Halophyte-Fodder Species Association May Improve Nutrient Availability and Biomass Production of the Sabkha Ecosystem

Abstract

Sabkhas are often regarded as marginal non productive areas. Yet, a wide range of halophytes together with less salt-tolerant fodder species thrive in these ecosystems. In the present study, the potential of halophytes in improving biomass production and nutrient uptake ofan un-grazed parcel edging an inland sabkha (100 km south-east of Tunis) was addressed. The vegetation of studied area was characterised by perennial halophytes tufts in association with fodder annuals, mainly Medicago species. Halophytes grew slowly and accumulated low contents of mineral nutrients (N, Pi, K⁺) and high Na⁺ concentrations in their shoots. Depending on the precipitation, the annual fodder species showed high growth activity (up to 40% of the plant annual biomass production of the ecosystem), which was sustained by a high capacity of nutrient uptake (up to 70% of the total nutrient uptake). The annuals were almost exclusively clustered under the halophyte tufts, or at their immediate vicinity, where soil N and Pi levels were significantly higher, and salinity significantly lower than between the tufts. The perennial halophytes provided optimal conditions for the growth of these annual Leguminosae, which valorised the nutrients accumulated around the halophytes, owing to their high growth rate, nutrient-absorption rate and use-efficiency. These data are of high ecological significance and suggest that the salt tolerant-fodder species association may constitute a low-cost and valuable approach for the restoration and reclamation of the marginal saline ecosystems.

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1 Introduction

Frequently associated with drought, salinity leads to considerable loss of fertile soils and threatens the world nutritional balance (Malcolm et al. 2003; Reynolds et al. 2005). About 1.5 billion ha of soils suffer excessive salt level throughout the world (Choukr-Allah 1996). Annually 10 million ha of arable lands are abandoned because of salt accumulation following the utilisation of saline irrigation water for agriculture. In Tunisia, 1.5 million ha (10% of the whole territory and 18% of its arable land) are affected by salt. Besides impacting plant water status, increasing salinity enhances plant nutrient requirements and may restrict the uptake of essential nutrients such as K⁺, Ca²⁺, and Mg²⁺ (Hu and Schmidhalter 2005), resulting in salt-induced nutrient stress. Such resource limitations control ultimately plant community properties (e.g. structure and species distribution), as well as ecosystem functions (i.e. productivity and nutrient cycling) (James et al. 2005).

Unlike conventional crops, halophyte plants are able to survive and to reproduce in environments (coasts, wetlands, inland deserts) where salt concentration reaches or even exceeds seawater salinity level. These species, which represent about 1% of the world’s flora, have evolved complex mechanisms at different levels (whole plant, cellular, and molecular) enabling them to successfully cope with these hostile conditions. Restoration of saline areas using salt-tolerant vegetation is progressively emerging as a sustainable and low-cost approach (Aschenbach 2006; Ravindran et al. 2007; Sargeant et al. 2008; Khan et al. 2009). Concomitantly, better understanding of plant ecosystems and their dynamics that are capable of significant productivity under salt stress is of paramount importance. For instance, the analysis of plant association in their natural environments may provide key information about their intrinsic potentialities and the likely ways of their utilisation in order to restore marginal salt-affected areas.

Coastal or continental sabkhas are saline ecosystems frequently or occasionally subjected to flooding, which are typical of the semi-arid and arid areas around the world. Because of the extreme environmental (edaphic and climatic) conditions prevailing there, these biotopes are considered as non productive wastelands (Böer and Gliddon 1998). However, vegetation in sabkhas is diverse and heterogeneous, consisting in numerous perennial halophytic plants in association with annual species, more or less sensitive to salt and mineral deficiency stresses. In Tunisia for instance, the annual fodder plant Hordeum maritima (Poaceae) is common in the saline depressions in close association with strict halophytes, such as Arthrocnemum indicum and Halocnemum strobilaceum (Hafsi et al. 2007). Sabkhas could be valorised by implementing agro-ecosystems using “alternative” cash-crop halophytes (Böer and Gliddon 1998; Keiffer and Ungar 2002). Indeed, among the 2600 recognised halophytic species, some present economic (human food, fodder, materials of high economic values) or ecological (soil desalinisation, dune fixation, phytoremediation, landscaping and ornament) potentials (Abdelly et al. 2006; Ghars et al. 2006; Weber et al. 2007).

Despite sabkhas are common in Tunisia these unique biotopes remain poorly investigated with respect to their spatial and temporal dynamics, vegetation structure, nutrient relations, and their agro-economical potentialities. In the framework of the sustainable saline ecosystem valorisation, the present study investigates the role of halophytes on soil physico-chemical characteristics and nutrient relations, enabling enhanced primary production of fodder species. The chosen area borders a sabkha located in a semi-arid region of Tunisia (mean annual rainfall ranging from 250 to 700 mm). The flora of this site is composed of strict halophytes (Arthrocnemum indicum, Halocnemum strobilaceum, Salsola cruciata, Suaeda fruticosa) and of glycophytes (mainly Medicago species).

2 Material and Methods

2.1 Experimental Site and Sampling Periods

An experimental parcel covering about 1,000 m² was delimited and protected from livestock grazing, at the border of the sabkha of Enfidha (100 km south-east from Tunis), situated in the semi-arid bioclimatic zone (moderate winters and mean annual rainfall rarely above 300 mm). Biomass production of the plant cover (perennial halophytes and annual glycophytes) was assessed three times annually during two successive years. The first year was characterised by irregular and scarce rainfall (235 mm), and the second one was relatively rainy (423 mm). The first sampling took place shortly after of the establishment of the annuals, the second at their flowering stage (generally corresponding to the period of halophyte maximum growth activity), and the third one following ripening of the annuals. At the final sampling, biomass may have been underestimated since most of the desiccated organs were lost.

2.2 Plant Sampling Method

Perennial plants. A non-destructive, indirect sampling method was used to evaluate the contribution of each species to total biomass production. In the protected study area (Fig. 1) observations were made in a representative (with respect to the plant cover) homogeneous 5 m × 5 m plot. Within this experimental area, the halophytes were thriving in isolated tufts of different sizes. At each sampling, diameter and height of the perennial tufts inside the observation plot were measured. For each species, size classes were defined, and their populations were counted. Then, tufts with sizes representative for each class, outside the reference square, were sampled (green twigs and dry twigs separately), and fresh weight (FW), dry weight (DW) after drying for 3 days at 80°C, and mineral content determined. For each species j, with size classes i = 1, 2, …, k, each containing n_i,j plants of mass m _i,j , dry weight was calculated as:

Fig. 1

Schematic representation of the studied parcel. T₁, T₂ and T₃ indicate the harvesting sites of tufts 1, 2, and 3 respectively. Numbers 1–4 represent the different vegetation zones from the periphery to the centre of the sabkha of Enfidha. 1: Most external zone, containing mainly fodder shrubs (Acacia cyanophylla and Medicago arborea), Poaceae and other annual glycophytes. 2: Transitional zone, between abundant and poor flora areas, characterised by Atriplex halimus and Suaeda fruticosa tufts, and other species typical of more saline (Hordeum maritimum and Triglochin bulbosa) or less saline (Trifolium tomentosum and Limoniastrum guyonianum) hydromorphic soils. 3: The third zone, colonised mainly by perennial halophytes, indicating temporarily inundated saline soils. The sssociation Salsola tetrandra-Suaeda fruticosa was frequent, in addition to Arthrocnemum indicum and Phragmites cummunis. 4: The fourth zone, characterised by the prominence of two species indicating high hydromorphy and salinity : Halocnemum strobilaceum and Arthrocnemum indicum. 5: Location of the studied parcel, delimited at the border of zones 2 and 3

$$ i = k $$

$$ {\text{D}}{{\text{W}}_j} = \sum {{\text{n}}_{_{i,j}}}{{\text{m}}_{_{_{i,j}}}} $$

$$ i = {\mathbf{1}} $$

Annual plants. Six 0.5 m × 1 m plots were selected inside the protected parcel, representative for the distribution of the annual species within the experimental area. Sampled shoots from each small area were partitioned into Leguminosae and Poaceae, and their respective FW and DW determined.

2.3 Soil Sampling Method

Three Arthrocnemum indicum tufts growing in association with annuals were selected. Tuft 1 was close to the sabkha periphery, whereas tufts 2 and 3 were close to its centre (Fig. 1). Soil samples (n = 4) were taken at the centre of each tuft, and along two orthogonal axes at 0.5, 1 and 2 m from the centre. At each position, five 20-cm wide soil horizons (from 0 to 1 m depth) were sampled.

2.4 Mineral Elements

Plants. Plant samples were finely grounded. Na⁺, K⁺ and inorganic phosphate (Pi) were extracted in 0.5% HCl and assayed by flame emission photometry and colorimetry respectively (Fleury and Leclerc 1943). For Pi, the extracts were first treated with organic carbon. Reduced nitrogen was determined by the Kjeldahl Ũmethod.

Soil. Assimilable phosphorous was extracted and estimated using the fine soil fraction according to the method described by Bonneau and Souchier (1979). Electrical conductivity (EC) was measured and soluble cations (Na⁺ and K⁺) were determined by flame emission photometry (Corning, UK) in aqueous extracts (soil/water: 1/10 w/w).

2.5 Statistical Analysis

A one way analysis of variance (ANOVA) at the P < 0.05 significance level was performed using the SPSS programme.

3 Results

3.1 Vegetation Inventory

Four vegetation zones were distinguished from the periphery to the centre of the sabkha (Fig. 1). The outer zone, which was partially cultivated, contained barley and fodder shrubs (Acacia cyanophylla and Medicago arborea), in addition to a mixture of naturally-growing vegetation, mainly comprising Poaceae (Lolium regidum, Lagurus ovatus, Aeluropus littoralis, Cynodon dactylon), Leguminosae (Medicago ciliaris, Medicago truncatulata, Medicago polymorpha, Medicago hispida, Medicago minima, Astragalus hamosus, Trifolium tomentosum, Scorpirus muricatus), and Compositeae (Calendula arvensis, Anacyclus clavatus, Pteranthus dichotomus, Pallenis spinosa, Scolymus hispanicus). The majority of these species is known to be salt-sensitive. However, Aeluropus littoralis is an indicator of moderately hydromorphic zones with variable EC (from 10 to 60 dS m⁻¹).

The second zone represents a transitional zone species-rich to species-poor areas. It was characterised by tufts of Chenopodiaceae, mostly Atriplex halimus and Suaeda fruticosa, tolerating a wide range in salinity (EC between 10 and 70 dS m⁻¹). Species typical of more saline (Hordeum maritima and Triglochin bulbosa) or less saline (Trifolium tomentosum and Limoniastrum guyonianum) hydromorphic soils, were also growing in this area. Indicator species of low EC soils (less than 25 dS m⁻¹: Medicago ciliaris and Trifolium scabrum) were also found.

The third zone (EC ranging between 10 and 70 dS m⁻¹) was mainly characterised by perennial halophytes, especially the association Salsola tetrandra-Suaeda fruticosa, also characteristic of low to moderate hydromorphic soils. Other species like Arthrocnemum indicum indicated temporarily flooded saline soils (EC up to 80 dS m⁻¹) or pronounced hydromorphy (Phragmites cummunis) or high salinity (Halocnemum strobilaceum). Four Medicago species, as well as Trigonella maritima and Trifolium tomentosum were also found.

Vegetation in the fourth zone distinguished by prominence of two species indicating strong hydromorphy and salinity: Halocnemum strobilaceum and Arthrocnemum indicum. The tufts of H. strobilaceum formed a suitable micro-habitat for Spergularia salina and Trifolium tomentosum.

Thus, the variations in species composition among the four zones indicated increasing salinity and hydromorphy gradients from the outer boundary towards the centre of the sabkha. Interestingly, the annual and perennial species were spatially associated, annuals thriving at the vicinity of the halophyte tufts, while almost no vegetation was found between these tufts.

3.2 Soil Salinity

Soil salinity (as EC, dS m⁻¹) in the centre of the tufts showed non-significant (at P < 0.05) spatial variation (0.55–0.88 dS m⁻¹) within the sabkha (Fig. 2a). These values correspond to a salinity ranging between 55 and 88 meq kg⁻¹ dry soils, i.e. a relatively low salt level. EC generally increased with distance from the tufts, exceeding 1 dS m⁻¹, and even 2 dS m⁻¹ (200 meq kg⁻¹ dry soil), at 2 m from the tuft centre, i.e. characteristic for a highly saline soil.

Fig. 2

Variation in soil (0–20 cm depth horizon) salinity with distance from the perennial halophytes. (a) EC of aqueous extracts (1 g de soil for 10 ml H₂O). (b) soluble sodium. Tuft 1 situated at the sabkha periphery, tufts 2 and 3 near its centre. Means of 4 replicates ± S.E. at *P < 0.05

EC was significantly higher (at P < 0.05) for tufts 2 and 3 (located inside the sabkha) than in tuft 1, closer to its periphery. This is consistent with the increasing salinity gradient from the periphery to the sabkha centre derived from vegetation analyzes. A horizontal salinity micro-gradient was thus observed from the centre towards the exterior of the halophyte tufts. Na⁺ concentration varied in parallel with the EC (Fig. 2b), along both large scale gradients and micro-gradients, indicating its large contribution to the total soil salinity.

3.3 Soil Fertility

Potassium concentration in the soil (2–4 mmol kg⁻¹ dry soil) did not vary systematically across the sabkha, nor with distance from the tufts (Fig. 3a). Exchangeable potassium concentration decreased from the periphery towards the sabkha centre (Fig. 3a) and with distance from the halophytes, though non significant. This gradient could be ascribed to substitution of K⁺ by Na⁺ in clay, which was abundant outside the tufts. Total soil nitrogen ranged from 1 to 2.5 mg N g⁻¹ soil, equivalent to 71–178 mmol N kg⁻¹ dry soil (Fig. 4a). Generally, significantly (at P < 0.05) larger amounts were found in tuft 1, i.e. higher nitrogen availability at the sabkha outer boundary. Moreover, total nitrogen decreased with distance from the tuft centre. These gradients, more or less pronounced according to the tuft size, reveal the importance of the litter for the soil nitrogen balance. Phosphorus concentration was variable among tufts (Fig. 4b). The upper soil horizon at the centre of tufts 2 and 3 contained more assimilable phosphorus than that farther from the tuft, suggesting that its availability was increased by soil enrichment with organic matter.

Fig. 3

Variation in soil (0–20 cm depth horizon) potassium content with distance from Arthrocnemum indicum tufts (a) soluble K⁺. (b) exchangeable K⁺. Tuft 1 situated at the sabkha periphery, tufts 2 and 3 near its centre. Means of 4 replicates ± S.E. at *P < 0.05

Fig. 4

Variations in soil N and P with distance from Arthrocnemum indicum tufts. (a) total N. (b) assimilable P. The samples were extracted from 0–20 cm deep horizon. Tuft 1 was situated at the sabkha periphery, tufts 2 and 3 were near its centre. Means of 4 replicates ± S.E. at *P < 0.05

3.4 Ecosystem Productivity

Biomass production. Two plant groups contributed to ecosystem biomass production: the perennial halophytes (Arthrocnemum indicum, Salsola cruciata and Suaeda fruticosa) and the annuals, mainly the Leguminosae (Medicago sp.), the Poaceae (Hordeum sp.) and the Compositeae. Maximal biomass production of the whole ecosystem was about 50% higher in the rainy year than in the dry year, especially in samplings 5 and 6 (Fig. 5a).

Fig. 5

Biomass production in the sabkha. (a) shoot dry weight (DW) per surface area unit as a function of the sampling dates. Annuals: essentially Leguminosae; perennials: halophytes. Samplings 1, 2 and 3: during the dry year, respectively in April, June and September. Samplings 4, 5 and 6: during the rainy year, respectively in January, March and June. (b) Primary production (DW) per surface area unit of the different plant types. For the halophytes, the annual production is estimated by the difference between the biomasses at the beginning (January) and the end (June) of the growing period. For the annuals, it corresponds to the spring harvests. Means of 4 replicates ± S.E. at *P < 0.05

The perennial halophytes consisted of dry as well as green twigs throughout the year. The green organ contribution to the total biomass production was predominant only during the spring, reaching 50–65% in Arthrocnemum indicum, Salsola cruciata and Suaeda fruticosa. In the remainder of the year, desiccated twigs part could make up 75% of the biomass (data not shown). While the primary production of Arthrocnemum indicum and Salsola cruciata was strongly improved by the rainfall (+23% and +45%, respectively), no impact was observed for Suaeda fruticosa (Fig. 5b). The rainfall effect was more pronounced for the annuals, especially the Leguminosae, which produced six times as much in the wet year. The proportion of these species to total ecosystem (perennials and annuals) biomass production increased from 15% in the dry year to 40% in the rainy year, of which the Leguminosae (mainly Medicago ciliaris, Medicago polymorpha, Medicago truncatula, and Medicago minima) contributed up to 80%.

3.5 Nutrient Uptake

K⁺ concentrations ranged between 0.3 and 0.8 mmol · g⁻¹ DW in perennial halophyte shoots, being generally higher in the dry year (Fig. 6). Potassium concentration in the green twigs of halophytes was three times that in the desiccated twigs, suggesting a remobilisation or leaching from the former. In annuals, K⁺ concentrations ranged from 0.4 to 1 mmol g⁻¹ DW, and were higher in the rainy year. Halophyte green twigs contained more nitrogen than the desiccated ones (Fig. 6). The highest N concentrations in Suaeda fruticosa (up to 3 mmol g⁻¹ DW) were always lower than those in the annuals, especially in the Leguminosae. For the latter, the fluctuations in N concentration were large (a factor two over the two years), depending on rainfall. For phosphorus, Pi concentrations in shoots of all species were relatively low (30–200 μmol g⁻¹ DW). In halophytes, and in contrast to K⁺ and N, Pi was uniformly distributed between the green and the desiccated twigs (data not shown). Pi concentrations of the annuals, particularly the Leguminosae, were four times higher in the rainy year than in the dry year. In spring, when the annuals attained maximal development, the Leguminosae (mainly including the four Medicago species), representing ca. 32% of the total biomass, contained 45% of the total nitrogen and 48% of the potassium (Fig. 6). Thus, the Medicago species were more efficient than the other species in the uptake of nutrient resources.

Fig. 6

Contribution of the plant groups to the biomass production and to N and K⁺ uptake in the sabkha. Data from the spring harvest during the rainy year, corresponding to the maximal development of the annuals. Each sector area is proportional to concentrations in shoots, per soil surface area unit

3.6 Na⁺ Accumulation

Most of the sodium transported to the plant cover was found in the halophytes. Na⁺ strongly accumulated in the halophyte green twigs (up to 3 mmol g⁻¹ DW) (Fig. 7), where it likely contributed to their osmotic adjustment. The tissue Na⁺ concentration ranged from 0.5 to 1.5 M, while Na⁺ concentrations in the desiccated organs represented only 20% of those accumulated in the green ones. Leguminosae and Poaceae tissues contained much lower (at P < 0.05) Na⁺ levels (0.2–0.3 mmol g⁻¹ DW), suggesting that (i) these plants may be provided with mechanisms for protection against sodium invasion, and that (ii) they exploited the low-salt levels superficial zones, while the halophytes owing to deeper roots, exploit more saline soil horizons.

Fig. 7

Sodium contents of the shoots of different species growing in the sabkha. Harvests 4, 5 and 6 were made in January, March and June of the rainy year, respectively. Means of 6 replicates ± S.E. at *P < 0.05

4 Discussion

As reported by Turner (2004), the natural ecosystems of the Mediterranean-climate areas are usually characterised by a mixture of perennial shrubs and trees (mainly xerophytes and halophytes) and annual crops or fodder plants. Growth activity of the annual is governed by the rainfall regime, the rainy season extending from autumn to spring, while the perennials grow slowly, but are able to cope with water shortage and soil/water salinity. Variations in biomass and productivity among and within natural ecosystems may be attributed mostly to differences in water and nutrient (especially N) availability and salinity (Sherman et al. 2003). In the arid to semi-arid regions bordering the Mediterranean Sea, water quality is a major factor limiting crop production (Cantero-Martínez et al. 2007).

In the present study, both soil analyses and vegetation distribution indicated increasing salinity from the periphery to centre of the sabkha. Vegetation cover was more abundant in the peripheral zones, containing the less salt-tolerant perennial halophytes and the annuals. Plant diversity, lower in the depression centre, was dominated by two highly salt-tolerant halophytes: Arthrocnemum indicum and Halocnemum strobilaceum. Similar heterogeneous distribution of salinity has been reported in other studies (Loveland and Ungar 1983; Bekki 1995), and has been ascribed to salt transport by rainwater towards the basin centre. Our data showed an inverse fertility gradient (notably of nitrogen), decreasing from the periphery to the sabkha centre. The low nitrogen availability in the depression centre could be due to the depressive effect of salinity on soil organic matter accumulation (subsequent to the low plant biomass production) and on microbial activity (Rosenberg et al. 1986; Mc Clung and Frankenberger 1987).

We found that the spontaneous Medicago spp., characterised by high nutritive value, largely contributed to the ecosystem primary production in the absence of water shortage. These annuals mainly thrived within or very close to the halophytes tufts, while the soil was almost bare between the tufts. Parallel studies performed in our laboratory pointed out that these spontaneous Medicago are particularly sensitive to salinity (Abdelly et al. 1995), and to N (Abdelly 1997) and P (Abdelly et al. 1991) deficiency. Furthermore, shoots of the annuals growing in association with the Medicago species contained relatively low Na⁺ concentrations (Fig. 7). Hence, the upper soil horizon, where these plants grew, was fertile and contained (relatively) low salt levels, as corroborated by the results of soil analysis (upper soil horizon in the tuft centre was always less saline than when taken at the tuft periphery). Desalinisation of the upper soil horizon by the superficial roots of halophytes could be responsible for this micro-gradient of salinity. Moreover, litter from the halophyte fallen organs and organic debris accumulated by the wind at the feet of tufts, may have contributed to localised soil enrichment in N and P (Fig. 4a, b). Soil aeration near these plants would be improved by this organic matter and by the higher soil level under the tufts, leading to better drainage capacity. Improved soil aeration is favourable for nitrification and N₂ fixation, favouring the colonisation of the halophytes tufts by the Medicago spp. Therefore, halophytes directly contributed to maintenance of a relatively low salinity and high fertility in the upper soil horizon, enabling the growth of annuals.

The halophytes may also play an indirect role by developing deep root systems exploiting the more saline soil horizons, as shown by the presence of halophyte roots at 1 m depth and by the vertical increasing salinity gradient (Table 1). The halophytes could thus limit rise of the salty water-table, allowing rainfall water infiltration into the upper soil layers. Several studies have demonstrated the role of halophytes in the soil desalinisation. Zhao (1991) showed that Salsola salsa biomass production could reach 20 t ha⁻¹, including 3 to 4 tonnes of salt exported from the soil. Less productive Batis maritima displays a similar desalinisation capacity (3 t ha⁻¹) (Le Houérou 1993), as does the succulent Sesuvium protulacastrum (Pasternak and Nerd 1996). The latter would be particularly interesting because of its high salt tolerance (growth stimulation up to 800 mM NaCl) despite accumulating high salt levels in the shoots (6 mmol g⁻¹ DW, representing ca. 35% of the whole plant biomass) (Messedi et al. 2001). In a 4-year study, Keiffer and Ungar (2002) observed a significant decline in brine-affected soils, following introduction of halophytes (Atriplex prostrata, Spergularia marina, and Suaeda calceoliformis), so that glycophytes could successfully establish. On the other hand, involvement of halophytes in the creation of micro-habitats favouring the development of Medicago spp. and their microbial symbionts (namely, root-nodulating and nitrogen-fixing rhizobia), has been reported by Bekki (1995) who showed that Medicago ciliaris plants growing in combination with Suaeda fruticosa, had a higher growth rates and better nodulation and nitrogen fixation potentialities than the isolated ones.

Table 1 Soil ionic characteristics in the central zone of the studied area in the Enfidha sabkha

Recently, Ravindran et al. (2007) assessed the desalinisation capacity of six halophytes (Suaeda maritima, S. portulacastrum, Clerodendron inerma, Ipomoea pes-caprae, Heliotropium curassavicum, and the tree Excoecaria agallocha), in terms of fast growth rate associated with high salt accumulation. All tested species decreased the EC of the saline soil used, in concomitance with an increase of the EC of plant samples. Salt removing capacity calculated over in 4 months of time was 504, 473.9, 396.3, 359.5, 325.2 and 301.5 kg ha⁻¹ of NaCl in S. maritima, S. portulacstrum, E. agallocha, C. inerma, I. pescaprae, and H. curassavicum respectively. Similar to our findings (Fig. 7), the desalinisation potential of the species tested was mostly associated with their salt accumulation capacity within their above ground tissues, without adversely impacting the plant growth activity. Salt compartmentalisation in the leaf vacuoles and osmotic adjustment are key mechanisms of plant salt tolerance. Both of these processes enabling the use of Na⁺ as a cheap osmoticum rather than its harmful accumulation in the cytosol, often take place in succulent halophytes lacking salt-excreting structures at their leaf surface (Tester and Davenport 2003; Debez et al. 2006).

5 Conclusions

This study revealed substantial soil and vegetation heterogeneity and diversity in the sabkha. In this area, the plant biomass production is largely determined by that of the forage annuals, especially the Leguminosae, growing in localised habitats surrounding bushy halophytes tufts. Thus, ecosystem micro-heterogeneity, combined with large-scale radial heterogeneity, is an important factor of its productivity, in addition to plant diversity. The salt-tolerant perennials improved the soil properties, mainly by decreasing the soil salinity owing to their high salt accumulation capacity. In addition, they provided “islands of fertility”, enabling the growth of fodder annuals with high agronomic value. The latter species used the mineral resources accumulated in the upper soil horizons, near the halophytes, owing to a sustained fats growth, associated to a high efficiency of nutrient availability. These data constitute a strong argument in favour of the practical utilisation of halophytes towards the restoration of marginal and/or cultivated salt-affected lands, by reducing the soil salinity level and improving its physical and chemical properties. Long-term data are required to better assess the positive impact of halophytes on the sabkha ecosystem.