1111/j.1365-2427.2010.02386.x -
Van Der Valk AG, Davis CB. 1978. The role of seed banks in the vegetation dynamics of prairie glacial marshes. Ecology 59: 322-335. doi: 10.2307/1936377
» https://doi.org/10.2307/1936377 -
Vandvik V, Klanderud K, Meineri E, Måren IE, Töpper J. 2016. Seed banks are biodiversity reservoirs: Species-area relationships above versus below ground. Oikos 125: 218-228. doi: 10.1111/oik.02022
» https://doi.org/10.1111/oik.02022 -
Vicente D, Oliveira LMD, Tonetti OAO, Silva AA, Liesch PP, Engel ML. 2016. Viability of Ocotea puberula (Rich.) Ness seeds during storage. Floresta e Ambiente 23: 418-426. doi: 10.1590/2179-8087.107414
» https://doi.org/10.1590/2179-8087.107414 -
Walck JL, Hidayati SN, Dixon KW, Thompson K, Poschlod P. 2011. Climate change and plant regeneration from seed. Global Change Biology 17: 2145-2161. doi: 10.1111/j.1365-2486.2010.02368.x
» https://doi.org/10.1111/j.1365-2486.2010.02368.x -
Wakshum S, Sebsebe D, Tamrat B. 2018. Ecology of soil seed banks: Implications for conservation and restoration of natural vegetation: A review. International Journal of Biodiversity and Conservation 10: 380-393. doi: 10.5897/IJBC2018.1226
» https://doi.org/10.5897/IJBC2018.1226 -
Wang GD, Wang M, Lu XG, Jiang M. 2015. Effects of farming on the soil seed banks and wetland restoration potential in Sanjiang Plain, Northeastern China. Ecological Engineering 77: 265-274. doi: 10.1016/j.ecoleng.2015.01.039
» https://doi.org/10.1016/j.ecoleng.2015.01.039 -
Wang N, He X, Zhao F, Wang D, Jiao J. 2020. Soil seed bank in different vegetation types in the Loess Plateau region and its role in vegetation restoration. Restoration Ecology 28: A5-A12. doi: 10.1111/rec.13169
» https://doi.org/10.1111/rec.13169 -
Wuertz D, Setz T, Chalabi Y, Boshnakov GN. 2023. fBasics: Rmetrics - Markets and Basic Statistics. R package version 4032.96. https://CRAN.R-project.org/package=fBasics 16 Oct 2023.
» https://CRAN.R-project.org/package=fBasics -
Xia J, Ning L, Wang Q, Chen J, Wan L, Hong S. 2017. Vulnerability of and risk to water resources in arid and semi-arid regions of West China under a scenario of climate change. Climatic Change 144: 549-563. doi: 10.1007/s10584-016-1709-y
» https://doi.org/10.1007/s10584-016-1709-y -
Zhao S, Zhang R, Liu Y, Yin L, Wang C, Li W. 2017. The effect of storage condition on seed germination of six Hydrocharitaceae and Potamogetonaceae species. Aquatic Botany 143: 49-53. doi: 10.1016/j.aquabot.2017.09.005
» https://doi.org/10.1016/j.aquabot.2017.09.005 -
Ziegler P, Appenroth KJ, Sree KS. 2023. Survival strategies of duckweeds, the world’s smallest angiosperms. Plants 12: 2215. doi: 10.3390/plants12112215
» https://doi.org/10.3390/plants12112215
