1. Introduction
The seed bank is the viable seeds stored in soil and are available for potential germination and recruitment of new individual plants [
1]. Seed banks sustain the diversity of plant communities and contribute to re-colonization [
2] and restoration of habitats [
3]. Therefore, they have both ecological and applied benefits. Understanding the factors affecting the composition and dynamics of a seed bank will give insights into ecosystem functioning and the future community responses to climate change [
4]. Seed banks are very important for population persistence in arid ecosystems where opportunities for seed germination and seedling establishment are unpredictable [
5] because rainfall, the major limiting factor, is scarce, unpredictable and highly variable in both space and time [
6]. Seed banks allow plants to persist in the environment, enduring successive years without rainfall until appropriate conditions for their germination and establishment occur [
7]. Seed banks in desert ecosystems are crucial to maintain the occurrence and genetic diversity of annual plant populations [
8,
9] because the only way for annual plants to survive in such an unpredictable risky environment is to accumulate a persistent seed bank [
10]. Generally, seeds of annual plants constitute a large proportion of seed banks in desert habitats [
11,
12]. Despite the importance of seed banks in desert ecosystems, studies aiming to understand their composition, spatial and temporal patterns are scarce [
4], in particular for the deserts of the Middle East [
12].
The size and species composition of seed banks in desert soils are influenced mainly by rainfall, which determines the growth and reproduction of the above-ground vegetation, and thus affects seed yields [
13]. Annual variation in rainfall may affect the germination events, growth and seed production of plants [
14], and also affect the accumulation of seeds in soil [
15,
16]. Furthermore, microtopographic conditions indirectly determine the spatial patterns of soil seed banks through driving the distribution of the above-ground vegetation [
12].
In addition to physical factors, above-ground vegetation composition influences soil seed reserves in deserts. Plants belonging to different plant life forms with various reproductive strategies contribute differently to the abundance and species richness of the soil seed bank. Trees and shrubs contribute less importantly to seed reserves in soil, while annual species contribute more to soil seed banks than other life forms [
12].
Desert vegetation is largely distributed in patches within a bare soil matrix [
17]. These patches are usually dominated by shrubs [
17] that play a strong nurse role in facilitating their under-canopy plants by creating more favorable microhabitats through mechanisms such as shading, increasing soil moisture content and buffering against extreme temperatures [
18,
19]. Various studies in arid regions showed that the frequency and intensity of facilitation increase with decreasing rainfall [
20,
21]. However, some recent studies indicated that facilitative effects of shrubs on their understory plants does not increase monotonically with decreasing precipitation, and that the positive effects of shrubs decrease or cease or may even be reversed under severely low rainfall conditions [
22,
23]. To interpret this later pattern, these studies suggested that facilitative effects of shrubs on soil moisture diminish [
22] or shift to negative influences [
23,
24] under severely low rainfall deficit.
The differences in habitat conditions between vegetation patches and bare ground affect the overall community composition and structure, and the spatial distribution of seed reserves in soil [
25,
26]. Shrubs facilitate the accumulation of seeds beneath their canopies by trapping seeds or acting as a barrier for their movement [
27]. Shrubs can also indirectly facilitate seed accumulation by acting as a perching site for seed-carrying birds [
28] or as a cache for granivorous rodents [
29]. Moreover, shrubs may indirectly enhance soil seed banks by facilitating the growth and seed production of the standing annual plant community [
26]. Accumulation of seeds under shrubs leads to spatial heterogeneity within soil seed banks, and causes greater seed abundance and seed species diversity beneath shrubs compared to open spaces [
30].
The variation in the effects of shrubs on soil moisture with different rainfall amounts may in turn influence the species richness, abundance, growth and reproduction of above-ground plants [
22,
23,
31] and, consequently, soil seed replenishment [
8]. Similarly, the individual and interactive effects of shrubs and rainfall on soil moisture content may influence the ability of an above-ground plant community to regenerate from the soil seed bank, which finally determines the seed bank–vegetation similarity, particularly in arid environments where annual plants constitute the main component of both the vegetation and soil seed bank.
The present study aimed to assess the effects of the desert shrub Haloxylon persicum Bunge ex Boiss. & Buhse (Chenopodiaceae) on the composition and species richness of soil seed banks of annual plants in northwestern Saudi Arabia during two consecutive growing seasons (2017–2018 and 2018–2019), which differed in precipitation. We hypothesized that: (1) shrubs facilitate the accumulation of soil seed banks, (2) the strength of the facilitative effects would be lower following a dry growing season than after a moister growing season, and (3) shrubs affect the degree of similarity between soil seed banks and the standing vegetation, and their effects vary with growing-season rainfall, with similarity being lower under shrubs than in openings after a dry growing season, but following a wetter season an opposite pattern is predicted.
3. Discussion
The total density of germinable soil seed bank of annual plants in the study area is relatively low, varying between 213 and 748 seeds/m
2. Comparable low densities of germinable seed bank of annual species were reported in the sandy Monte Desert in Argentina [
15], where seed density ranged between 295.2 and 608.1 seeds/m
2. Most studies on soil seed banks, particularly in arid regions, were based on the total direct seed counts from soil samples and not on the germinable fraction of seeds, resulting in higher seed estimations [
32].
Our results support the hypothesis that shrubs accumulate a large and diverse seed bank beneath their canopies. Accumulation of seed bank under shrubs may be the result of seed input received by wind and water and trapped beneath shrubs [
27,
33]. Shrubs also offer perches and food to birds, which may contribute to recruiting zoochorous species to soil seed banks [
34]. By modifying the physical and chemical properties of soil, improving soil microrelief, reducing direct sunlight, and enhancing soil moisture and fertility, shrubs can indirectly increase the soil seed bank by facilitating colonization, growth, flowering, and seeding of herbaceous species under their canopies [
18,
19]. In the present study,
H. persicum shrubs improved sub-canopy soil fertility by enhancing soil organic carbon and nutrients (N, P and K). Compared to bare ground, soils beneath
H. persicum canopies had greater content of silt and clay, which may be related to the accumulation of wind-blown, fine soil particles below shrubs [
35]. The fine soil texture under shrubs facilitates the accumulation of more seeds in the soil seed bank [
36]. It is apparent that shrubs affect the soil seed bank through various mechanisms. In spite of not knowing the relative contribution of each of these mechanisms in determining the impact of
H. persicum shrubs on the soil seed bank, we suggest that the physical role of shrubs in trapping seeds is the most important, followed by the facilitative effects of shrubs on above-ground vegetation.
For both microhabitats, the density of germinable soil seed bank was about twice larger after the wet growing season than after the dry season. Likewise, the species richness of the seed bank was about 1.2 times greater following the wet growing season than after the dry season. The enhancing effects of rainfall on seed banks were reported by Gutiérrez and Meserve [
32] in an arid thorn scrub community in north-central Chile, Li et al. [
37] in the Hengduan Mountains region of southwest China, and Gomaa [
16] in the Eastern Desert of Egypt.
In accordance with our hypothesis, the facilitative effects of
H. persicum shrubs on the soil seed bank were more intense after the wet growing season than after the dry season. This may be attributed to the variation in the effects of shrubs on the above-ground annual vegetation between growing seasons, where shrubs enhanced the standing annual plants, as measured by species richness, during the wet growing season, consequently increasing seed output and enriching the soil seed bank. Conversely, shrubs exerted a negative effect on the understory above-ground annual species during the dry season, which finally reduces seed yield. The change in the effect of shrubs on annual vegetation between the two growing seasons in our study may be related to the fact that shrubs enhanced water availability in the sub-canopy soil during the wet growing season, but reduced soil moisture content beneath their crowns during the relatively dry season. Similar observations were reported by O’Brien et al. [
24] in a semi-arid shrubland and by Gomaa et al. [
23] in a hyper-arid Arabian desert. During small rain events, shrubs might decrease water availability beneath their canopies by intercepting rainwater [
31,
38]. Additionally, water intercepted by shrub crowns during small rain events is lost to evaporation and in wetting the canopy surface, and is less likely to reach soil below shrubs [
39]. Under severely low rainfall, all of these factors make the sub-canopy soil dryer than soil of the shrub interspaces. Conversely, under moderate and heavy rains, shrubs pass water intercepted by their crown to the understory soil through stemflow [
40,
41]. In addition, the low evaporation under shrubs [
22] may increase moisture retention in the sub-canopy soil. Therefore, during a relatively wet year, sub-canopy soil is wetter than bare soil.
There is a correspondence between the patterns of species richness of annual vegetation and seed bank–vegetation similarity. For both microhabitats, the overall similarity between seed bank and standing annual vegetation was greater in the wet growing season than in the dry season. At microhabitat level, the similarity was greater in open areas than under shrubs in the dry season. By contrast, the soil seed bank was more similar to above-ground vegetation in sub-canopy microhabitat than in bare ground during the moist growing season. These results suggest that the greater the species richness of the above-ground annual vegetation, the greater the degree of similarity between the floristic composition of the seed bank and the standing annual vegetation. Communities characterized by preponderance of annual plants show high resemblance between the seed bank and vegetation composition [
12,
42] because annual plants rely mainly on the seed bank for their regeneration and contribute more to the seed bank than perennials. The degree of correspondence between soil seed bank and standing annual vegetation recorded in our study was relatively high (overall similarity mean = 0.58) and comparable to that reported for the north edge of the Taklimakan Desert [
43], southern Gurbantunggut Desert dunes during winter [
44] and sandy grasslands of eastern Inner Mongolia [
45], where the similarity coefficients were 0.778, 0.63 and 0.66, respectively.
During the wet growing season, which had the greatest species richness of both the seed bank and above-ground annual plants, the average seed bank–vegetation similarity was high (>0.70). This suggests the potential use of soil seed banks for the restoration of annual vegetation in case of habitat deterioration due to anthropogenic activities or climate change effects. Our results showed also that
H. persicum shrubs enhanced soil fine particle content, soil nutrients and accumulation of the soil seed bank beneath their crowns. Therefore,
H. persicum shrubs could be applied in the rehabilitation of desertified ecosystems in arid regions. Desert shrubs are known as potential tools in the restoration of desertified arid lands [
46].