Recovery of Perennial Plant Communities in Disturbed Hyper-Arid Environments (Sharaan Nature Reserve, Saudi Arabia)

Abstract

Background: Human activities such as agriculture are known to markedly affect natural ecosystems, including plant communities and soil properties. Biological activities are reduced in hot, hyper-arid ecosystems compared to temperate and tropical climatic conditions. Anthropogenic disturbances therefore have greater impacts on the ecosystem’s recovery potential. This study aimed to assess the diversity and recovery of post-agriculture plant communities in the Sharaan Nature Reserve (SNR), located in northern Saudi Arabia. Methods: Three types of habitats representative of different disturbance situations were identified in the reserve and sampled through 103 floristic and pedological surveys. The floristic composition was recognized and relative quantification of soil atomic elements was performed. The obtained data were processed using different statistical treatments such as the Shannon index and Bray–Curtis dissimilarities, non-metric multidimensional scaling (NMDS), Kruskal–Wallis tests and Redundant analysis (RDA). Results: Investigations led to the identification of 48 plant species belonging to 24 genera and 22 botanical families. Specific plant community structures were correlated with each habitat, and bioindicator plant species were identified. Polycarpaea repens and Stipagrostis plumosa were linked with natural habitats, while Atriplex leucoclada was specific to disturbed habitats. In contrast, Asteriscus graveolens and Haloxylon salicornicum were found to be ubiquitous species. Conclusions: The presence of bioindicator species was closely associated with the different soil properties measured in each habitat. Restoration strategies related to the overall dynamic plant community succession pattern observed in the Sharaan Nature Reserve are discussed. Active ecological restoration strategies based on targeted active ecological restoration interventions should facilitate the recovery and restoration of disturbed plant communities in hyper-arid areas.

1. Introduction

Managing natural habitats in hyper-arid environments is a major challenge, of which understanding the vegetation–environment relationship through the identification of environmental factors responsible for the formation and distribution of plant communities are the main keys [1,2]. In these harsh areas, some environmental factors are known to influence plant community composition [3,4,5], for example, topographic factors as well as soil properties [6,7], in particular soil electrical conductivity (EC), pH [8], and texture [9]).

Many studies have highlighted the influence of soil variables on the structure and composition of vegetation in arid environments [10,11,12]. They suggest that natural or anthropized habitats have abiotic (soil properties) as well as biotic (plant and animal species) characteristics that allow us to identify and characterize different types of habitats. For example, disturbed habitats should present advanced stages of disturbance in terms of biodiversity and chemical properties of the soil, which can be observed through several indicators such as low concentration of organic matter or the presence or absence of certain plant species.

In general, plant community responses to environmental and spatial variables, such as soil properties, can be very complex and depend on several parameters such as climate variation, urbanization, and agriculture [13]. Agriculture is one of the main human activities threatening biodiversity and natural habitats by directly modifying the soil properties, reducing connectivity, introducing alien species, and increasing ecosystem fragmentation [14,15]. Soil physicochemical properties are considered to be a key factor governing floristic diversity, and the deterioration of soil chemical properties often leads to a decline in biodiversity, especially in hyper-arid areas [13,14,15,16]. This biodiversity loss largely contributes to the disruption of local ecosystem functioning by significantly reducing ecosystem services and resilience to various ecological and anthropogenic disturbances [17]. Anthropogenic activities have impacts on plant biodiversity, fauna, and natural habitats, often via the conversion of natural areas into agricultural plots [17,18] whose abandonment after decades of use may hamper the recovery of the native plant communities [19,20]. As data on plant communities present before agricultural conversion are often lacking, plant communities growing in the untouched surrounding natural ecosystems are often considered as being representative of the reference plant communities [20,21]. Several studies worldwide have shown that the recovery of reference plant communities in abandoned agricultural areas may take up to five decades [22,23,24]. The length of this ‘natural recovery process’ largely varies depending on the extent of ecosystem disturbance and on whether the ecosystems have already crossed irreversible thresholds towards alternative stable states. Otherwise, it is accepted that natural recovery processes can be enhanced and facilitated by certain specific actions within an assisted regeneration process [25].

Moreover, there is evidence that there is little available literature exploring the soil–vegetation relationship in arid areas [26], and even less in abandoned cultivated environments in the Arabian Peninsula.

In fact, cultivation land-use legacies have been widely studied around the world in different ecosystems, i.e., in Africa, Asia, Australia, Europe, and North America, including semi-arid shortgrass steppe lands and in the Sonoran Desert [23,27,28]. However, agricultural legacies in natural ecosystems in the Middle East, including the Arabian Peninsula, have received far too little attention [29]. Apart from the study of Al-Rowaily et al. [30]., which reported changes in the perennial floristic composition and in the soil properties following 40 years of agricultural abandonment in the Al-Kharj area (southeast of Riyadh, Saudi Arabia), no studies on this issue have been carried out in the Arabian region.

Sharaan Nature Reserve (SNR) is a protected area located in AlUla County (NW KSA). It was created in 2020 with the main objective of protecting biodiversity from human activities, including grazing, off-road driving, plastic pollution, and agriculture. Within the reserve, many areas have long been cultivated as oases and/or other local market garden crops. These cultivated areas were subsequently abandoned following the creation and closure of the reserve but remain easily identifiable by the traces of recent agriculture in these sites. In the reserve, three types of areas, here referred to as habitats, were defined: (a) natural habitats representing preserved natural ecosystems where no traces of human activity were observed; (b) disturbed habitats in abandoned farms, representing extreme disturbance situations; and (c) semi-natural habitats with visible traces of human activities, representing intermediate disturbance situations. The choice of the SNR for the present study was mainly based on this historical context, as well as the current protection status, which provides optimal experimental conditions for the study.

This paper addresses the issue of soil–vegetation relationships in hyper-arid environments through the analysis of the recovery dynamic process of disturbed plant communities due to agriculture from the perspective of ecological restoration of the vegetation in SNR.

We suggest the existence of a close and specific relationship between soil properties (chemical elements) and vegetation whose precise understanding would allow us to formulate some relevant solutions to one of the most crucial management issues in the reserve—the restoration of habitats by re-establishing natural plant communities. The hypothesis suggests that precise knowledge of this relationship, including the causal links between vegetation structure, dynamic stage, characteristic indicator species, and chemical properties of each identified habitat, could allow targeted active restoration interventions likely to support the natural recovery of plant communities in the reserve to be tested.

In this study, we aimed to investigate the potential differences in soil chemical properties from the 103 different surveys in the reserve, with the goal of restoring disturbed and semi-natural habitats.

Therefore, the paper will try to fill the gap, first, in terms of knowledge of the biodiversity of local perennial flora and then the dynamic processes of recovery of disturbed habitats and natural plant communities in the SNR. Its final purpose will be to develop an ecological restoration approach that can help the natural process of recovery of these communities by providing specific technical support to this management issue in the SNR.

2. Materials and Methods

2.1. Study Area

The study was carried out in the Sharaan Nature Reserve (SNR) in AlUla County, in northwestern Saudi Arabia. The SNR was designated as a nature reserve by the RCU while contributing to the national Saudi Green Initiative that aims to restore vegetation cover throughout the country. Since 2020, fences have been installed to avoid human and animal disturbance, such as agriculture, off-road driving, overgrazing, and plastic pollution [31].

SNR spans 1500 km² (579 mi²) of soaring red-rock canyons, sprawling desert, and valleys carpeted in delicate wildflowers, offering a treasure trove of natural biodiversity. The reserve is located in a hyper-arid environment with 50 mm of average annual rainfall that mainly occurs during occasional thunderstorms between November and February. The average annual wind velocity is 10.4 km/h and the average annual temperature ranges from 4 °C to 38.9 °C (mean 28.4 °C), with significant variations in averages between winter and summer (meteostat.net). Soils are formed up to 1.5 m depth on Cambrian sandstone formations [32]. For the study, a 25 km² area representative of the SNR environment was selected, encompassing the 103 study sites (Figure 1).

2.2. Definition of Habitats and Selection of Study Sites

Site selection was based on visible signs of human activities (i.e., overgrazing, traces of off-road driving, plastic residues, etc.) and the use of satellite images to precisely locate the abandoned farm boundaries. The three types of habitats were defined and localized according to these criteria (Figure 1, Supplementary Table S2):

Natural habitats: These habitats represented the most advanced vegetation stage in hyper-arid environments, where no traces of human activity were observed. They included areas of rich open vegetation consisting mainly of shrub species but with the presence of Acacia sp., indicating a potential local vegetation climax. Sandy dunes were also present, dominated by Haloxylon persicum Bunge, an indicator of optimal vegetation in open, sandy environments.

Disturbed habitats: These habitats represented the most degraded environments related to past agricultural activities (i.e., abandoned farms). The vegetation was mainly composed of dense herbaceous plants, dominated by Poaceae species, and sometimes, no vegetation was observed. The soil was mainly silty-clayey with visible surface cracks and crusting.

Semi-natural habitats: These habitats represented moderately degraded environments with some traces of human activities (i.e., overgrazing, traces of off-road driving, plastic residues). These habitats were often located near abandoned farms where agriculture had partially impacted the ecosystem. The vegetation was mainly dominated by Haloxyon salicornicum (Moq.) Bunge ex Boiss. and the soil was mainly sandy.

A total of 103 sites representative of the three different habitats were selected for this study.

2.3. Vegetation Sampling

Circular floristic surveys were carried out in 50 m² plots (for a 4 m radius circle) in the 103 sites, and the species cover was evaluated using the percentage abundance method [33]. As the study was interested only in perennial plants from a floristic point of view, the surveys were conducted in November 2021 (dry season) to avoid confusion with annual species. According to Berg and Steinberger (2012), in the study of vegetation in desert environments, perennial plants are more important than annual vegetation, which may be absent for several years because of climate variations in this environment [34].

The species identifications, nomenclature, life forms, and chorology were based on the reference work of Chaudhary [35,36,37] and that of Gillet [38].

2.4. Soil Sampling and XRF Data Analyses

Soil samples were collected from the center of each circle used for floristic sampling, for a total of 103 soil samples. Previous studies in this area revealed a single soil horizon between 0 and 80 cm deep, including soil profiles in disturbed and natural ecosystems [39,40]. A soil collection depth of between 30 cm and 40 cm was therefore chosen as representative of the total soil horizon profile. For each soil sample, 600 g of soil was collected and directly sieved using a 2 mm sieve in the field. Before further analyses, soils were dried at 105 °C for 3 days.

Relative quantification of soil atomic elements, from magnesium (Mg) to uranium (U), was performed on the 103 soil samples using a portable X-ray fluorescence (XRF) device (XRF S1 Titan, Bruker, Billerica, MA, USA). Triplicates of each soil sample were prepared by packing 10 g of soil into a plastic cap and covering it with a prolene film (SCP Science; Baie-D’Urfe, QC, Canada) for each replicate. Then, three XRF measurements were performed on each replicate, resulting in a total of nine measurements per soil sample (GeoExploration mode with the following settings: phase 1, 30 s; phase 2, 30 s; and phase 3, 45 s). The nine measurements were then averaged and calibrated according to the limit of optical detection of each atomic element (provided by Bruker) (Supplementary Table S3).

Common soil physicochemical parameters such as organic matter, organic carbon, nitrogen, and pH have been measured in the Sharaan Nature Reserve in previous studies, and have revealed very low soil fertility (often below technical thresholds for carbon, organic matter, and nitrogen) and thus no significant differences between disturbed and natural ecosystems could be detected for these parameters [39,40,41].

2.5. Statistical Analyses

All statistical analyses were performed with R software (R version 4.3.1) using a data matrix designed for this purpose (Supplementary Table S2). To measure the plant species richness and plant community structure, the Shannon index and Bray–Curtis dissimilarities were calculated using the vegan package, as well as the non-metric multidimensional scaling (NMDS) algorithm. The Kruskal–Wallis tests were then performed to assess the significance of each group using the dunn.test function in the dunn.test package (p < 0.05).

Redundant analysis (RDA) was performed using the BiodiversityR package to correlate plant diversity with the soil properties. Hellinger transformation was performed before RDA using the vegan package. A random independent permutation test and Holm correction were then applied to identify significant soil chemical elements associated with plant diversity (p < 0.01).

Principal component analysis (PCA) was performed using the FactoMineR package for the soil property analyses. XRF measurements provide the relative abundances of atomic elements from Mg to U, which results in a compositional dataset including some correlated variables and non-detected elements (values = 0) [42]. Centered-log ratio (clr) transformation was therefore applied to the dataset using the compositions package [43]. Principal component analysis was then performed to identify correlated variables using the FactoMineR package [44]. Only nine variables, representative of the chemical dataset variability and known as important parameters related to soil chemical fertility, were selected in the results section (Mg, Al, Si, P, S, K, Ca, Fe, and Cu). Permutational multivariate analysis of variance (PERMANOVA, p < 0.001) was performed to test the significance of the three soil clusters using the adonis2 function (with 999 permutations and the Euclidean method) from the vegan package.

Kruskall–Wallis test followed by a posthoc pairwise test was then performed to test the significance of each chemical element in the three habitats using the dunn.test function in the dunn.test package (p < 0.05).

3. Results

3.1. Overview of Plant Diversity in the Sharaan Nature Reserve

This study involved 103 floristic surveys in which 48 species of plants belonging to 24 genera and 22 different botanical families were identified (Supplementary Figure S1 and Table S1). The Flora in the study area was mainly dominated by Poaceae (seven species, 15%), Fabaceae (six species, 13%), and Amaranthaceae (four species, 8%). Other families were also moderately present, such as Zygophyllaceae, Boraginaceae, and Brassicaceae (three species each, 6%). Apocynaceae, Convolvulaceae, Cucurbitaceae, Lamiaceae, Resedaceae, and Solanaceae families were present to a very minor extent (two species each, 4%), while the remaining families present in the study area were represented by a single species each (2%).

Regarding the biological types of the species, it turns out that Chamaephytes dominate with 24 species (44%), followed by Hemicryptophytes and Phanerophytes with 10 species (18%) each. The other life forms are only weakly represented in the inventory (Supplementary Table S1).

The chorology of the identified taxa is dominated by the Saharo-Arabian element with more than 50% (30 species), followed by the Sudanian element (26%, 16 species) as well as the Irano-Turanian element (11%, 7 species). The other elements only have between 1 and 2 species each (Supplementary Table S1).

3.2. Plant Community Structure

We assessed the impacts of anthropogenic activities on the vegetation by comparing the plant diversity and plant communities of the three previously defined habitats (i.e., disturbed, semi-natural, and natural). No significant differences were observed between the semi-natural and natural habitats, in contrast to the disturbed habitats (i.e., abandoned farms), with respect to the vegetation density, species diversity, and plant communities, indicating that agriculture had a greater impact on the plant community structure compared to other human activities (such as grazing, off-road driving, or plastic residues in semi-natural habitats) (Figure 2). A significantly higher vegetation density but lower vegetation diversity was observed in the abandoned farms compared to natural and semi-natural habitats, indicating that some species largely dominated the disturbed habitats (Shannon index, Figure 2a,b).

To determine the species that were most represented in each of the three habitats, the total number of individuals was calculated (total number of counts/species in each habitat; Figure 3; Supplementary Table S1). As expected, one species, i.e., Atriplex leucoclada, largely dominated the disturbed habitats in abandoned farms. This species was also found in semi-natural habitats but not in natural habitats, indicating that the semi-natural habitats, which were often located in the vicinity of abandoned farms, had also been impacted by agriculture. In contrast, the Polycarpaea repens and Stipagrostis plumosa species were mainly found in natural and semi-natural habitats, suggesting that they could be bioindicators of non- or low-disturbed habitats. Finally, Asteriscus graveolens and Haloxylon salicornicum were both found in the three habitats, indicating that these generalist species were able to withstand high anthropogenic disturbances and develop in contrasting environments.

Other plant species were more rarely found in natural habitats and can indicate minor differences in the microclimatic conditions and/or the soil properties. For instance, Acacia gerardii and Lycium shawii were found in species-rich open shrubland formations, often in shady places with deep loamy sandy soils. In contrast, Ficus palmata and Lavandula pubescens were found near the foot of red sandstone cliffs, often inaccessible to animals, with a conglomerate of sandy soil and alluvial sediments. Haloxylon persicum, Convolvulus spicatus, and Moltkiopsis ciliata were especially found in deep sandy soils such as dunes and small sand mounds (nabkhas) in open environments often exposed to wind and dust.

3.3. Soil Chemical Properties Partially Explain Differences in Plant Communities

We first measured the soil chemical properties of sites (by X-ray analyses, see Methods) to assess whether the differences in plant communities could be related to changes in the soil chemical properties in the three habitats (Table 1, Supplementary Figures S2 and S3, and Tables S2 and S3). Globally, differences were observed in soil chemical properties between habitats, in accordance with their contrasted plant community structures (R² = 0.34, p < 0.001) (Supplementary Figure S2). For most chemical elements, a gradient was observed from natural to disturbed habitats, with a decrease in Si content and an increase in other elements, suggesting an increase in soil fertility in disturbed habitats (Table 1). Interestingly, these results showed a minor impact of agriculture on the soil properties of semi-natural habitats located near abandoned farms.

A redundancy analysis (RDA) was then performed to identify the soil chemical elements that could best explain the variance in the plant communities (Figure 4 and Supplementary Figure S4). The global RDA model explained 34% of the dataset variability. The first axis explained 19% of the variability and separated the disturbed habitats from the natural habitats. The second axis separated sites within the natural habitats and explained only 2% of the dataset variability, indicating that the natural habitat variability was poorly explained by the soil chemical composition. The soil Si, Mg, and Al contents, related to the differences in soil properties in the three habitats, were the chemical elements that best explained the plant community structure (11%, 6%, and 3% respectively; p < 0.05; Supplementary Figure S4). The two species Polycarpaea repens and Stipagrostis plumosa and Atriplex leucoclada were associated with the sandy natural habitats and the silty-clayey disturbed habitats, respectively, in accordance with the observed plant community structures (Figure 2 and Figure 3), thereby suggesting that these three species could serve as indicator species for these different habitats.

3.4. Relationship Between Vegetation, Species, and Soil Properties

The RDA (Figure 4) sufficiently assessed the vegetation–species–soil relationship in the study area. The distribution of plant communities characterized each by a specific type of environment, indicator species, soil type, and sometimes the presence of certain chemical indicator elements as part of agriculture legacy, is summarized as follows:

• -. The natural habitats presented three types of plant communities that are the species-rich open shrubland formations of Acacia gerardii and Lycium shawii growing in deep loamy sandy soils; the foot of red sandstone cliffs formations of Ficus palmata and Lavandula pubescens growing in a conglomerate of sandy soil and alluvial sediments; open sandy environment of Haloxylon persicum, Convolvulus spicatus, and Moltkiopsis ciliata found in deep sandy soils.

• -. Semi-natural habitats are communities dominated by Polycarpaea repens and Stipagrostis plumosa in sandy soils characterized by high SI and Mg concentrations.

• -. Disturbed habitats present plant communities dominated by Atriplex leucoclada in silty-clayey soils with high Cu concentrations.

3.5. “Active” Restoration Strategy (Targeted Active Ecological Restoration Interventions)

The results obtained following this study made it possible to define the pillar species characteristic of each of the habitats studied in relation to the degree of disturbance of the soil chemical properties. This led to a better understanding of the recovery process of abandoned cultivated and neighboring areas in order to define possible intervention actions aiming to facilitate this process, which naturally could take decades. Our results suggest that it would be recommended to intervene in the disturbed habitats at the edaphic level by improving the chemical properties of the soil (progressive supply of chemical elements) as well as at the biotic level by plantations based on Asteriscus graveolens/Haloxylon salicornicum and Polycarpaea repens/Stipagrostis plumosa. For semi-natural habitats, it would be advisable to intervene with an optimal supply of chemical fertilizing elements as well as plantations of Asteriscus graveolens/Haloxylon salicornicum and Polycarpaea repens/Stipagrostis plumosa (Figure 5).

4. Discussion

4.1. Diverse Flora Despite the Harsh Climatic Conditions

The floristic analysis of the study area revealed significant flora diversity, with a substantial share of perennial species. Regarding the dominant families, our results were generally in agreement with previously published findings in the hyper-arid zones of Saudi Arabia. Indeed, Poaceae, Fabaceae, and Asteraceae are the most represented families in Saudi Arabia [35,45]. Families such as Fabaceae and Zygophyllaceae were reportedly dominant in the few studies where perennial plants dominated the flora inventories, while Al-Rowaily et al. [30] reported the dominance of Chenopodiaceae in abandoned cultivation areas.

The low number of annual taxa in the inventory was due to the absence of rain in the region over a period of several months. Indeed, in hyper-arid ecosystems, water availability during the rainy period is closely related to the extent of annual flora expression [46]. Annual plants are also specifically biologically and phenologically adapted to these environments, which ensures their plasticity during extreme climatic periods [47,48]. However, the absence of rain for months or even years is a recurring phenomenon in these regions [49]. This could both impact the biodiversity of annual species and restrict the growth and development of trees, shrubs, and sub-shrubs [50] despite the fact that these plants are known for their resistance to arid environmental conditions.

The dominance of perennial plants in disturbed habitats has been reported in several studies. For instance, El-Sheikh [51] showed that the dominant flora in the late stages of succession in abandoned areas in Egypt consisted of shrubs and trees. This pattern has been also reported in several studies carried out in Saudi Arabia [30,49]. These results suggest that these disturbed areas are not conducive to the long-term expression of annual plants—contrary to perennial plants—and that the latter are more competitive over the long term in these habitats.

The dominance of Chamaephytes in hyper-arid areas of Saudi Arabia has been observed by several authors [52,53,54,55]. This could be related to the local biotic and abiotic conditions [56].

On the other hand, several authors in KSA [55] have reported the dominance of the Saharo-Arabian chorotype, which seems to dominate the flora of the country, especially the central part [57,58].

4.2. Plant Community Diversity Reflects the Different Degrees of Ecosystem Disturbance

Perennial species represent pillars of the plant communities structuring hyper-arid ecosystems in Saudi Arabia. When the pedoclimatic conditions are favorable, these perennial plants form patches of species-rich vegetation, or so-called fertility islands, which are viewed as being sites where a large part of the biological activity occurs in arid zones [39,59].

The dominant plant species observed in the study area constituted bioindicator species highlighting the different degrees of ecosystem disturbance. P. repens and S. plumosa, which were significantly associated with natural habitats, are known as characteristic species in natural desert environments with little or no disturbance [60]. In hyper-arid areas of Saudi Arabia, S. pulmosa is known as a representative species of open sandy desert shrubland plant communities, often associated with H. persicum, which prevails in natural environments that are quite rich in organic matter [61]. P. repens is a psammophilous species that is found mainly in inland dune ecosystems, such as in the UAE, where it is characteristic of Leotadenio-Rhynchosietum schimperi communities [62].

In contrast, A. leucoclada is a pioneer halophyte plant species that is commonly present in highly disturbed ecosystems in the Arabian Peninsula and Egypt, mainly in sabkhas (mudflats), coastlands, and inland salt marshes [51]. Moreover, other species identified in each habitat also provided consistent information on the habitat disturbance stages and/or the specific microclimatic conditions. For instance, plant communities with A. gererdii and L. shawii species associations were also observed in natural habitats in the Najd region, where they constituted woodland communities (very open tree stands) [63]. According to this author, these plant communities can be dominated by different Acacia species (A. arabica (Lam.) Willd., A. ehrenbergiana Hayne, A. tortitis (Forssk.) Hayne, A. raddiana Savi, A. farnesiana (L.) Willd.), but A. gerrardi especially prevails in these groups for particular edaphic and climatic reasons. In another study, Ficus palmata and Lavandula pubescens species association was also observed in a difficult-to-access environment (i.e., with rocky ridges, cliffs, and hills) where plants were protected from animal grazing [64].

In contrast, some species were ubiquitous with respect to their habitats. This was the case for A. graveolens and H. salicornicum. The latter generalist species has high resistance to hyper-arid climatic conditions and grazing, although it is grazed by camels [65,66]. H. salicornicum-dominated plant communities are present in almost all biogeographic sectors of Saudi Arabia at variable abundance rates [62]. This species is known to contribute to plant communities involved in dynamic transitions towards local climax vegetation or even degraded formations following any disturbance. In hyper-arid environments, H. salicornicum is often associated with other pioneer species, such as A. graveolens and Farsetia burtoniae Oliv., thereby representing part of the sparse herbaceous communities present on lower dune slopes [67]. This association is a marker of the advanced dynamic stages of pioneer vegetation, enhancing the natural recovery process prior to the establishment of native shrub plant communities.

4.3. Vegetation Recovery After a Disturbance Largely Depends on the Soil Properties

It is known that agricultural land use is often responsible for altering ecological processes in natural systems and that plant communities often require decades or even centuries to recover from these disturbances [20]. Changes observed in the typology of plant communities can indicate the degree of disturbance caused by land-use changes and abandonment [29]. The ecosystem post-cultivation ‘natural recovery process’, via the resettlement of native plant communities, is usually measured by comparison with control sites in which there is little or no disturbance [20]. Perennial vegetation cover and diversity are very low in abandoned agricultural land areas in the Sharaan Nature Reserve, thereby indicating the extent of disturbance that these environments have undergone. This could be explained by the fact that the establishment of shrub vegetation following a major disturbance, including agriculture, cannot be rapid and would take varying lengths of time [68]. This is closely related to the profound soil chemical composition modifications that take place, which play a major role in the establishment of the original vegetation [69]. The changes in soil chemical properties may have impacted the type of subsequently established vegetation, particularly in terms of time and floristic composition, which will, in turn, be influenced by the edaphic conditions in the hyper-arid environment [29,70]. In fact, it is widely recognized that such changes in soil chemical composition alter the stability, hydrological [71], and biological [72,73] processes in hyper-arid regions.

4.4. Understanding Soil–Vegetation Relationships for Restoration Planning

In the Sharaan Nature Reserve, natural habitats have three types of plant communities, each characterizing a given type of environment as well as particular edaphic conditions. The soils encountered in natural habitats are typical desert soils. According to Ping et al. [26], these soils are very dry and poor in nutrients, organic matter, and soluble salts. Furthermore, the richness in mineral elements could be due to wind erosion [8]. In this type of natural habitat, and in the presence of protection, as is the case in the study area (reserve area fenced since 2020) suffering from several anthropogenic actions such as grazing before closure, it is generally more reasonable not to plan any specific restoration action [74] given the multiple examples of ecosystems recovering over a period of decades without human intervention [75]. Several studies carried out in arid environments [76,77], have noted that closure would be a favorable tool for increasing phytomass and its expansion and enhancing their contribution to carbon sequestration. However, Liu et al. [78] highlighted that long-term fencing of more than 11 years would not be suitable for vegetation restoration and that rational and controlled grazing would be more favorable for the natural vegetation in these environments.

The semi-natural habitats within the reserve are presented as areas dominated by biennial species (P. repens, S. plumosa) found in sandy rangelands rich in mineral elements such as SI and Mg. These habitats, supposed to be affected by the surrounding agricultural activity, are quite similar to natural habitats in terms of soil properties. In contrast, the vegetation in this habitat remains a pioneer, indicating early stages of vegetation dynamics characterized by progressive recolonization by annual and biennial species [79], which should facilitate reaching more advanced stages, allowing the recruitment of shrubs and trees [80,81]. The presence of certain chemical elements in high concentrations cannot be considered as a deep modification of the chemical composition of the soil as these are proportions close to those in reference natural habitats. The restoration of these habitats may suggest a reinforcement of the plant cover. In hyper-arid environments, planting annual and biennial native pioneer species should facilitate shrub and tree establishment during restoration [82].

Disturbed habitats appear as plant communities mainly dominated by A. leucoclada growing in silty-clayey soils with high Cu concentrations.

The vegetation in these rangelands appears in a pioneer state with a floristic poverty associated with the existence of certain indicator plant species for this type of habitat. This could be related to the soil quality in these habitats, which seems to be deeply affected by the agricultural legacy, suggesting the use of different fertilizers and chemical additives, making these soils rich in various mineral salts where species such as A. leucoclada are frequently found [51].

The presence of these chemical elements in significant amounts altered soil with a very compact clayey-loamy texture. This confirms the history of extensive use of fertilizers in these areas, while the presence of Cu suggests the use of fungicides. This should have consequences on the type of vegetation that will subsequently be established, particularly in terms of time of recolonization and floristic composition, which will be mainly influenced by the edaphic conditions of the hyper-arid environment [29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85]. This is why the restoration of these habitats must take into consideration the current soil quality as well as the overall dynamics of local vegetation. Improving soil properties, as well as planting certain native species, can help to establish and facilitate the natural process of restoring local vegetation.

4.5. Targeted Active Ecological Restoration Interventions to Facilitate the Recovery of Abandoned Cultivated Areas in the Sharaan Nature Reserve

The goal of any restoration strategy is to reproduce the structure and functioning of the ecosystem that existed before the disturbance [83]. This was the main objective of creating the Sharaan Nature Reserve. Ecological restoration is an approach that aims to stimulate natural succession processes to develop stable structural and functional dynamics [84]. Passive restoration strategies involve minimal human intervention and are based on the natural succession process, while active restoration strategies include high-density planting of species and their respective management [85].

Several authors in arid areas, such as Ghazal [70] in Kuwait, have suggested conducting targeted ‘active ecological restoration’ interventions to facilitate the recovery process in environments that have suffered such damage through actions such as planting, especially in the early stages of recovery. In fact, human-driven revegetation could be an interesting strategy to promote native flora recovery, and also prevent the development of exotic invasive species imported by agriculture [86]. Active restoration strategies are often used for the most degraded ecosystems as they are costly and more suitable for this type of habitat than “passive” approaches [87,88].

Following an “active” ecological restoration approach in the study area, the recommendations resulting from our study should constitute an important tool for local managers to improve the facilitation and success rate of operations planned at the level of these areas. The implementation of these recommendations through “active” intervention in disturbed and semi-natural habitats by planting species and improving the chemical properties of the soil should significantly enhance the chances of success of the recovery process of these lands and, consequently, the ecological restoration of the site.

The results obtained from our study have helped to explain the vegetation–species–soil relationship whose causal links are identified. This should lead to the proposition of precise solutions to the disturbed and semi-natural habitats restoration issue in the Sharaan Nature Reserve by precisely determining how and when to intervene within the framework of an active restoration strategy [89] that consists of two main levels of intervention:

• -. Intervention at the vegetation level consists of planting key species such as biennial grasses (P. repens and S. plumosa) at the level of the disturbed habitats as a first step. It has been shown that for the most degraded habitats, planting this type of grass will increase the chances of success of the restoration strategy [82]. In the second step, planting shrub species such as A. graveolens and H. salicornicum should constitute a good active restoration approach aimed at revegetating these degraded areas. For instance, direct sowing of prepared seeds of H. salicornicum could be an effective and easy method for revegetating disturbed and semi-natural habitats in the Sharaan Natural Reserve, as it is a key species for the restoration of natural desert landscapes in the Saudi Arabian region, particularly in the most deteriorated areas [90,91]. It has been proven in tropical forests that similar active restoration methods using native species can accelerate ecosystem functioning by activating the biogeochemical cycle of soil nutrients and carbon sequestration [92].

• -. In semi-natural habitats, the same interventions can be considered, including planting native key species. Many studies in different ecosystems [93,94,95,96,97] have reported the use of the most common native plant species in active restoration approaches instead of less common species whose planting “at late successional stage” could constitute a promising restoration strategy to maximize diversity [95,96,97,98,99].

• -. Intervention at the soil level should mainly be based on the different plantations, i.e., intervention at the vegetation level. This should contribute through the planting of native species to the improvement of soil quality as well as the stabilization of chemical element concentrations [100]. This method is usually used in dry and degraded environments [101,102]. However, other methods, such as active soil-based restoration that specifically targets soil properties, could also be used [103]. Soil-based restoration techniques have been widely used to restore soil properties in degraded drylands [100,101,102,103,104,105].

Such a method should be considered in disturbed habitats in a progressive manner in terms of quantity and time. It would be interesting to proceed to some techniques already tested in dry environments that have given satisfactory results such as biocrust inoculation [106] or organic amendments [107].

These active techniques acting on soil properties aim to improve the poor chemical properties of soils in disturbed habitats to achieve average to good quality, as well as those in semi-natural habitats to achieve optimum quality (Figure 5).

According to Kimmell et al. [108], active soil restoration has been identified as an effective strategy, allowing the improvement of soil quality as well as the restoration of ecosystems.

5. Conclusions

The Sharaan Nature Reserve represents an interesting example of a natural ecosystem that has been subject to severe human disturbance in the past, and whose natural vegetation is still able to recover, particularly since the ban on these activities and the granting of a protection status as a gazetted nature reserve. The reserve is characterized by quite rich perennial flora structuring of a fairly diverse vegetation community in three main types of habitats characterized by different plant communities associated with diverse soil properties and degrees of disturbance. These plant communities reflect a dynamic pattern that suggests that following post-agriculture abandonment, highly degraded plant communities could potentially recover in favor of diverse natural communities. The success of this process would depend on the prevailing local ecological and edaphic conditions. However, the hyper-arid conditions may constitute a challenge by limiting and/or delaying the natural restoration process of the reserve habitats despite the presence of the fence, which constitutes a great advantage, allowing us to consider some restoration approaches.

The targeted active ecological restoration strategy should enable faster recovery of disturbed and semi-natural habitats through intervention actions at the soil and vegetation scale, and therefore constitutes a solution to this management issue in the reserve.

More in-depth work exploring the dynamics of these plant communities over different seasons and in the longer term remains to be considered in order to better understand the soil–vegetation relationships in these dry ecosystems.

Testing different documented restoration techniques and other innovative methods in the reserve regarding the planting of certain plant species in precise dynamic stages, as well as improving soil quality, should constitute an interesting research subject in the future.

Author Contributions

S.Y.: Conceptualization, Methodology, Investigation; M.D.M.: Writing— Original draft preparation, Writing—Review and Editing; S.B.: Data curation, Writing—Review and Editing; R.S.: Investigation; J.N.: Investigation; H.B.: Conceptualization, Resources, Supervision; S.D.A.: Writing—Review and Editing. S.K.R.: Writing—Review and Editing; B.P.Y.-H.L.: Writing—Review and Editing; A.H.M.: Resources, Supervision, Writing—Review and Editing. All authors have read and agreed to the published version of the manuscript.

Data Availability Statement

Data will be made available on request. The data are not publicly available due to privacy reasons.

Acknowledgments

This study was supported by the Royal Commission of AlUla (RCU), Saudi Arabia.

Conflicts of Interest

Authors Sami Youssef, Stéphane Boivin, Robin Sallio, Jérôme Nespoulous and Hassan Boukcim were employed by the company Valorhiz. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The authors declare that this study received funding from VALORHIZ SAS. The funder had the following involvement with the study: the study design, collection, analysis, interpretation of data, the writing of this article.

Footnotes

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Figures and Table

Figure 1. Selected study sites for the three habitats in the Sharaan Nature Reserve (SNR).

Figure 2. Plant community structure related to the three habitats. Vegetation density (a) vegetation diversity (Shannon index) (b) and non-metric dimensional scaling (NMDS) based on the Bray-Curtis dissimilarities between sites (c) for the three different habitats. Letters indicate significant differences between habitats (Kruskall-Wallis test followed by a pairwise post-hoc Dunn test, p value [less than] 0.05).

Figure 3. The five most represented plant species dominating the three habitats. Species with a mean of at least 1 individual was considered as representative of a habitat. Here the log10 of the counts for each representative species is represented for the three different habitats. Letters represent significant changes between species in the three habitats (Kruskall-Wallis statistical test followed by a pairwise post-hoc Dunn test; p [less than] 0.05).

Figure 4. Composition of plant communities related to the soil properties. Plots of the two first axes of the redundant analyses (RDA) of the plant species diversity and the soil physicochemical properties for the three habitats. Black dots represent species. Only the species associated with soil properties were indicated.

Figure 5. Biotics and abiotics targeted active ecological restoration interventions. The colored thin arrows represent active intervention actions.

Table 1

Relative abundance of the nine main chemical elements in the three habitats provided by the XRF measurments. Letters represent significant differences between habitats (Kruskall-Wallis tests followed by posthoc pairwise dunn tests; p value < 0.05).

Element	Habitats	Min	Median	Max	SD
Mg	Natural (n = 68)	0.8973	1.4859 a	1.8829	0.2285
	Semi-natural (n = 12)	1.5399	1.7284 b	2.0664	0.2016
	Disturbed (n = 23)	1.6798	2.0852 c	2.3585	0.1867
Al	Natural	2.2664	6.5202 a	10.3591	1.9456
	Semi-natural	6.2573	8.4983 b	10.8977	1.5356
	Disturbed	6.2183	10.5449 c	11.8795	1.4910
Si	Natural	29.7204	42.6153 a	54.3260	4.6719
	Semi-natural	31.4926	38.5654 b	45.2652	3.9230
	Disturbed	26.58581	34.1651 c	43.5530	3.6081
P	Natural	0.0325	0.0620 a	0.1377	0.01896
	Semi-natural	0.0726	0.0813 b	0.1018	0.0093
	Disturbed	0.0699	0.0940 b	0.1145	0.0114
S	Natural	0.0063	0.0063 a	0.0198	0.0026
	Semi-natural	0.0063	0.0063 a	0.0063	0.0000
	Disturbed	0.0063	0.0063 a	0.0063	0.0000
K	Natural	0.0845	0.4796 a	1.0386	0.2162
	Semi-natural	0.5379	0.6466 b	1.0886	0.2268
	Disturbed	0.4833	1.0712 c	1.2166	0.1890
Ca	Natural	0.2510	1.3692 a	3.0900	0.6804
	Semi-natural	1.3242	1.9230 b	3.7612	0.8842
	Disturbed	1.6285	3.2759 c	4.1316	0.6284
Fe	Natural	0.4058	1.3536 a	3.9808	0.7199
	Semi-natural	1.4212	1.8451 b	4.2142	1.0836
	Disturbed	1.525	4.2229 c	4.6544	0.9351
Cu	Natural	0.0007	0.0010 a	0.0026	0.0003
	Semi-natural	0.0011	0.0013 b	0.0028	0.0006
	Disturbed	0.0011	0.0027 c	0.0032	0.0005

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/land13122033/s1, Figure S1: Contribution of botanical families in the inventory; Figure S2: Soil physicochemical properties in the three habitats. Principal component analysis (PCA) of the 103 soil samples using the physicochemical dataset (Table S2) (a) Boxplot representing nine of the physicochemical measurments which structure the dataset (b). As the granulometry data are composional (relative abundance), a center-log ratio tranformation (clr) was applied. Statistical analyses were performed using Kruskal-Wallis tests followed by a posthoc Dunn test (p < 0.05); Figure S3: Relative abundance of the soil atomic elements in the three habitats. Principal component analysis (PCA) of the 103 soil samples using the X-ray fluorescence dataset (relative abundance from the magnesium to uranium) (a) Boxplot representing the center-log ratio (clr) of the relative abundance for the nine main elements of the analysis (b). Statistical analyses was performed using Kruskal-Wallis tests followed by a posthoc Dunn test (p < 0.05); Figure S4: Fraction of variance explaining the plant communities. The corresponding fractions of variance explained by the RDA for each of the soil physicochemical properties. Random independent permutation test and Holm correction (p < 0.05); Table S1: List of plant species for floristic analyses; Table S2: Location, habitats and vegetation survey of the 103 study sites (counting table); Table S3: Relative abundance of the atomic elements in the 103 selected soil samples.

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