Biotic and abiotic determinants modulate interactions between standing vegetation and soil seed bank across fine spatial scales

doi:10.21203/rs.3.rs-2608797/v1

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Biotic and abiotic determinants modulate interactions between standing vegetation and soil seed bank across fine spatial scales

https://doi.org/10.21203/rs.3.rs-2608797/v1

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Background and Aims

Standing vegetation and soil seed banks are tightly related compartments in annual plant communities. However, little is known about how this relationship changes spatially and temporally and their dependence on abiotic and biotic factors. We investigated the similarity between both compartments under contrasting water availability conditions, perennials and biocrusts.

Methods

We established a field experiment in a Mediterranean annual plant community growing on gypsum soils. We evaluated the relationships between aboveground vegetation and soil seed bankover three years and along three spatial scales and tested the effects of water availability (irrigation), perennial vegetation and biocrust on both compartments.

Results

The soil seed bank was more similar to the standing vegetation closer to the third year, when seed bank was collected. The similarity between both compartments was higher at the large spatial scale (20 ´ 20 cm) but the modulatory effects of irrigation, perennial tussocks and biocrust were more evident at medium (10 ´ 10 cm) and fine scale (5 ´ 5 cm). The similarity increased with irrigation and was higher under perennial vegetation. The biocrust acted mainly as a barrier to the incorporation of seeds into the permanent seed bank.

Conclusion

Our findings suggest that abiotic and biotic factors had hierarchical effects on the similarity between the standing vegetation and soil seed bank compartments. Interannual shifts such as rainfall amount and frequency, were the main determinants but tussocks, biocrust, and irrigation modulated similarity, thereby showing that annual plant communities are driven by complex processes.

Annual plant community

biological soil crust

gypsum soils

Mediterranean drylands

similarity

soil seed bank

spatial scales.

Standing vegetation and soil seed banks constitute two complementary compartments of plant diversity in natural communities (Bakker et al. 1996; Fenner and Thompson 2005), and they are tightly related in terms of species abundance and composition (Olano et al. 2005; Hopfensperger 2007). The dynamic relationship between both compartments over time is described by the so-called spiral dynamics model (Caballero et al. 2008). According to the spiral model, the composition of the standing vegetation will determine the identity of the seeds that enter the seed bank each year, which then determine the composition of the aboveground vegetation in the next season, and the continuation of this internal feedback indefinitely can be viewed as a form of spiral. In this model, the transient seed bank that is refilled every year by the current seed rain can vary depending on the standing vegetation, whereas the permanent bank that remains after every germination event is far more stable and resilient (Caballero et al. 2008).

Several factors affect the transition from seed to seedling through germination, including the depth of the seed in the soil profile (Traba et al. 2004), microhabitat conditions (Tielbörger et al. 2012; Willis et al. 2014), and endogenous physiological condition of the seed (Baskin and Baskin 2004). After germination, the fate of the emerging seedling is regulated by a complex hierarchical set of assembly filters (sensu Götzenberger et al. 2012), including biotic processes (e.g., competition and facilitation), which each individual must overcome to successfully establish. Each factor operates at different spatial scales, what could lead to changes in the similarity between the standing vegetation and soil seed bank across space. However, few studies have evaluated the relationship between vegetation and the seed bank on a spatially explicit basis (Chick et al. 2018), and they rarely considered the fine spatial scales at which most processes involving seeds occur (but see Peralta et al. 2016), including seed dispersal and seed post-dispersal predation (Azcárate and Peco 2006; Azcárate et al. 2010), and the incorporation of seeds into deep soil layers (Luzuriaga et al. 2005). Most of these processes are affected by seed traits, such as size or dispersal structures (Venable et al. 2008; Peco et al. 2009; Azcárate et al. 2010; Thomson et al. 2011), as well as biotic factors that determine the habitat structure (Peralta et al. 2016, 2019) and abiotic components, including the wind, soil structure, and soil hardness (Thompson et al. 2014).

Annual plant communities that inhabit drylands are excellent model systems for evaluating the relationships between standing vegetation and soil seed bank compartments at different scales. The changes in the standing vegetation and soil seed bank in these ephemeral communities are mainly conditioned by the soil water content (Chesson et al. 2004; Miranda et al. 2011). Rainfall patterns determine water availability, which is modulated at fine spatial scales by perennials but also by biological soil crusts (referred to as biocrusts in the following) that mainly comprise lichens and cyanobacteria, these biocrusts are important ecosystem components in drylands (Martínez et al. 2006; Berdugo et al. 2014; Chamizo et al. 2016; Chen et al. 2020). The effects of perennials on water availability at fine spatial scales (Pariente 2002; López-Pintor et al. 2003; Maestre and Cortina 2004) and their consequences for the distribution and performance of annuals have been well documented (Holzapfel et al. 2006; Pugnaire et al. 2011). The interactions between annuals and perennials are highly dependent on water stress, i.e., facilitative interactions may shift to become competitive interactions under extremely low water availability conditions (Bertness and Callaway 1994; Maestre et al. 2009; Luzuriaga et al. 2012). Perennials can also determine the soil seed bank structure and composition of annual communities because they act directly to trap seeds from seed rain or from secondary dispersal (Bullock and Moy 2004). In addition, biocrusts regulate soil water retention (Belnap 2006; Berdugo et al. 2014; Faist et al. 2017), favor annual plant growth in intermediate water stress conditions (Peralta et al. 2019; Sánchez et al. 2022) and act as seed traps contributing to the incorporation of seeds into the soil seed bank (Zhang et al. 2016). However, biocrusts may also act as physical barriers to greatly reduce seed germination, and seedling emergence and establishment (Belnap et al. 2001; Li et al. 2005; Peralta et al. 2016). Despite the importance of both perennials and biocrusts as determinants of annual plant communities, their interactive effects on the similarity between vegetation and soil seed bank compartments have not been comprehensively evaluated to the best of our knowledge.

Thus, in the present study, we evaluated the extent to which the similarity between standing vegetation and soil seed bank compartments varied at fine spatial scales under contrasting water availability conditions and biotic interactions. We conducted a three-year field experiment based on the annual plant communities that grow in gypsum habitats in Central Spain. We manipulated the water availability (through an irrigation treatment) and monitored the effects of a conspicuous and dominant perennial tussock (Macrochloa tenacissima) and biocrust cover on the similarity between the standing vegetation and soil seed bank at fine spatial scales. Gypsum annuals generally have a low dispersal capacity because of their small plant height (average height of 10.5 cm) and most lack specialized dispersal structures (Fllner and Shmida 1981; Venable et al. 2008). Therefore, seeds usually accumulate close to the mother plants instead of dispersing over long distances (Olano et al. 2005; Peralta et al. 2023). Consequently, we sampled an array of spatial scales using quadrats with areas of 5 ´ 5 cm, 10 ´ 10 cm, and 20 ´ 20 cm. The specific aims of this study were: (I) to evaluate the effect of water availability (irrigation treatment), and the presence or absence of Macrochloa tenacissima or biocrust cover on the similarity between the annual standing vegetation and soil seed bank at three different fine spatial scales; (II) to assess whether the similarity between the vegetation and both the complete soil seed bank (SSBc) and persistent soil seed bank (SSBp) responded in a consistent manner to the same factors; and (III) to determine whether the similarity between the standing vegetation and soil seed bank compartments is scale dependent.

We expected that the similarity between the standing vegetation and both soil seed banks, especially with the SSBc, would increase with the water availability because more benign conditions should enhance seed production by standing vegetation and seed germination from the seed bank, thereby increasing the similarity between both community compartments. Amelioration of the water conditions due to reduced evapotranspiration caused by tussocks or biocrust could increase the similarity between both compartments. However, competition with perennials in drier years and the physical barrier exerted by the biocrust might prevent species emergence from the soil and the incorporation of new seeds into the seed bank beneath to reduce the similarity. We also hypothesized that the similarity between the standing vegetation and seed bank might differ between SSBc and SSBp because the complete seed bank includes the transient seed bank, which depends on the seeds produced each year by the aboveground plant community. By contrast, in the case of persistent seed banks, changes in the similarity between the two compartments could be related to species-specific dormancy dynamics. Finally, we expected that the similarity would be greatest at the 20 ´ 20 cm sampling scale because the probability of more completely representing the local floristic pool increases with the sampling area size. It should be noted that this size is also the average plant height in the community, and thus it is the most frequent dispersal distance for seeds.

Study site

This study was conducted at Sotomayor Experimental Station in Aranjuez, Madrid, Central Spain (590 m a.s.l.; 40°02¢N, 3°37¢W), which has a semi-arid Mediterranean climate with mean annual rainfall of 365 mm and a mean annual temperature of 15°C (AEMET, data for the period of 1981–2010 at Getafe station (40°17¢58¢¢N, 3°43¢20¢¢W; 620 m a.s.l.)). The rainfall is highly variable and unpredictable in the study area, where it is distributed in two rainy periods during the autumn and spring. The rainfall variability during the three years of our study (2008–2010) was highly representative of this variability, with extremely dry weather in both the autumn (79 mm/m²) and spring (38.5 mm/m²) in 2008, a wet autumn (160 mm/m²) and dry spring (77.5 mm/m²) in 2009, and a dry autumn followed by a rainy spring in 2010 (40.3 and 343.6 mm/m², respectively).

The vegetation in the area comprises scattered tussocks of Macrochloa tenacissima (L.) Kunth and gypsum specialized shrubs (e.g., Helianthemum squamatum (L.) Dum. Cours., Lepidium subulatum L., Centaurea hyssopifolia Vahl, and Gypsophila struthium L. in Loefl.). Bare areas among tussocks are covered by well-conserved, heterogeneous, and species rich biocrusts composed mainly of lichens (e.g., Diploschistes diacapsis (Ach.) Lumbsch, Squamarina lentigera (G.H. Weber) Poelt, Fulgensia subbracteata (Nyl.) Poelt, and Psora decipiens (Hedw.) Hoffm) (Martínez et al. 2006). Bare areas are seasonally covered with a very rich annual plant community (ca. 38 plant species/0.25 m2, Luzuriaga et al. 2012) comprising tiny plants (mean maximum height of 10.5 cm), and some have a strict affinity for gypsum soils such as Chaenorhinum reyesii (C. Vicioso & Pau) Benedí and Campanula fastigiata Dufour ex Schult. (Luzuriaga et al. 2015). Germination mainly occurs in the autumn, but a fraction of dormant seeds is incorporated into the soil seed bank for most species (Sánchez et al. 2014; Peralta et al. 2016).

Experimental design and data collection

In total, 24 plots with areas of 50 ´ 50 cm were randomly selected in two different microenvironments, with 12 plots beneath mature M. tenacissima tussocks (Tussocks) and 12 in open areas at least 1 m distant from the nearest M. tenacissima plant (Open areas). This sampling plot size was sufficiently large to represent the community completely (see Luzuriaga et al. 2012; Peralta et al. 2016). Half of the plots in each microenvironment received natural rainfall (Control) and half were watered each week from February to March (Irrigation), which is the most critical period for plant development and reproduction in these annual plant communities. In total, 28 L/m² was applied to each plot (Irrigation treatment), which corresponded to an increase in the average rainfall of 50% in this system compared with the average rainfall during the same period in the preceding 30 years (AEMET, https://www.aemet.es/es/datos_abiertos/AEMET_OpenData). The rainfall was extremely high in 2010 and the soil was at the field capacity, so the irrigation treatment was not conducted in this year. Thus, we employed a fully crossed bifactorial design with four experimental scenarios (i.e., Control-Tussock, Control-Open, Irrigation-Tussock, and Irrigation-Open). For further details of the experimental design, please refer to the studies by Luzuriaga et al. (2012) and Peralta et al. (2016).

During March–April in 2008, 2009, and 2010 when the maximum plant community development occurred, we overlaid a rectangular mesh divided into 100 cells measuring 5 ´ 5 cm on each plot and the ground cover was visually estimated for each annual species in each cell (n = 2400 ´ 3 years). The biocrust cover was also recorded in each cell in 2008. During April and September in 2010, after vegetation sampling, we collected 32 soil cores per plot, where each corresponded to a cell measuring 5 ´ 5 cm, by using a checkerboard design and avoiding the plot edges (Fig. 1). The soil cores had a diameter of 3 cm and depth of 3 cm, and most of the germinable seeds were present in these cores (Childs and Goodall 1973; Russi et al. 1992). In particular, 384 soil samples were collected at each sampling time point (32 cells ´ 4 experimental scenarios ´ 3 replicate plots). Soil seed bank samples collected in April contained seeds that remained in the soil after germination but before seed dispersal from the standing vegetation (Persistent soil seed bank: SSBp). Soil samples collected in September contained seeds present in the soil following recent seed dispersal from the vegetation (transient seed bank), which usually occurs in June–July, as well as viable seeds that did not germinate and persisted in the soil seed bank (i.e., transient + persistent seed bank = Complete soil seed bank, SSBc) (Walck et al. 2005).

The seedling emerging method (Roberts 1981) was used to identify the species in each soil sample. Each soil sample was mixed with organic soil and placed in individually labeled pots, which were then placed in a greenhouse with a permanent water supply (see Peralta et al. 2016 for more details). Germination was checked each week. After cultivation for five months, we applied gibberellins (1000 ppm) to stimulate germination by the remaining seeds and continued checking germination for two more months (Caballero et al. 2003). Identified seedlings were recorded and removed immediately, whereas those that were difficult to identify were transplanted to other pots for identification to the species level.

Data analyses

The abundances of annual species in the soil seed banks were converted into presence or absence data per cell. Only cells with at least one species in the seed bank and in the standing vegetation were used (n = 2145 cells) (for SSBc: 377, 380, and 379 in 2008, 2009, and 2010, respectively; for SSBp: 317, 342, and 350 in 2008, 2009, and 2010).

Bray–Curtis distances (Bray and Curtis 1957) were used to measure similarities in the species compositions between annual standing vegetation and both seed banks (SSBp and SSBc) at the cell level (5 ´ 5 cm). Vegetation in each sampling year (2008, 2009, and 2010) was compared with both SSBp and SSBc during 2010 in each cell. Bray–Curtis distances were transformed into similarity indexes (calculated as 1 – Bray–Curtis index) to facilitate interpretation of the similarity between the standing vegetation and soil seed bank compartments.

To evaluate whether the similarity between standing vegetation and soil seed bank compartments was scale dependent, 5 × 5 cm cells were grouped into 10 ´ 10 cm and 20 ´ 20 cm cells, and the vegetation and soil seed bank compositions were recalculated by summing the corresponding 5 ´ 5 cm cells. Thus, each plot contained 32 cells of 5 ´ 5 cm, 16 cells of 10 ´ 10 cm, and four cells of 20 ´ 20 cm (i.e., 384, 192, and 48 cells, respectively) (Fig. 1b). Similarity indices were calculated between the vegetation and seed bank species compositions for these new cells using the aforementioned procedure. Similarity indices observed at each scale were analyzed using linear mixed models, with the presence of M. tenacissima (Tussock vs. Open) and irrigation treatment (Irrigation vs. Control) included as fixed factors, biocrust total cover as a covariable, and vegetation sampling year as a random factor. The interaction between presence of M. tenacissima and irrigation treatment was included in the models. All analyses were performed using the following packages in R 4.0.5 (R Core Team 2021): vegan (Oksanen et al. 2016) to calculate the Bray–Curtis distances, nlme (Pinheiro et al. 2021) to generate the linear mixed models, MuMIn (Bartoń 2019) to calculate the variability explained by random and fixed components of the models, and ggplot2 (Wickham 2016) to generate and edit all of the figures, except for Fig. 1.

We recorded 69 plant species comprising 57 annuals and 12 perennials in the soil seed bank and standing vegetation. Among the annuals, 15 species were found only in the standing vegetation and nine species were exclusives to the soil seed bank.

The species composition of the seed bank (collected in 2010) was more similar to the standing vegetation compositions observed in 2010 and in 2009 than that in 2008, and at the large spatial scale (20 ´ 20 cm) than fine scales in both SSBp and SSBc (Fig. 2). SSBc always shared higher similarity with the standing vegetation than SSBp, except in 2008 when the opposite occurred.

At the 5 × 5 cm scale, M. tenacissima tussocks significantly affected the similarity between standing vegetation and SSBc (Table 1; Fig. 3A). In addition, the effects of irrigation treatment and biocrust cover depended on the presence of perennial tussocks. The similarity was higher with no irrigation (Control) beneath tussocks (Fig. 3A). In SSBc, we detected lower similarity values in open areas with biocrust cover, but the similarity was lower under high biocrust cover beneath tussocks (Table 1 and Fig. 4). By contrast, we found the opposite in SSBp, where the lowest similarity values were detected with high crust cover in open areas, whereas the similarity was greater with high biocrust cover beneath tussocks. The sampling year explained the largest amount of variability (36% in SSBc and 18% in SSBp), and tussock, irrigation, and biocrust cover together explained altogether 5% and 2% of the variability in the similarity between vegetation with SSBc and SSBp, respectively.

At the scale of 10 ´ 10 cm, the similarity between the standing vegetation and SSBc was higher beneath non-irrigated tussocks (Control-Tussock) (Table 1 and Fig. 3B), whereas the similarity was higher in open areas under irrigation treatment. The similarity with SSBp at this scale was also higher under M. tenacissima with no irrigation (Fig. 3B). The effects of biocrust cover were the same as at the scale of 5 ´ 5 cm (Table 1 and Fig. 4). At the scale of 20 ´ 20 cm, year was the main factor that affected the similarity between the standing vegetation and both seed banks, and none of the fixed factors affected SSBc, and only tussock had a significant effect on the similarity between standing vegetation and SSBp (Table 1). In particular, the similarity increased beneath tussocks (Fig. 3C).

Overall, in both soil seed bank types (SSBc and SSBp), the highest similarity between the standing vegetation and soil seed bank compartments always occurred under the Control-Tussock scenario (Fig. 3). In addition, the similarity with both soil seed banks at all scales tended to be higher under the Tussock scenario than the Open scenario.

The effect of biocrust was strongly influenced by the presence of M. tenacissima, and the response differed with each seed bank type (Fig. 4). The similarity betweenstanding vegetation and SSBc was higher in open areas when the biocrust cover increased at both the 5 ´ 5 cm and 10 ´ 10 cm scales. In the presence of M. tenacissima tussocks, higher biocrust cover reduced the similarity between the standing vegetation and SSBc. By contrast, SSBp had the opposite relationship in both scenarios (Tussock-Open). High biocrust cover increased the similarity in the presence of M. tenacissima tussocks, whereas it reduced the similarity in open areas. No significant effect of biocrust cover was detected on similarity at the 20 ´ 20 cm scale (Table 1) for either seed bank type.

The compositions of annual plant communities are determined by two diversity compartments comprising the conspicuous standing vegetation and the hidden soil seed bank. As expected, the standing vegetation and seed bank were tightly connected in the present study, with remarkable similarity between them, which is typical in Mediterranean grasslands (Osem et al. 2006; Hopfensperger 2007). The similarity was higher as the scale increased over the small range of spatial scales tested in our study. However, the modulatory effects of biocrust cover, perennial tussocks, and artificial irrigation on similarity was more evident at medium and finer scales. In general, biocrust was the most important factor at fine scales, where it reduced the similarity in SSBp in 5 × 5 cm cells. This clear effect of biocrust on the similarity was highly dependent on the presence of M. tenacissima according to the complex interaction between these two biotic components and their variations across spatial scales.

Spatial and temporal patterns in similarity between the standing vegetation and soil seed bank compartments

We found that the similarity between the standing vegetation and soil seed bank varied across spatial scales. The low similarity found in 5 × 5 cm cells for both seed banks was probably related to the dispersal distance of these annual plants, which can easily exceed this fine scale (Peralta et al. 2016, 2023). If seeds fall more than 2.5 cm away from the adult plant, they will fall outside of the cell. Evidently, the similarity should increase when the observed soil sample is larger. In fact, the highest similarity between both diversity compartments (around 55%) occurred at the largest spatial scale considered (20 ´ 20 cm), and this value is similar to those observed in other grassland communities at larger spatial scales (Hopfensperger 2007), probably because the dispersal distance of most species in the community was at least 20 cm away from the mother plant (Venable et al. 2008; Thomson et al. 2011; Olano et al. 2012). In addition, as the sampling area increases, there is a greater likelihood of encountering more species and matching with those in the sampled soil seed bank. Thus, the spatial scale determined the effects of biocrust and perennial vegetation on the seed bank–vegetation interaction. The effects of biocrust were evident at 5 ´ 5 cm and they interacted with those of tussocks at 10 ´ 10 cm, but the effects of tussocks were found at all scales. This finding is in agreement with the size of the M. tenacissima tussocks, which were around 1 m in diameter, and it contrasts with the high spatial variation with the biocrust at finer scales (Martínez et al. 2006; Concostrina-Zubiri et al. 2018).

Furthermore, year was the main factor related to the vegetation–soil seed bank interaction. Most of the observed variability in the vegetation–soil seed bank similarity was related to the year when the standing vegetation was sampled, where the similarity was higher with the vegetation in the previous year. However, the relationship between similarity and the time between observations was not linear. Indeed, the soil seed bank samples collected in 2010 and the vegetation recorded in 2010 and 2009 were quite similar, but the similarity was lower when the vegetation in 2008 was considered. This temporal pattern in the similarity agrees with that expected according to the spiral model, with decreased similarity along time (Caballero et al. 2008). However, the significant difference between the similarity in 2008 and the other two years could be explained by the extremely dry conditions during the first year, but above average rainfall during 2009 and 2010, and rapid increases in the similarity with the soil seed banks. The contrasting rainfall patterns within this short time period demonstrate its great influence on the community dynamics, as found previously in gypsum outcrops (Peralta et al. 2019) and other Mediterranean grasslands (Carmona et al. 2015), and also on the changes in the soil banks in these environments (Olano et al. 2012). The increase in similarity as the rainfall increased was not as clear with the irrigation treatment, which simulated an increase in spring rainfall but not autumn–winter rainfall. Thus, irrigation could have allowed established species to develop better and produce more seeds, but it did not promote the incorporation of species that were not present in the assemblage during the autumn. These findings demonstrate the great important of the variability in the rainfall pattern. In fact, observing the contrasting rainfall patterns over three years highlighted the resilience of the communities as well as their rapid recovery from dry years and the corresponding lack of reproduction, which has been observed under artificial experimental droughts in these gypsum annual grasslands (López-Rubio et al. 2022).

Biotic and abiotic factors modulated aboveground–soil seed bank similarity

The presence of M. tenacissima tussocks and irrigation treatment also affected the similarities between the standing vegetation and soil seed bank, although to a much lesser extent. Near tussocks, the similarity between the standing vegetation and seed bank increased, especially with no water irrigation, probably due to increased germination of the seeds of annual species near M. tenacissima tussocks where the water availability was greater (López-Pintor et al. 2003; Quevedo-Robledo et al. 2010; Soliveres et al. 2011). Furthermore, under milder conditions, vegetation will produce more seeds that many be incorporated into the seed bank, thereby increasing the similarity between both community compartments (Zhao et al. 2007). Previous studies also found that perennial shrubs can act as seed traps by increasing the number of seeds under the canopy (Bullock and Moy 2004), which may synergistically increase the similarity due to the improved conditions near tussocks.

Biocrust cover decreased the similarity between vegetation and the SSBp in open areas at both the 5 ´ 5 cm and 10 ´ 10 cm scales. In addition, the biocrust reduced the similarity with SSBc but only near M. tenacissima tussocks. Thus, the presence of a well conserved biocrust filtered the seeds that entered and/or emerged from the soil, and hence the community assembly (Sánchez et al. 2022). The effects of biocrusts on plant development have been widely reported (Havrilla et al. 2019), where they can act as physical barriers (Romão and Escudero 2005; Ortiz et al. 2022). In particular, biocrusts can prevent seeds from entering the soil so they remain on the surface exposed to seed predators, which may reduce the number of seeds that germinate in the following season (Li et al. 2005). Moreover, biocrusts can decrease the germination of seeds that are already in the soil by hindering the emergence of seedlings (Hawkes 2004; Escudero et al. 2007; Peralta et al. 2016). This barrier effect was expected to be even greater at our study site where the dominant lichen species is Diploschistes diacapsis (Ach.) Lumbsch (8% of mean cover at 5 ´ 5 cm). This crustose lichen forms almost continuous and very hard large carpets, with few hollows, thereby greatly hindering the accumulation of seeds and their incorporation into the seed bank (Prasse and Bornkamm 2000; Belnap et al. 2001; Li et al. 2005), especially into SSBp. By contrast, the similarity with SSBc increased because many recently dispersed seeds were trapped in the biocrust and germinated in the following season. At the 20 ´ 20 cm scale, this effect disappeared in both soil seed banks, probably due to the higher heterogeneity of biocrusts at this spatial scale, with a patchy distribution containing several species, border areas, and small portions of soil intermingled where large amounts of seeds could accumulate, thereby diluting the effects of the biocrust cover (Concostrina-Zubiri et al. 2018).

In summary, we found clear increases in the similarity between the standing annual vegetation and soil seed bank at the larger spatial scales evaluated in our study, which were probably related to dispersal. Our results also confirmed the predictions of the so-called spiral model by showing that the similarity between the soil seed bank and vegetation was tightly related and it changed with time. In addition to these two intuitive and major patterns, the similarity between the two plant community compartments was modulated by the different biotic and abiotic determinants assessed in the present study. In particular, two consistent trends were identified where the presence of M. tenacissima tussocks increased the similarity between the two compartments of the annual plant community whereas the biocrust cover had the opposite effect. SSBp was affected the most by biocrust, especially at the very small scale (5 ´ 5 cm). In conclusion, our findings are compatible with hierarchical effects of the variables considered in this study on the similarity between the standing vegetation and soil seed bank compartments. Interannual shifts were the main determinants of similarity but tussocks, biocrusts, and irrigation slightly modulated the similarity, thereby demonstrating that multiple processes affected vegetation–soil seed bank interactions.

SSBc

Complete soil seed bank

SSBp

Persistent soil seed bank

Acknowledgements

We thank the Spanish Meteorological Agency (AEMET) for providing climatic data. We also acknowledge Jose M. González and Marcelino de la Cruz for their assist with the statistical analysis and Silvia Matesanz for her valuable comments of the manuscript.

Funding

This study was supported by the European Social Fund managed by the Regional Government of Madrid (Remedinal TE-CM: S2018/EMT-4338) and by the Horizon 2020 initiative from the European Commission (GYPWORLD, H2020-MSCA-RISE-777803).

Author Contributions

Ana M. Sánchez, Arantzazu L. Luzuriaga and Adrian Escudero contributed to the study conception and design. Material preparation and data collection were carried out by Ana M. L. Peralta, Ana M. Sánchez and Arantzazu L. Luzuriaga. The data analysis was performed by Roberto López-Rubio and David S. Pescador. The first draft of the manuscript was written by Roberto López-Rubio and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Competing interests

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.

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Table 1

Results obtained with linear mixed models to assess the effects of M. tenacissima presence (Tussock-Open), irrigation treatment (Irrigation-Control), and biocrust cover on the similarity indexes between the standing vegetation and the complete and persistent soil seed banks estimated at three scales (5 ⋅ 5 cm, 10 ⋅ 10 cm, and 20 ⋅ 20 cm). Co: sign of the coefficient, Chisq: Chi-square. Amounts of variability explained by fixed effects (M. tenacissima presence, irrigation, and biocrust cover), repeated measures random effect (sampling year), and the whole model are indicated. Significant data are highlighted in bold.
Scale	5 ⋅ 5 cm						10 ⋅ 10 cm							20 ⋅ 20 cm
	Complete seed bank N = 1136			Persistent seed bank N = 1009			Complete seed bank N = 506				Persistent seed bank N = 472			Complete seed bank N = 142			Persistent seed bank N = 142
	Co	Chisq	P	Co	Chisq	P	Co	Chisq	P	Co		Chisq	P	Co	Chisq	P	Co	Chisq	P
Tussock	+	7.15	0.007	-	1.20	0.27	+	7.15	0.007	-		8.31	0.004	+	2.55	0.11	+	14.54	0.0002
Irrigation	+	2.34	0.17	-	0.74	0.39	+	2.34	0.17	-		19.33	< 0.0001	+	0.88	0.35	-	3.07	0.08
Biocrust cover	+	0.21	0.64	-	15.94	< 0.001	+	0.21	0.64	-		0.60	0.44	+	0.06	0.81	+	0.16	0.69
Tussock * Irrigation	-	7.67	0.006	+	0.12	0.73	-	7.67	0.006	-		11.87	< 0.001	-	0.01	0.95	-	0.46	0.5
Tussock * Biocrust	-	12.32	< 0.001	+	11.60	< 0.001	-	12.32	< 0.001	+		4.37	0.037	-	0.39	0.53	-	0.25	0.62
Irrigation * Biocrust	-	0.68	0.41	+	0.95	0.33	-	0.68	0.41	-		2.55	0.11	-	0.02	0.89	+	0.45	0.50
Tussock * Biocrust * Irrigation	+	0.29	0.59	-	1.85	0.17	+	0.29	0.59	-		2.04	0.15	+	1.34	0.25	+	0.03	0.87
Variability	Fixed factors	Random factor	Model	Fixed factors	Random factor	Model	Fixed factors	Random factor	Model	Fixed factors		Random factor	Model	Fixed factors	Random factor	Model	Fixed factors	Random factor	Model
explained	0.04	0.53	0.57	0.02	0.18	0.20	0.04	0.53	0.57	0.08		0.19	0.27	0.01	0.79	0.80	0.06	0.53	0.59

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Biotic and abiotic determinants modulate interactions between standing vegetation and soil seed bank across fine spatial scales

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