*Article* **Vegetation Composition of the Halophytic Grass** *Aeluropus lagopoides* **Communities within Coastal and Inland Sabkhas of Saudi Arabia**

**Basharat A. Dar 1, Abdulaziz M. Assaeed 1, Saud L. Al-Rowaily 1, Abdullah A. Al-Doss <sup>1</sup> and Ahmed M. Abd-ElGawad 1,2,\***


**Abstract:** Sabkhas are unique, highly saline ecosystems, where specially adapted plants can grow. *Aeluropus lagopoides* (L.) Thwaites is a halophytic forage plant growing in salt marsh habitats of inland and coastal sabkhas of Saudi Arabia. The present study provides an analysis of vegetation composition and distribution of the *A. lagopoides* community in five different regions within Saudi Arabia, emphasizing the environmental factors that affect species distribution. The floristic survey revealed the presence of 48 species, belonging to 26 families. Poaceae, Chenopodiaceae, Mimosaceae, Zygophyllaceae, and Asteraceae are the largest families (50% of total species). Phanerophyte, followed by chamaephytes, are the most frequent forms, indicating a typical saline desert life-form spectrum. The vegetation analysis revealed the dominance of *A. lagopoides* in all locations, where it was the most dominant species in Qareenah, Qaseem, and Salwa locations, and the second most dominant species in Jouf and Jizan locations. The flourishment of this halophytic grass within a wide soil range in sabkhas revealed its adaptability to the harsh environment, which could be ascribed to its structural adaptations and modifications, as well as the phenotypic plasticity. The Qareenah and Qaseem locations attained the highest species richness and evenness, while the Jizan location was the least diverse. Within the studied locations, other highly salt-tolerant species were determined with high abundances, such as *Suaeda aegyptiaca* (Hasselq.) Zohary, *Zygophyllum album* L.f., *Tamarix nilotica* (Ehrenb.) Bunge, *Cressa cretica* L., and *Salicornia europaea* L. The soil analysis showed a significant variation for all parameters among the studied locations, except for pH, chloride, and clay content. The Qaseem location revealed the highest values of most soil parameters, while the Jizan location showed the lowest. The canonical correspondence analysis (CCA) showed that the community structure and diversity are mainly affected by the soil salinity and moisture. Due to the economic potentialities of *A. lagopoides* as a forage plant and sand stabilizer, the conservation of its habitats is of vital importance. In addition, this grass could be integrated as a promising forage candidate that can be planted in saline-affected areas, even in the summer dry season.

**Keywords:** phenotypic plasticity; mangrove grass; salt marshes; coastal habitat; biodiversity

#### **1. Introduction**

Sabkhas are geological phenomena formed in an arid or semi-arid climate, as broad plains or salt flats, containing evaporates dictated by the local water table [1]. Geographically, it has a large habitat range, distributed worldwide through Southeast Europe, the siliciclastic coast of California, Mexico, North Africa from Morocco to Somalia, the Middle East and the Arabian Peninsula, Australia, and Asia [2–4]. Sabkhas are grouped into two major landform types [5], low-lying coastal salt marshes [6,7] or inland interdune areas as

**Citation:** Dar, B.A.; Assaeed, A.M.; Al-Rowaily, S.L.; Al-Doss, A.A.; Abd-ElGawad, A.M. Vegetation Composition of the Halophytic Grass *Aeluropus lagopoides* Communities within Coastal and Inland Sabkhas of Saudi Arabia. *Plants* **2022**, *11*, 666. https://doi.org/10.3390/ plants11050666

Academic Editors: Robert Philipp Wagensommer and Panayiotis Dimitrakopoulos

Received: 9 January 2022 Accepted: 24 February 2022 Published: 28 February 2022

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**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

salt-crusted depressions [8]. Nearly all key species in these saline habitats are perennial halophytes forming different plant communities [4,9].

The Arabian Peninsula is also characterized by high salinity, high annual temperature variations, and shallow waters. Saudi Arabia possesses harsh natural desert environments without rivers or lakes. It is distinguished by various ecosystems, including mountains, wadis, meadows, rocky mountains, sandy deserts, and saltpans with distinct plant communities [10,11]. The salt-affected areas of Saudi Arabia are classified into the coastal plain, inland zone, and littoral salt marshes [12]. Coastal and inland saline habitats, called sabkhas, are highly stressful environments, as they are highly saline and wet unique ecosystems, where specially adapted halophytic plants can grow [13]. These sabkhas are mostly saturated with brine, and the soil surface is often encrusted with thick salt crust [14]. Natural saline habitats vary in salinity levels due to differences in topography, soil properties, and micro-climate, both spatially and temporally [15]. Vegetation composition in these ecosystems is influenced by complex heterogonous environmental factors, including duration and degree of inundation by seawater and both overground and underground freshwater input [16], coastal and inland geomorphology, microtopography, soil moisture content, and soil type [17].

Specific plant species can dominate sabkha habitats, forming monospecific stands. The vegetation of these monospecific stands forms zones with distinct plant communities [18], forming a variety of specialized habitats of distinct vegetation mosaics [19]. Most of the key species in the saline habitats are perennial halophytes, which constitute about 2% of the world's flora [18,20], predominantly belonging to the families Chenopodiaceae, Zygophyllaceae, Plumbaginaceae, Poaceae, and Juncaceae [21]. The distribution of some halophytic species is best correlated along a gradient of soil variables, such as salinity, moisture content, soil texture, organic matter, and calcium carbonate [22].

Among the Poaceae family, *Aeluropus lagopoides* (L.) Thwaites is one important key species of saline habitats of Saudi Arabia [23]. Geographically, it has a wide habitat range, distributed through Southeast Europe, North Africa, the Middle East, Arabian Peninsula, and Central Asia [3]. In Saudi Arabia, *A. lagopoides* grows in various coastal and inland sabkhas [23,24]. It is restricted in the form of specialized vegetation patches in the Wadi Hargan, Riyadh, salt marsh sabkha of the Qaseem and Jouf, and coastal zones of the Salwa and Jizan regions [25,26]. It is of economic importance, where it is utilized as fodder in arid areas, used to stabilize sand dunes [27], and can be used for landscaping of the urban areas [28].

Knowledge of the ecological distribution of key species is the primary characteristic of its conservation strategy in its ecosystem [29]. Apart from the establishment and maintenance of the protected area, baseline information about the key species, vis a vis the associated species, edaphic factors of the habitats, environmental variation, anthropogenic activities of the regions, are crucial [25,30]. This ecogeographical survey is considered central to all the conservation issues and a key requisite in the development of the conservation strategy [31,32]. According to our field observations, *A. lagopoides* has various phenotypic characteristics and forms distinct vegetative patches within various regions of Saudi Arabia. To the best of our knowledge, no study has dealt with the vegetation composition of the key forage halophyte *A. lagopoides* in Saudi Arabia. Therefore, the present study aims to assess the vegetation structure of *A. lagopoides* communities in the various regions/habitats around Saudi Arabia, considering regional heterogeneity, edaphic factors, and variation of climatic gradients. This study will help in understanding the distribution of this important forage plant that flourished in one of Earth's harsh environments and, in consequence, shows the potential of conserving this plant, as well as integrating it in a foraging system.

#### **2. Results**

#### *2.1. Floristic Composition of the Studied Regions*

As expected, the plant diversity of the studied sabkha regions is low, in which the species had to withstand harsh environmental conditions, i.e., the high salinity content (Table S1). The floristic analysis revealed the presence of 48 species of vascular plants, which are mainly perennials (75%). The highest number of species (24 species: 22 perennials and 2 annual) were recorded in the inland Sabkha of Qareenah, Riyadh region, which is represented by about 34% of the total recorded species, while the sabkha of the northern Al-Jouf region recorded the lowest number of species (all eight perennial species) which is about 10% of the total recorded species (Figure S1). However, the species' evenness was highest in the inland sabkhas of the Qaseem region, representing about 42% of the recorded species, and the lowest was in the coastal sabkha of Jizan, representing about 9% (Figure S1). Summing up, the coastal sabkhas (Salwa and Jizan) recorded the highest number of species (43 species: 36 perennials and 6 annuals), which is represented by 60% of total recorded species, compared to the inland sabkhas (Qareenah, Qassem, and Jouf) that represented 40% of the total recorded species (29 species: 21 perennials and 8 annuals).

The identified plant species belonged to 26 families, where Poaceae, Chenopodiaceae, Mimosaceae, Zygophyllaceae, and Asteraceae were the major families that represented 50% of the total species (Figure 1A and Table S1).

**Figure 1.** Floristic composition of the surveyed region. (**A**) Represented families, (**B**) life forms, and (**C**) chorotype spectra. SA-AR: Saharo-Arabian, SU: Sudian, AF: African, ME: Mediterranean, IR-TU: Irano-Turanian, EU-SI: Euro-Siberian, PL-T: Plurireginalbor-trop, SU-ZA: Sudano-Zambezian, SUB-T: Subtropical-Tropical, SA-South-American, NT-Neotropical, AM-American.

On the one hand, The recorded plant species were classified into six life forms, according to Raunkiaer's system, of which 29% were phanerophytes and 27% chamaephytes, while hemicryptophytes, geophytes, and helophytes were represented by 19%, 17%, and 2%, respectively (Figure 1B). On the other hand, the chorological analysis of the identified

species revealed that 62.50% of those species were monoregional, and the Saharo-Arabian element was the most present chorotype (27.08%) (Figure 1C). However, 22.92% of the identified species were classified as biregional plants, whereas Sudanian-African was the most represented element (6.25%). The pluriregional chorotype was also represented, with 14.58% of the total recorded species, and the most represented ones were the Euro-Siberian-Mediterranean-Irano-Turanian and Saharo-Arabian-Mediterranean-Irano-Turanian, which represented 4.17% each.

#### *2.2. Vegetation Analysis of the Studied Regions*

The analysis of importance values of each species, based on the relative cover and density, led to the recognition of the dominant and important species within each location (Table 1). The details of all species are presented in Table S2. The Qareenah region was the most diversified, with 24 species. This group attained the highest richness (Simpson diversity index = 0.95). In this location, *A. lagopoides* was the first dominant species (importance value = 44.41), while *Zygophyllum coccineum* L. was the second most dominant (importance value = 25.64). The other important species recorded were *Juncus rigidus* Desf., *Tamarix nilotica* (Ehrenb.) Bunge, *Rhazya stricta* Decne., *Acacia gerrardii* Benth., and *Phragmites australis* (Cav.) Trin. ex Steud. (Table 1).

**Table 1.** Plant species richness, evenness, and dominance of the studied sabkha locations of Saudi Arabia.


\* represents the importance value based on the relative plant density and cover.

The location of Qaseem is dominated by *A. lagopoides* (importance value = 94.20). In this location, *Suaeda aegyptiaca* was determined as the second most dominant species (importance value = 28.61). The other important species that attained high importance values were *Cressa cretica* L., *J. rigidus*, *Lycium shawii* Roem. and Schult., and *Salicornia europaea* L. This location attained a Simpson diversity index of 1.6 and Shannon evenness of 0.74. On the other hand, the Salwa location showed the lowest Simpson diversity index (1.04), and it was dominated by *A. lagopoides* (importance value = 66.62), followed by *Zygophyllum album* L.f. (importance value = 41.05). The other important species within this

location were *P. australis*, *J. rigidus*, *S. aegyptiaca* (Hasselq.) Zohary, and *Phoenix dactylifera* L. (Table 1).

The Jouf location was the least diversified (eight species) among the recognized groups, and it is dominated by *T. nilotica* as the most dominant and *A. lagopoides* as second most dominant species. This group attained a Simpson diversity index of 1.53 and Shannon evenness of 0.75. The other important species recorded in this group were *Z. album*, *C. cretica*, and *S. aegyptiaca* (Table 1). Lastly, the Jizan location comprised 15 recorded species. This community attained a Simpson diversity index of 1.81 and Shannon evenness of 0.75. The most dominant in this location was *S. aegyptiaca* (importance value = 80.76), while *A. lagopoides* was the second most dominant species. The other important species of this group were *Panicum repens*, *Cyperus conglomeratus* Rottb., *Aerva javanica* (Burm.f.) Juss. ex Schult., and *Zygophyllum simplex* L. (Table 1). *A. lagopoides* dominated in all studied locations, either as most dominant, as in the inland sabkhas of Qareenah, Qaseem regions, and Coastal sabkhas of Salwa, or second most dominant species, in the inland sabkhas of Jouf and coastal sabkha of the Jizan region (Table 1).

The application of detrended correspondence analysis (DCA) on the vegetation data showed the separation of the Jizan location, on the right side of the DCA diagram (Figure 2). However, the other location showed quite significant overlapping, with a close correlation between the Qassem and Salwa locations.

**Figure 2.** Detrended correspondence analysis (DCA) ordination of the studied locations () based on the importance value of dominant, co-dominant, and important species (•) recorded from each location. Ael lag: *Aeluropus lagopoides,* Tam nil: *Tamarix nilotica*, Jun rig: *Juncus rigidus*, Lyc sha: *Lycium shawii*, Pho dac: *Phoenix dactlifera*, Phr aus: *Phragmites australis*, Sal eur: *Salicornia europaea*, Sua aeg: *Suaeda aegyptiaca*, Zyg alb: *Zygophyllum album*, Cre cre: *Cressa cretica*, Cyp con: *Cyperus conglomeratus*, Zyg sim: *Zygophyllum simplex*, Aer jav: *Aerva javanica*, Pan rep: *Panicum repens*, Sau mon: *Suaeda monoica,* Rha str: *Rhazya stricta*.

Moreover, the cluster analysis of the vegetation data of all recorded species confirmed the data of DCA, where it revealed that the Jizan location is different than other locations (Figure 3). Salwa and Qaseem locations showed similar vegetation composition, while Jouf and Qareenah were different in the vegetation structure.

**Figure 3.** Hierarchical clustering of different studied locations based on the importance values of the recorded plant species (n = 48).

#### *2.3. Vegetation-Soil Relationship*

The soil analysis of the five studied locations showed significant variations regarding all measured parameters, except for pH, Cl−, and clay (Table 2). The Qaseem location attained the highest moisture, clay, silt, salinity, Ca, Mg, Na, K, Cl, SO4, HCO3, and organic matter (Table 2). The Salwa location is characterized by high sand content, while the soil of the Qareenah location revealed the highest content of calcium carbonate. The Jizan location had the lowest moisture content, pH, organic matter, K, sulphate, bicarbonate, and calcium carbonate, while the Jouf location attained the lowest salinity content.

**Table 2.** Soil chemical and physical properties of the studied locations dominated by *Aeluropus lagopoides* community.

