Biomass Production and Ion Composition of Some Halophytes Irrigated with Different Seawater Dilutions

First International Conference on Saltwater Intrusion and Coastal Aquifers— Monitoring, Modeling, and Management. Essaouira, Morocco, April 23–25, 2001

Biomass production and ion composition of some halophytes irrigated with different seawater dilutions

S. Daoud*; M.C. Harrouni** and R. Bengueddour*** *Faculté des Sciences, Univ. Ibnou Zohr, Agadir **Institut Agronomique et Vétérinaire Hassan II, Agadir *** Faculté des Sciences, Univ. Ibnou Tofail, Kenitra

Abstract

Halophytic plant species have different degrees of tolerance to salinity, the aim of our study is to investigate a number of Moroccan and acclimated halophytes in relation to their potential to be utilised as cash crops in areas affected by salinity or to be irrigated with seawater in coastal areas, and to determine the level of salinity tolerance of these plants. A quick check system was developed in IAV Hassan II (Agadir) for the selection of promising plants with adequate salt tolerance. In our study plants belonging to different families: Avicennia germinans (Avicenniaceae); Aster tripolium (Asteraceae); Batis maritima (Batidaceae); Limoniastrum multiflorum (Plumbaginaceae); Rottboellia fasciculata (Poaceae); Sesuvium verrucosum; Sesuvium portulacastrum (Aizoaceae) and Spartina alterniflora (Poaceae) were grown in the quick check system under greenhouse conditions and watered with 5 seawater concentrations (0% (control), 25%; 50%; 75% and 100% seawater) obtained by diluting seawater with tap water. Plants survived in all treatments, growth and biomass production were enhanced in most species by low salinity and differed from one species to another at high salinity. However signs of growth inhibition were noticed at high seawater concentrations. The ash content of plants varied with the species; it ranged from below 10% in the excluders (shoots of A. germinans, S. alterniflora, R. fasciculata and L. multiflorum) to over 40% in the includers (shoots of A. tripolium, B. maritima and the 2 Sesuvium) which accumulated high mineral levels. Inorganic matter increased with the increase of salinity up to a certain concentration depending on the species. Na and Cl were the dominant ions and their concentrations increased with the increase of seawater concentration while K concentration decreased.

Seawater irrigation did not affect Ca uptake and transport through the plant conditions which prevent Na induced Ca deficiency and enhance plant growth. These results support the recommendation for the use of halophytes under saline irrigation as promising species for the valorisation of coastal lands and strongly salt affected zones. Key words : Salinity, halophytes, quick check system, salinity tolerance, biomass production, ion composition.

Introduction Seawater intrusion into coastal aquifers is one of the causes for salinity problems in coastal regions. No conventional crop plants can give an acceptable yield beyond a limited degree of salinity. Generally the intrusion of seawater induces salinity in the aquifers well above the level tolerated by conventional plants. An alternative approach is the domestication of naturally occurring halophytes for crop production since they already have the requisite level of salt tolerance (Gleen et al. 1993 and Choukr-Allah, 1993). Halophytes are plants that grow naturally in saline environments, such as salt marshes, salt spans and salt deserts (Jeffries, 1981). Since Morocco has over 3,500 km of coastline, it is advisable to use the brackish water resources available. Seawater cannot be used for drinking but may be suitable for irrigated agriculture in coastal areas. Indeed, seawater irrigation of halophytes offers an opportunity to bring these lands into a form of agricultural production. There are more than 1500 known halophytic plant species throughout the world. They constitute the basis for the selection of plant material that combines economic utility with the ability to grow, produce and reproduce under high salinity (Aronson, 1989). In recent years, it has been demonstrated that revegetation of saline habitats with halophytic species is profitable and provides many additional benefits as they can be used for fodder, fuel, oil, wood or fibre production. They can also be used for land reclamation, dune stabilisation or as ornamental plants (Lieth and Al Massoum, 1993a). There are some 32,000 km of sandy coasts unused for agriculture, they could be brought under cultivation in a variety of conceivable aqua-agro-systems in littoral, tidal and estuarial zones, by appropriate new methods of agro-management (Aronson, 1986). Increased research on the selection of halophytic species of economic uses, with appropriate management could result in the rehabilitation and revegetation of salt-affected land. In Morocco an important number of halophytic species can be found in river marshes at sea level but also in saline ecosystems of the Saharan bio-climatic range.

The aim of our study is to assess plant species occurring in saline environments and select from these prospective candidates for a variety of applications. In order to forecast sustainability a screening programme is being developed consisting of physiological, ecological, chemical and agronomic analyses. This will help to select halophytic species for their ability to tolerate salinity and for their economical potential.

Materials and methods Eight halophytic species belonging to different families were tested for their salt tolerance potential (Avicennia germinans; Aster tripolium; Batis maritima; Limoniastrum multiflorum; Rottboellia fasciculata; Sesuvium portulacastrum; Sesuvium verrucosum and Spartina alterniflora). Experiments were conducted at IAV Hassan II Complexe Horticole d’Agadir (30° 20' Northern latitude, 9° 30' Western longitude, 32 m above sea level) under greenhouse conditions. The plants were grown for four weeks on a quick check system, it is an automated irrigation and drainage system, where plants were put in 100 L containers and regularly flooded with the required water. Small electric pumps were used to recycle water several times during a 12-hour-day period on the time basis of 45 mn flooding and 20 mn of total drainage. The plants were cultivated in plastic black pots on coastal sand substrate with four replicates per species. Experiments consisted of five salinity treatments: tap water (control); 25; 50; 75 and 100% seawater. These dilutions were obtained by tap water addition. Plants were adjusted to saline water irrigation by rising the salinity of the solution in increments of 1/8th every 2 days until the required concentration was reached. A nutrient solution containing 60mg/l N, 6.5 mg/l P, 40 mg/l K and trace elements was used in order to fertilise the five treatments. Temperature was monitored daily with a “mini-maxi” thermometer. At the end of the experiments the plants were harvested for biomass and other parameters assessment. Plants were washed with distilled water through a fine sieve and separated into shoots and roots. The dry weight (dw) was obtained after oven drying the plants at 65-70 °C for 48 hours. Growth was estimated on the basis of dry weight. Shoot and roots of each plant were ground in an electric grinder and 500 mg samples were taken and burnt in a muffle furnace at 485 °C. The ash content was obtained by weight difference before and after calcination. Mineral composition of shoots and roots for each species was determined from ash analyses. Na and K contents were determined by flame photometer after ash dissolving in 2N HCl. Ca and Mg contents were determined with an atomic absorption spectrometer. Concentrations of these minerals in plant tissues are expressed on a dry weight basis.

Results General conditions During the first experiment the average minimum temperature was 21.5 °C with an absolute minimum of 18.5 °C and the average maximum temperature was 41.9° C with an absolute maximum of 50.0 °C. During the second experiment, the average minimum temperature registered was 15.9 °C with an absolute minimum of 12 °C and the average maximum was 40.7 °C with an absolute value of 44 °C. Chemical characteristics of seawater dilutions used for irrigation of plants in the quick check system prior to fertiliser addition in comparison with tap water showed that Cl, Na, K, Ca, Mg and concentrations increased with the increase of seawater ratio. However Cl and Na are the dominant ions (Table 1). N and P contents were very low compared to the other ions, they were improved by addition of fertilisers in the second experiment. Table 1: Characteristics of tap water and seawater dilutions prior to fertiliser addition

+ - + ++ ++ - pH EC Na Cl K Ca Mg N-NO3 P (mg/l) Treatments (dS/m) (mg/l) (mg/l) (mg/l) (mg/l) (mg/l) (mg/l)

Tap water 8.05 00.77 039.91 540.00 003.50 095.59 0011.20 Trace 1.35

25% seawater 7.70 12.10 3722.00 6452.37 116.67 098.53 0065.60 0.60 1.35

50% seawater 7.55 22.00 5201.80 8968.80 183.33 132.35 0984.00 0.30 1.25

75% seawater 7.64 30.80 8071.70 13453.20 194.44 141.18 1064.00 0.16 1.50

100% seawater 7.55 38.50 11211.0 18834.48 377.78 266.18 1976.00 0.21 2.05

Survival and growth parameters After 45 days of growth in the five seawater dilutions, all species tested had 100% survival in all treatments. The effect of salt stress on plants was expressed on dry matter production. Shoots and roots of most species showed an increase of the dry weight in low and moderate salinity treatments. Indeed, R. fasciculata; S. portulacastrum and S. verrucosum had the maximum biomass production in treatment 25% seawater, while A. germinans and B. maritima showed their maximum biomass production in treatment 50% seawater. However, A. tripolium and S. alterniflora produced maximum dry weight in the control treatment (Table 2). Beyond the optimum treatment a progressive decrease in dry weight of different parts of the plants was registered with the increase of seawater concentration. However, the percentage of the reduction in full strength seawater treatment differed from one species to another (Table 3). A. germinans;

B. maritima; L. multiflorum; R. fasciculata and S. verrucosum had less than 50% redution, S. portulacastrum had about 51% reduction; A. tripolium and S. alterniflora had more than 70% reduction. Table 2: Dry matter production (g) in shoots and roots of plants in the five treatments 0% 25% 50% 75% 100% Shoot Root Shoot Root Shoot Root Shoot Root Shoot Root Plant species

A. tripolium 21.40 08.25 12.33 04.95 08.67 04.95 10.83 04.54 04.63 02.81 A. germinans 2.06 1.67 2.55 2.16 2.98 1.93 1.42 0.96 1.31 0.90 B. maritima 06.38 2.63 7.17 2.83 10.16 3.33 9.67 2.33 9.17 2.16 L. multiflorum 10.86 03.04 13.06 02.87 08.98 02.18 08.52 02.05 07.98 02.55 R. fasciculata 11.00 03.00 13.25 01.50 12.50 01.88 07.88 01.50 07.75 02.25 S. verrucosum 05.38 01.53 05.50 01.13 04.63 01.00 03.25 0.63 03.13 0.70 S. portulacastrum 03.50 0.50 3.88 0.50 03.38 0.45 02.50 0.38 01.75 0.20 S. alterniflora 40.79 53.72 20.68 25.85 16.99 22.92 14.57 21.96 08.86 18.13

Table 3: Reduction percentage (%) of the plants in high salinity treatments compared to the control Plant species 50% 75% 100% A. tripolium 54.06 48.16 74.91 A. germinans -31.64 36.19 40.75 Batis maritima -49.72 -33.19 -25.75 L. multiflorum 10.32 15.93 24.85 R. fasciculata -02.71 33.00 28.57 S. verrucosum 18.52 43.85 44.57 S.portulacastrum 04.25 28.00 51.25 S. alterniflora 57.77 61.35 71.44

The root to shoot ratio in terms of dry weight did not vary in the same manner for all plants, each species having its own pattern for this parameter (Table 4).

Table 4: Root to shoot ratio of the plants in the five seawater treatments

Plant species Tap water 25% seawater 50% seawater 75% seawater 100%seawater A. tripolium 0.39 0.40 0.57 0.42 0.61 A. germinans 0.81 0.85 0.65 0.68 0.69 B. maritima 0.43 0.41 0.35 0.26 0.25 L. multiflorum 0.22 0.19 0.21 0.17 0.22 R. fasciculata 0.30 0.13 0.17 0.20 0.30 S. verrucosum 0.30 0.21 0.22 0.20 0.23 S. portulacastrum 0.15 0.13 0.14 0.16 0.12 S. alterniflora 1.03 1.17 1.25 1.38 1.84

Ash content In all species, the increase of salinity increased the ash content of plants both in the shoots and in the roots. However, the ash content varied with the species (table 5). It ranged from below 10% in the shoots of the excluders (A. gerninans; L. multiflorum; R. fsciculata and S. alterniflora), to over 40% in the shoots of the includers (A.tripolium; B. maritima; S. portulacastrum and S. verrucosum) which accumulated high mineral levels. It increased with the increase of salinity up to a certain concentration depending on the species. In the excluders the ash content was higher in the roots compared with the shoots, whilst in the includers root ash content was lower than that of the shoots. Table 5: Ash content (% of dry matter) in shoots and roots of plants in the five seawater dilutions 0% 25% 50% 75% 100% Shoot Root Shoot Root Shoot Root Shoot Root Shoot Root Plant species

A. tripolium 24.04 13.48 28.13 14.40 31.11 12.90 32 16.88 34.59 18.02 A. germinans 09.40 14.38 9.74 17.72 11.20 24.18 11.78 24.30 11.54 23.22 B. maritima 25.88 21.18 45.22 32.28 54.68 44.88 46.20 46.44 56.34 31.20 L. multiflorum 14.82 9.83 16.29 13.68 13.24 13.19 11.17 10.88 13.52 12.08 R. fasciculata 06.48 32.52 08.06 21.36 09.22 33.28 10.72 25.76 08.08 25.60 S. verrucosum 31.46 34.56 34.24 36.54 37.02 35.78 42.48 36.08 38.56 34.38 S. portulacastrum 29.34 22.52 38.88 21.36 39.56 20.86 40.00 14.58 34.48 13.98 S. alterniflora 09.82 15.04 13.52 17.31 13.94 21.64 16.90 32.66 18.12 38.16

Ion composition Mineral analysis was performed for several elements. Figure 1 shows a comparison between sodium and potassium in shoots and roots of the plants. Sodium is the most abundant ion and its concentration increased with the increase of seawater concentration. The figure indicates that the

plants which are in the category of includers ( A. tripolium; (B. maritima; S. verrucosum and S. portulacastrum ) concentrate more sodium in the shoots compared with the excluders (A. gerninans; L. multiflorum; R. fsciculata and S. alterniflora). In high seawater concentration treatments, the increase of sodium concentrations in the shoots was accompanied by a decrease in potassium content but in the roots potassium concentrations showed little variation or even increased with salinity. The K/Na ratio decreased with the increase of salinity in shoots and roots of most species. With the exception of the control treatment, this ratio was, on average, higher in the roots compared with the shoots, especially for S. portulacastrum (Figure 3). Magnesium and Calcium were present at lower concentrations than potassium and their concentrations varied with the species but were roughly comparable (Figure 2). The increase of seawater concentration did not have any noticeable effect on the contents of Mg and Ca. Nevertheless the Ca/Na ratio was affected by salinity and showed a general pattern of decrease with the increase of seawater concentration (Figure 3). L. multiflorum shoots showed the highest values compared with the other species, while B. maritima and R. fasciculata had high Ca/Na ratio in the roots.

Discussion Growth parameters Most species tested had their maximum biomass production in low salinity treatments. High seawater concentration reduced growth of all species. These results broadly match those obtained by Kelly et al.(1982), Gleen and O’Leary (1984), Gorham (1996); Harrouni et al.

Aster tripoplium Batis maritima

7 9

6 8 7 5 6 4 5 3 4 3 mmol/g DW mmol/g DW 2 2 1 1 0 0 Na K Na K Na Cl K Na Cl K Shoot Root Shoot Root

Sesuvium verrucosum Sesuvium portulacastrum

7 7 6 6 5 5 4 4

3 3 mmol/g DW 2 mmol/g DW 2 1 1 0 0 Na Cl K Na Cl K Na Cl K Na Cl K Shoot Roots Shoot Root

Avicennia germinans Limoniastrum multiflorum

7 7 6 6 5 5 4 4 3 3 mmol/g DW

2 mmol/g DW 2

1 1

0 0 Na K Na K Na Cl K Na Cl K Shoot Root Shoot Root

Rottboellia fasciculata Spartina alterniflora

7 7 6 6 5 5 4 4 3 3 mmol/g DW 2 mmol/g DW 2 1 1 0 0 Na Cl K Na Cl K Na Cl K Na Cl K Shoot Root Shoot Root

0% 25% 50% 75% 100% 0% 25% 50% 75% 100%

Figure 1: Na, Cl and K content (mmol/g dry weight) of shoots and roots of plants in 5 seawater treatments (tap water; 25%; 50%; 75% and 100% seawater)

Aster tripolium Batis maritima

2 2

1,5 1,5

1 1 mmol/g DW 0,5 mmol/g DW 0,5

0 0 Ca Mg Ca Mg Ca Mg Ca Mg Shoot Root Shoot Root

Sesuvium verrucosum Sesuvium portulacastrum

2 2

1,5 1,5

1 1 mmol/g DW mmol/g DW 0,5 0,5

0 0 Ca Mg Ca Mg Ca Mg Ca Mg Shoot Root Shoot Root

Avicennia germinans Limoniasrtum multiflorum

2 2

1,5 1,5

1 1 mmol/g DW mmol/g DW 0,5 0,5

0 0 Ca Mg Ca Mg Ca Mg Ca Mg Shoot Root Shoot Root

Rottboellia fasciculata Spartina alterniflora

2 2

1,5 1,5

1 1 mmol/g DW 0,5 mmol/g DW 0,5

0 0 Ca Mg Ca Mg Ca Mg Ca Mg Shoot Root Shoot Root

0% 25% 50% 75% 100% 0% 25% 50% 75% 100%

Figure 2: Ca and Mg content (mmol/g dry weight ) of shoots and roots of plants in 5 seawater treatments (tap water; 25%; 50%; 75% and 100% seawater)

Aster tripolium Batis maritima

2,00 2,00

1,50 1,50

1,00 1,00

0,50 0,50

0,00 0,00 K/Na Ca/Na K/Na Ca/Na K/Na Ca/Na K/Na Ca/Na Shoot Root Shoot Root

Sesuvium verrucosum Sesuvium portulacastrum

2,00 2,00

1,50 1,50

1,00 1,00

0,50 0,50

0,00 0,00 K/Na Ca/Na K/Na Ca/Na K/Na Ca/Na K/Na Ca/Na Shoot Root Shoot Root

Avicennia germinans Limoniastrum multiflorum

2,00 2

1,50 1,5

1,00 1

0,50 0,5

0,00 0 K/Na Ca/Na K/Na Ca/Na K/Na Ca/Na K/Na Ca/Na Shoot Root Shoot Root

Rottboellia fasciculata Spartina alterniflora

2,00 2,00

1,50 1,50

1,00 1,00

0,50 0,50

0,00 0,00 K/Na Ca/Na K/Na Ca/Na K/Na Ca/Na K/Na Ca/Na Shoot Root Shoot Root

0% 25% 50% 75% 100% 0% 25% 50% 75% 100%

Figure 3: K/Na and Ca/Na ratio of shoots and roots plants in 5 seawater treatments (tap water; 25%; 50%; 75% and 100% seawater)

(1999); Daoud et al.(2001) and Harrouni et al. (2001) who reported that low NaCl concentrations stimulate growth of some halophytic species, but an excess of salt decreases growth and biomass production. Maas (1987) reported that in most halophytic species growth decreases gradually with the increase of salt rate in the culture medium above a critical threshold specific to each species. The root to shoot ratio is an indicator of the effect of the growing conditions in the root system as it shows the change, if any, in the sink in comparison with optimal conditions of growth. Under drought stress conditions (especially moderate) it increases in order to enable the plant to increase its capacity for water uptake from the growing medium (Harrouni,1989). Under saline conditions up to a certain limit, the effect of salinity can be comparable to that of water stress as salt acts more as an osmoticum than as a toxic element. Thus the plants react as in the conditions of drought stress. Ash content The increase of seawater concentration involved an increase of the ash content in all parts of the plant, such response was reported by many authors (Watson et al., 1987 ; O’Leary, 1985 ; Harrouni et al., 1999; Koyro and Huchzermeyer, 1999a; Daoud et al., 2001 and Harrouni et al., 2001). The ash content differed according to plant species and plant organs. In general higher values were in the shoots of includers compared with their roots due to an excessive accumulation of NaCl in cell leaves in response to external salinity ( Darrel, 1995 and Abbas, 1995). These ions could represent more than 50% of the ash minerals (Le Houérou, 1992). Salt accumulation is one of the ways through which halophytic plants overcome the physiological water stress which is due to high salt content in the external medium (Gorham, 1996). It increased with the increase of salinity up to a certain concentration depending on the species. The means whereby these plants control their salt uptake and accumulation varied between species. However, some species (R. fasciculata; S. verrucosum and S. portulacastrum) had their maximum ash content in treatment 75% seawater; these species may regulate their osmotic potential by the accumulation of NaCl in the vacuole, but beyond a certain amount, plants exclude salt through their roots. Salt exclusion minimizes ion toxicity but accelerates water deficit which reduces growth at high salinity conditions (Koyro, 1997 and Koyro et al.1999a). Salt inclusion is the main mechanism of adaptation of terrestrial halophytes to high salinity. This mechanism facilitates osmotic adjustment but can lead to ion toxicity in the old leaves and in water deficit and shortage of carbohydrates in the younger leaves or in the meristematic zone if the plants are exposed for long time to high salinity (Koyro et al., 1999b).

Ion composition In saline treatments , Na and Cl were the most abundant ions in the plants and their concentrations increased with the increase of seawater concentration in the culture medium, while K content decreased. This response of halophytes reflects the utilisation of metabolically undesirable ions for osmotic adjustment (Flowers and Laüshli, 1983; Flowers, 1985) a process in which Na can be much more suitable than K (Marschner, 1995) since it accumulates preferentially in the vacuoles (Koyro and Huchzermeyer, 1999b). Seawater irrigation did not affect Ca uptake and transport through the plant although increased salinity is reported to reduce the amount of Ca in the plant (Lynch and Lauchli, 1985; Marschner, 1995; Koyro and Huchzermeyer, 1999a ). Ca/Na ratio decreased with the increase of salinity in most species but it considerably differed in different parts of a given plant. L. multiflorum shoots showed the highest values compared with the other species, while B. maritima and R. fasciculata had high Ca/Na ratio in the roots. Lynch and Lauchli (1985) reported that Ca increases salt tolerance of plants. This ameliorating effect of Ca is in accordance with its functions in membrane integrity and control of selectivity in ion uptake and transport. As a matter of fact in these plants the reduction of growth in full strength seawater treatment was very low, it was about 25% and 29% in L. multiflorum and R. fasciculata respectively. Moreover B. maritima had 26% higher biomass in full strength seawater compared with the control. These results show that for these species the limit of salt tolerance, which is defined as 50 % growth reduction , is in salinity higher than that of seawater.

Conclusion Halophytes irrigated with seawater represent a considerable potential as crop plants. Their growth may be stimulated by the presence of salts in the growth medium. At high salinity their growth is presumably limited by many factors but mainly because an imbalance in nutrient uptake, essentially K and Ca. Studies of salinity tolerance of plants irrigated with seawater in a quick check system under greenhouse conditions is the first step for the development of cash crops. Increased research on the selection of halophytic species which have an economic utilisation may enable the rehabilitation and revegetation of salt-affected lands given that the appropriate soil and irrigation management is applied.

Acknowledgements This work was carried out in the framework of the Concerted Action Project “Sustainable Utilisation of Halophytes in the Mediterranean and Subtropical Dry Regions”, financed by the

EU. Additional funds were obtained from UNESCO. The combination of the two inputs enable the establishment of a good infrastructure for research on halophytes and hence the achievement of substantial work.

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