Seasonality and light: drivers of abundance, species richness, and diversity in the soil seed bank of a woodland savanna

doi:10.21203/rs.3.rs-3103987/v1

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Seasonality and light: drivers of abundance, species richness, and diversity in the soil seed bank of a woodland savanna

https://doi.org/10.21203/rs.3.rs-3103987/v1

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Understanding the composition of the soil seed bank, as well as the influence of seasonality and light on seed germination, is crucial for comprehending how changes in these conditions impact the recruitment of new individuals in the aboveground community, the dynamics of natural regeneration, and responses to disturbances. In this study, we investigated the effects of seasonality and light on the abundance, species richness, and diversity of the soil seed bank. The study was conducted in the woodland savanna of Glebe II, located within the Aimorés Wildlife Refuge, which is part of the Mosaic of Conservation Units of São Paulo State Savanna, in southeastern Brazil. We analyzed the soil seed bank using the seedling emergence method in both dry and rainy seasons. Soil was collected from 25 permanent plots, divided equally. One part was placed for germination in a nursery with a polyethylene screen cover, providing 14% shading (light treatment), while the other part was placed in a nursery with a polyethylene screen cover, providing 70% shading (shady treatment). Abundance, species richness, and diversity were evaluated for each season and treatment. Our results revealed greater abundance and species richness in the soil seed bank collected during the rainy season and maintained under shady treatment. In contrast, we observed greater diversity in the soil seed bank collected during the dry season and maintained under light treatment. These findings demonstrate that seasonality and light conditions have distinct effects on different attributes of the soil seed bank in the woodland savanna.

biodiversity

seasonality

Brazilian savanna

seedlings

germination

Savanna

Seasonal changes in rainfall and temperature may affect the formation and composition of the soil seed bank (Thompson and Grime 1979; Garwood 1989; Salazar et al. 2011; Baskin and Baskin 2014). The dispersion moment may influence the input of seeds into the bank, i.e., several species have strategies such as the period they disperse their seeds and the presence of dormancy to avoid germination in unfavorable periods and enhance the establishment of seedlings in the environment (Garwood 1989; Salazar et al. 2011; Jara-Guerrero et al. 2020). These factors may influence the viability, the density, the floristic composition, and the diversity of the soil seed bank (Thompson and Grime 1979; Thompson 1987).

The presence or absence of light may influence the germination of some plant species, therefore, leading to the exiting of such species from the soil seed bank (Baskin and Baskin 2014). Studies with woodland savanna species have shown that in a greater part of the study species, germination occurs independently of the presence of light (Zaidan and Carreira 2008; Lima et al. 2014). Studies conducted with soil seed banks in other forest formations, where it was maintained in light and shady conditions, did not find a significant difference between these light conditions (Batista Neto 2005; Scherer and Jarenkow 2006; Menezes et al. 2019), which could indicate that the greater part of the seeds in forest areas are neutral photoblastic, i.e., germinate independently of light availability (Baskin and Baskin 2014). For the woodland savanna, we are unaware of the existence of studies that evaluate the influence of different light conditions over soil seed banks.

Soil seed banks are an important mechanism for the resilience and persistence of some species in the above ground community (Baskin and Baskin 2014; Yang et al. 2021). In the event of vegetation disturb or degradation, the seed bank represents an important tool for the regeneration in this area, providing seeds that may colonize the locale (Albuquerque et al. 2010; Suding 2011; Mmusi et al. 2021; Bekele 2022). Knowing the soil seed bank composition, the influence of seasonality in its formation, and how light affects the germination of species present in it allow us to comprehend how the changes in these variables impact the recruiting of new species (Mašková and Poschlod 2021), which processes are involved in the dynamics of natural regeneration in the area (Girmay et al. 2022), and how it may respond to possible disturb. We believe that the soil seed bank collected in the rainy season has a higher richness, abundance, and diversity, once some species that disperse in the dry season, due to unfavorable conditions, do not germinate and maintain themselves in the soil seed bank. We expect that the soil seed bank collected in the fields and maintained in the nursery is predominantly composed of neutral photoblastic species seeds, not significantly differing in both light conditions.

Our aims were (a) to verify whether there are differences in the abundance, species richness, and diversity in the soil seed bank collected in dry and rainy seasons and (b) to verify if different light conditions affect the soil seed bank germination.

Characterization of the study area

We conducted the study at Glebe II of the Aimorés Wildlife Refuge, part of the Mosaic of Conservation Units of Cerrado Paulista, within an area of 308.068 ha, situated in the municipality of Bauru, in the center-west of São Paulo State, southeastern Brazil, at 22º19’41” to 22º21’06”S and 48º59’49” to 49º01’12”W, and altitude range of 519 to 603 metros (Sfair et al. 2010). The climate is Cwa (Koeppen 1948), characterized by a hot and rainy summer and cold and dry winter. The average temperature values varied throughout the experiment, with the lowest averages recorded in the dry season and the highest in the rainy season. In the municipality of Bauru, São Paulo State, Brazil, the rainy season covers the months from October to March and the dry season covers the months from April to September (Figueiredo and Paz 2010).

In the South-west part of Glebe II of the Aimorés Wildlife Refuge, with a forest physiognomy classified as woodland savanna, popularly known as cerradão, there are placed 100 permanent plots measuring 10 m x 10 m, totalling one discontinuous hectare (Weiser 2007). We collected soil from 25 of these plots.

Material collection, experiment assembling and monitoring

We collected the soil seed bank in April (dry season) and October (rainy season) of 2019. By using a wooden frame measuring 20 cm x 10 cm, inside each plot, we collected soil at a depth of 5 cm, excluding the litter layer, at five distinctive points: in each corner of the plot and in its center, to maximize the number of seeds of different species collected in the area (Thompson 1986; Butler and Chazdon 1998). Thus, each sample was composed of five subsamples. In the second sampling, we also collected the soil in the center and in each corner of the corresponding plot, with the collection point being as near as possible to the previous collection point.

We disposed the obtained soil in each spot of the same plot in a single-identified plastic bag, totalizing 25 samples. We homogenized the material and divided each sample into two equal parts, being one placed on a tray which was exposed to natural light in an area covered by a white polyethylene screen, with shading of 14% (light treatment), to protect the emerged seedlings from the attack of herbivores, as well as to avoid the contamination of the trays by the seed arrival. We placed the other portion on a tray that remained under a shading screen of 70% (shady treatment), to simulate the forest environment of the woodland savanna and stimulate the germination of shade-tolerant species. We maintained the experiments under natural temperature and light conditions.

We deposited the soil in aluminum trays, watering them daily. With the trays containing the soil seed bank, we placed 10 aluminum trays containing sand to verify whether there was a contamination on the trays. Both, in the trays containing the soil collected in the woodland savanna and in the control trays containing only sand, the soil layer was about 2.5 cm thick.

We evaluated the soil seed bank indirectly using the seedling emergence method, where we counted the seedlings from the germination of the seeds present in the deposited material on the trays (Simpson et al. 1989). We evaluated the abundance and species richness from the soil seed bank from different seasons (dry and rainy) for six months each. As we identified the seedlings that emerged, we removed them from the trays. Every two months, we transplanted the not yet identified seedlings into vases and turned the soil present on the trays in order that the seeds that were at the bottom could be brought up to the surface and thus have higher conditions to germinate.

We identified the species through taxonomic keys, literature, and field manual consulting, as well as by the comparison with exsiccates deposited in the acquis of the Herbarium of the Department of Biologic Sciences, School of Sciences, Bauru Campus, São Paulo State University (Herbarium UNBA). When it was impossible to identify the species at some taxonomic level, we grouped the individuals into morphospecies according to their morphological similarities until they grew up enough to allow their identification.

We elaborated a floristic list containing taxonomic data. We verified the valid name of the identified species by consulting the site World Flora Online (WFO 2023), and we organized a floristic list according to the classification system by the Angiosperm Phylogeny Group (APG IV 2016) and updates on the Angiosperm Phylogeny Website (Stevens 2001 onwards).

Data analysis

We calculated the density of seedlings m^− 2 indirectly, considering just the seeds that germinated and emerged in the experiment.

We used the vegan package (Oksanen et al. 2017) on the software Rstudio, version 1.3.1093 (RStudio Team 2020), to calculate the diversity of species present in the soil seed bank in each season through the Shannon-Wiener diversity index. We also calculated the Simpson concentration index and estimated floristic similarity in all treatments using the Sorensen index. We considered that values greater than 0.5 (50%) being of high similarity (Kent and Coker, 1994).

We submitted the abundance and species richness data in the different treatments and periods of soil collection at the Shapiro-Wilk normality test and homoscedasticity test in the SAS software, version 9.4 (SAS Institute Inc., Cary, NC). For the abundance data that did not comply with the pre-requisites for parametric tests, we performed the data transformation recommended by the box-cox test (Log 0). We conducted the ANOVA test with Tukey post hoc. We conducted all calculations at a confidence level of 95% on the statistical program SAS version 9.4 (SAS Institute Inc., Cary, NC).

To verify the effect of seasonality over abundance and species richness, we compared those that germinated during the dry season and those that germinated during the rainy season under the light and shady treatments. To investigate the light effect on abundance and species richness, we compared the specimens that germinated under the light and shady treatments during each season. We also jointly analyzed the effect of seasonality and light on abundance and species richness.

Density and abundance of seedlings

There was no emergence of seedlings in either of the control trays. The density of seedlings found in the dry season was 222 seedlings m⁻² and in the rainy season 585.2 seedlings m⁻². We recorded, in total, 555 individuals in the dry season and 1,463 individuals in the rainy season (Table 1). ANOVA test denoted that seasonality has a significant effect (p < 0.0001) over the abundance of emerged seedlings in the soil seed bank, with the highest number of individuals found in the rainy season (Fig. 1a).

Table 1

*The abundance of emerged seedlings in the soil seed bank collected in the dry and rainy seasons and maintained in light and shady treatments.*
Season/treatment	Light	Shady	Total
Dry season	180	375	555
Rainy season	299	1164	1463
Total	479	1539	-

In relation to light, we found a density of 191.6 seedlings m⁻² in the light treatment and 615.6 seedlings m⁻² in the shady treatment. Of the total seedling individuals, 479 germinated in the light and 1,539 individuals germinated in the shady treatment. Light presented a significant effect (ANOVA; p < 0.0001) on the seedling abundance, with a higher number of emerged individuals in the soil seed bank maintained in the shady treatment (Fig. 1b).

Seasonality and light presented a significant effect (ANOVA; p < 0.0001) over the soil seed bank (Fig. 2), with greater seedling abundance occurring in the soil seed bank collected in the rainy season and maintained in the shady treatment (Table 1). The species Erigeron bonariensis, Luehea grandiflora, Miconia albicans, Oxalis corniculate, and Phyllanthus orbiculatus presented the highest number of individuals in the soil seed bank collected in the rainy season and maintained in the shady treatment, representing jointly 73% of the total number of emerged individuals.

Floristic composition

We identified 1,885 (93.4%) individuals at some taxonomic level (Supplementary Information 1), of which 1,782 (88.3%) we identified at the species level, 50 (2.5%) at the gender level, 53 (2.6%) at the family level. The 133 remaining individuals (6.6%) were still found at the initial development stages, not allowing any identification.

The floristic composition varied in the soil seed bank in the dry and rainy seasons: 20 species just occurred in the dry season, 17 in the rainy season, and 41 occurred in both seasons. A significant seasonality effect (ANOVA; p = 0.0003) over the species richness, with a higher number of species being found in the rainy season seed bank (Fig. 3a).

In relation to light, among the registered species, 12 species only occurred in light treatment, 26 in shady treatment, and 40 occurred in both treatments. Species richness in the soil seed bank suffered a significant light effect (ANOVA; p < 0.0001), with a higher number of species occurring in the shady treatment (Fig. 3b).

Jointly analyzed, seasonality and light presented a significant effect (ANOVA; p < 0.0001) over the species richness of the soil seed bank. Species richness in the shady treatment of the rainy season was significantly higher than the other treatments. However, the light treatment of dry and rainy seasons presented the lowest values of species richness, do not differ significantly among themselves (Fig. 4).

They stand out as the richest families in this study were Asteraceae (18 species), Fabaceae, and Poaceae (eight species each).

Diversity and similarity

We found greater diversity in the soil seed bank collected in the dry season (H’= 3.256) than in that one collected in the rainy season (H’ = 2.657). The Simpson concentration index was 0.943 for the dry season and 0.887 for the rainy season. The similarity between the soil seed bank obtained in the dry season and that one obtained in the rainy season was 69%. The soil seed bank in the shady treatment was more diverse (H’= 2.934) than that one in the light treatment (H’ = 2.833). The obtained values for the Simpson concentration index were 0.859 in light and 0.915 in shady treatment. The similarity between the soil seed bank in light and in shady treatment was 68% (Table 2). We found greater diversity in the soil seed bank obtained in the dry season and maintained in light treatment (Table 3).

Table 2

*Sorensen similarity index obtained in the soil seed bank collected in the dry and rainy seasons and maintained in light and shady treatments.*
	DL	DS	RL	RS
DL	100%	-	-	-
DS	55%	100%	-	-
RL	51%	50%	100%	-
RS	58%	68%	65%	100%
Legends: Treatment - DL = soil seed bank obtained in the dry season and maintained in light treatment; DS = soil seed bank obtained in the dry season and maintained in shady treatment; RL = soil seed bank obtained in the rainy season and maintained in light treatment; RS = soil seed bank obtained in the rainy season and maintained in shady treatment.

Table 3

*Shannon e Wienner diversity index (H’) and Simpson concentration index (1-D) obtained in the soil seed bank collected in the dry and rainy seasons and maintained in light and shady treatments*.
Treatment	Richness	H’	1-D
DL	34	3.239	0.950
DS	45	3.072	0.931
RL	26	2.029	0.693
RS	42	2.595	0.881
Legends: Treatment - DL = soil seed bank obtained in the dry season and maintained in light treatment; DS = soil seed bank obtained in the dry season and maintained in shady treatment; RL = soil seed bank obtained in the rainy season and maintained in light treatment; RS = soil seed bank obtained in the rainy season and maintained in shady treatment.

Density and abundance of plantlets

The non-emergence of seedlings in any control tray allowed us to conclude that there was no contamination on the trays. Seasonality influences the soil seed bank. The soil seed bank obtained in the rainy season presenting higher density and greater abundance of seedlings than the soil seed bank obtained in the dry season. In tropical forests, some species have seasonal dormancy to avoid adverse periods, such as those of lesser water availability in the environment (Garwood 1989). In different savanna physiognomies, the greatest seed dispersion occurs at the end of the dry season and beginning of the rainy season, and in dense savannas diaspores are dispersed in greater abundance in the dry season (Salazar et al. 2012). For many savanna species, the seed germination is associated with the rainy season; once during this period, water is not a limiting factor for establishing of new seedlings, existing different strategies, such as the presence of dormancy in the seeds, dispersion agents, and period of dispersion, which may provide the germination in this season (Oliveira 2008; Salazar et al. 2011; Escobar et al. 2018).

Higher temperatures that occurred in the months from October and January in which the experiment was conducted, may have influenced the greater abundance in the rainy season. Plant species have different temperature requirements for germination; some may germinate in a wide temperature range; however, others germinate only at low or high temperatures (Baskin and Baskin 2014). Thus, changes in temperature throughout the different seasons may inhibit or stimulate the germination of several species, controlling the exiting or permanence of many seeds in the soil seed bank. Several savanna species have their optimum temperatures for germination between 20 ºC and 30 ºC (Zaidan and Carreira 2008; Brancalion et al. 2010; Escobar et al. 2018).

Light influences the soil seed bank. The shading (70%) provided greater seedling emergence from the soil seed bank, contrary to our initial hypothesis and the standard in forest environments with shading of 50% (Scherer and Jarenkow 2006; Menezes et al. 2019) and 60% (Batista Neto 2005). The canopy of the study area reduces the light entrance into the community, favoring the shade-tolerant species. We highlight that the shady treatment condition is more similar to the forest environment where the material was collected.

When we analyzed seasonality and light jointly, we observed in the soil seed bank obtained during the rainy season and maintained in the shady treatment, significantly greater abundance than of the other treatments.

Floristic composition

Seasonality influences the floristic composition, differing in the dry and rainy seasons. The presence of some species only in a season suggests that such species form transient soil seed banks and, those found in both seasons, form persistent banks (Thompson et al. 1997).

Light affects the floristic composition of emerged seedlings in the soil seed bank. Shady treatment provided greater richness in species in the soil seed bank, suggesting that most of these species are shade tolerant. The species Baccharis dracunculifolia, Cecropia pachystachya, Plathymenia reticulata, Solanum mauritianum, Solanum paniculatum, Trema micrantha, and Xylopia aromatica, classified as shade intolerant (Durigan et al. 2004), emerged in the soil seed bank maintained in shady treatment. The germination process depends on other environmental conditions, such as water availability, temperature, and oxygen concentration, factors that may have caused the germination of such species in the shady treatment (Kerbauy, 2008; Brancalion et al. 2015). The presence of dormancy in the seeds of P. reticulata, Siparuna guianensis, and X. aromatica (Escobar et al. 2018), may have contributed to the lower abundance of these species.

We found a higher number of species than recorded in the soil seed bank of savanna physiognomies (cerrado denso and cerrado sensu stricto) (Salazar et al. 2011), and grassland physiognomies (campo cerrado and campo sujo) (Salazar et al. 2011; Machado et al. 2013), probably due to the exposure of the soil seed bank to different light conditions, which allowed the germination of shade-tolerant and light demanding species.

In other environments, the soil seed bank also presented the Asteraceae and Poaceae families among those with the highest species richness (Gasparino et al. 2006; Figueiredo et al. 2014; Moressi et al. 2014). Many species of these families have small seeds, which facilitate their incorporation into the soil seed bank. Comparing the soil seed bank with the above ground community, the families with the highest species richness were Vochysiaceae, Bignoniaceae (Francisco 2020); Rubiaceae, Myrtaceae, Lauraceae (Francisco 2020; Santos 2020), and Fabaceae (Weiser 2007; Francisco 2020; Santos 2020). From these, we found only Fabaceae and Rubiaceae; however, the species presented in the soil seed bank not always are the same in the above ground vegetation (Thompson and Grime 1979; Townsend et al. 2010).

Diversity and similarity

Seasonality and light affected the diversity of the soil seed bank. The dominance of certain species influences the results of diversity and similarity in the different treatments. The soil seed bank obtained during the dry season presented greater diversity than that obtained during the rainy season. This is due to the greater species richness and high evenness, demonstrated by the Simpson concentration index, recorded during the dry season. In the rainy season, some species presented abundance superior to the other species, leading to a lesser evenness and impacting the diversity value found in this season. The diversity found in the dry season was the closest to that found in different above ground community components in the sampled (H’ = 2.84 (Santos 2020); H’ = 3.253 (Francisco 2020).

In relation to light, we found greater diversity in the shady treatment because all attributes that compose diversity (abundance, species richness and evenness) were greater in the shady treatment than in the light treatment.

As we jointly analyzed the soil seed bank collected in different seasons and the light and shady treatments, we found greater diversity in the soil seed bank collected in the dry season and maintained in light. Despite the lower abundance value, the Simpson concentration index obtained for the soil seed bank collected in the dry season and maintained in the light was the highest, with evenness being the factor that most contributed to diversity. The soil seed bank obtained in the dry season and maintained in the shady also presented high diversity, with evenness and richness being the attributes that most contributed to diversity. The soil seed bank collected in the rainy season and maintained in the light and shady treatments presented the lowest diversity values.

The similarity among the different treatments and collection seasons was high. The greater similarity (68%) occurred between the soil seed banks of dry and rainy seasons maintained in the shady treatment. The soil seed bank collected in the different seasons share several species; however, there are also species that will only be present in the soil seed bank in a single season. Such data indicate that the soil seed bank is influenced by seasonality, with different species being recruited to the area according to environmental conditions, such as temperature, amount of light that reaches the soil seed bank, and water availability in the environment.

We conclude that seasonality and light influence the abundance, species richness, and diversity of the soil seed bank. In rainy seasons, as well as in environments of shady condition, the soil seed bank presents greater abundance and species richness. Diversity is higher in the dry season and in environments with light condition.

Funding

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.

Competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Author Contributions

Solange dos Santos Silva: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Writing – review & editing, Funding acquisition. Veridiana de Lara Weiser: Conceptualization, Methodology, Validation, Resources, Writing – review & editing, and Supervision.

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Seasonality and light: drivers of abundance, species richness, and diversity in the soil seed bank of a woodland savanna

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Abstract

Figures

Introduction

Material and methods

Characterization of the study area

Material collection, experiment assembling and monitoring

Data analysis

Results

Density and abundance of seedlings

Floristic composition

Diversity and similarity

Discussion

Density and abundance of plantlets

Floristic composition

Diversity and similarity

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1