GUEZLAOUI et al. Revue Agrobiologia (2018) 8(2): 1145-1154

Revue Agrobiologia www.agrobiologia.net ISSN (Print): 2170-1652 e-ISSN (Online): 2507-7627

ECOLOGICAL CHARACTERIZATION AND PHYLOGENY OF HALOPHILOUS COMMUNITIES. EXAMPLE OF SOUTHERN SPAIN AND NORTHERN ALGERIA

GHEZLAOUI Sidi-Mohammed Bahae-Ddine1*, ALONSO María Ángeles2, ABI-AYAD Linda1, GALLARDO Ana Juan2, MORENO Joaquín2 and TERRONES Alejandro2

1. Department of Agronomy. Faculty of Life Sciences of the Earth and the Universe. University of Tlemcen. Laboratory of Ecology and Management of Natural Ecosystems. Team N ° 5: Conservation and valorization of threatened species in Mediterranean habitats. B.P. 13 000. Algeria. 2. Biodiversity Institute C.I.B.I.O. Department of Environmental Sciences and Natural Resources. University of Alicante. Spain.

Reçu le 29/10/2018, Révisé le 01/12/2018, Accepté le 08/12/2018

Abstract Description of the subject: Halophilic ecosystems are among the habitats of greatest interest because they contain plant stands that are able to cope to considerable salt stress that cannot be supported by the rest of the vegetation, including glycophytes. Objective : The objective of this study is to understand which are the variables that determine the structure of halophilic plant communities, in order to create a tool for conservation. Methods : We made an ecological approach, based on floristic surveys at two sites known by the presence of salt, also called salt lakes. In order to better understand the structure of this type of plant, and on the basis of the results obtained, the variables which have more weight in the multivariate analysis are the species, adaptation and biotype criteria. Results : The biological aspect reveals dominance in these ecosystems of the euhalophytes species 24% to 30%. For biological types, the therophyte aspect prevails in the Sebkha of Messerghine (Algeria) with 54%. On the other hand, it is the nanophanerophytes that dominate the Saladar de Mata (Spain) with 41%. Finally, the analysis of the phylogenetic structure of the two stations on both sides of the Mediterranean Sea, offers a strong correlation between the botanical families of followed by the families of Poaceae, Cyperaceae and Juncacea. Conclusion : Given the results of this work, it can be concluded that in all the variables studied. The adaptation of the species to the clean saline environment is the one that has the most weight in the development of the halophilic community, compared to other ecological variables. Keywords : Ecology-Phylogenetic-Halophytes-Algeria-Spain

CARACTERISATION ÉCOLOGIQUE ET PHYLOGENIQUE DES COMMUNAUTÉS VÉGÉTALES HALOPHILES. EXEMPLE DU SUD DE L'ESPAGNE ET DU NORD DE L'ALGÉRIE Résumé Description du sujet : Les écosystèmes halophiles figurent parmi les habitats qui suscitent le plus d’intérêt, car ils abritent des peuplements végétaux qui sont capable de faire face à un stress salin parfois considérable, et qui ne peut être supporté par le reste de la végétation, notamment les glycophytes. Objectifs : L'objectif de cette étude est de comprendre quelles sont les variables qui déterminent la structure des communautés végétales halophiles, afin de créer un outil pour la conservation. Méthodes : Nous avons réalisés une approche écologique sur deux sites connu par la présence du sel, appelés aussi lacs salés. Afin de connaitre mieux la structure de ce type de végétaux, et sur la base des résultats obtenus, les variables qui ont plus de poids dans l'analyse, sont les critères espèce, adaptation et biotype. Résultats : L’aspect biologique révèle une dominance au niveau de ces écosystèmes des espèces euhalophytes 24% à 30%. Pour les types biologiques l’aspect thérophytes l’emporte au niveau de la Sebkha de Messerghine (Algérie) avec 54% par contre, c’est les nanophanérophytes qui dominent au niveau du Saladar de Mata(Espagne) avec 41%. Enfin l’analyse de la structure phylogénétique des deux stations de part et d’autre de la méditerranée offre une forte corrélation entre les familles botaniques qui peuplent les écosystèmes salins. La famille qui possède la plus grande présence est celle des Amaranthaceae suivie par les familles des Poaceae, Cyperaceae et Juncacea. Conclusion : Compte tenu des résultats de ce travail, il peut être conclu que dans toutes les variables étudiées l'adaptation de l’espèce au milieu salin propre, est celle qui a le plus de poids dans l'élaboration de la communauté halophile, par rapport à d'autres variables écologiques. Mots clés : Ecologie, Phylogénétique, Halophytes, Algérie, Espagne.

* Auteur correspondant: GHEZLAOUI Sidi-Mohammed Bahae-Ddine, Mail:[email protected]

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GUEZLAOUI et al. Revue Agrobiologia (2018) 8(2): 1145-1154 INTRODUCTION in order to highlight the ecological parameters that have a direct influence on the The Mediterranean basin is recognized configuration of these halophyte plant as a region of great interest, as in all its communities in these types of ecosystems. geographical areas, several have been To achieve this objective, the methodology designated as hot spots [1]. that has been used is that of the study of In the Mediterranean vegetation stands, there is metacommunities. a type of vegetation that often develops in the The flora and halophilic vegetation of salt zones, occupying the endoretic basins, in southeastern Spain and northwestern Algeria this case the Chotts, Sebkhas, Dayas and the are very similar for geological, geographical Saladars, areas of migration of many birds. and bioclimatic reasons (Le Floc'h 2001) [6]. The appearance of halophyte species is This study provided the first data on the essentially linked to the evaporation of phreatic comparison of these two distinct zones, waters which deposit the salts on the surface characterized by ecovicariant [2]. metacommunities. The study of the structure of these ecosystems The localities analyzed share a large number of and the comparison with fragments of similar genera and species, which could provide the ecosystems on a wider geographical scale is basis for producing different models in order to fundamental for studying the structural and provide new views (panoramas) to be given to evolutionary dynamics of these taxa. This the phenomena of climate change [7]. theme is necessary for conservation biology [3]. The concept of meta-community not only MATERIALS AND METHODS proposes the study of the ecosystem as a unit, but also as a flow of information between 2.1. Study zone neighboring communities, and how they relate The study was conducted on two distinct to one another [4]. According to the concept areas. La Laguna de la Mata (Alicante) in the of, a meta-community is a set of communities southeast of the Iberian Peninsula (Spain) and that interact through migrations between the Sebkha of Messerghine (Oran) in different patches of information transmission. northwestern Algeria, Loc. 1 and Loc. 2 (Fig. It includes the concept of dynamics of 1). These study sites were chosen according to metapopulations, set interactions and local different criteria, including a similar biotope. populations [5]. The two saline lakes are close to the coast The objective of this study is to understand the (coastline), but do not belong to coastal salines variables that determine the structure of fed by sea water. They share the same bioclimat halophyte plant communities, mediterranean semi-arid (www.globalbioclimatics.com).

Figure 1: Station location (Loc 1 and Loc 2).

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GUEZLAOUI et al. Revue Agrobiologia (2018) 8(2): 1145-1154 This choice is guided by the presence of Genkel [21], divided the halophytes into three halophytic stands at the two stations on both groups: euhalophytes, crinohalophytes, and sides of the two banks. This type of vegetation glycohalophytes, but this classification has is locally common on gypsum substrates in the been modified by Nagalevskii [22], and Zhao Maghreb. It represents only a small flora and et al. [23]. Salt tolerance in euhalophytes is rare structures of vegetation, with the based on accumulation, as they accumulate exception of the steppes of Sparta and Atriplex salts in their tissues, crinohalophytes depend indicated at the more continental level [8]. on excretion of toxic ions like Na+ and Cl− as they are capable of excreting salts out of the 2.2. Electrical conductivity plant body, and glycohalophytes rely on avoiding mechanism by preventing the The electrical conductivity of the soil accumulation of excess salts [24]. (C.E) was measured by the saturated pulp method. To extract 1/5 (20 g of soil + 100 ml 2.4. Phylogenetic characterization. of distilled water). At each station we sampled soil at the nutrient horizon of the taxa Phylogeny can be defined as "the inventoried. Many authors agree that in a salt historical course of the descendants of environment, the root system is superficial [9, organized beings" based on the basic concept 10, 11, 12]. of descent with modification. The formal support of representation, admitted by all, is 2.3. Florist characteristics the phylogenetic tree [25]. This representation is the formal support of the "resemblance" or We have done floristic surveys on areas the difference between the different taxa. From occupied by a halophilous vegetation along the anatomy to molecular biology, to ontogeny and sebkha of Messerghine (Oran) and the Saladar paleontology, the concept of resemblance was de Mata (Alicante). The Stigmatiste method approached in different ways according to the was used for the sampling of vegetation [13, school of systematic [26]. 14]. The minimum area of the station There are several algorithms or heuristics to Messerghine is 32 m2. On the other hand of in subject the construction of trees to computers. the Saladar de Mata it is about 60 m2. We Before proceeding to the molecular considered the abundance index for each phylogenetic construction, it is necessary to species in reference to the [15]. The taxa were have an alignment of the sequences since each determined from the new flora of Algeria and position will be a putative character [27]. In the southern desert regions of Quezel & Santa our study, the sequences were obtained from [16], Bonnier [17], and the vascular flora of Genbank © public access database. http: eastern Andalusia [18]. //www.ncbi.nlm.nih.gov/genbank. The elaboration of floristic tables in which The sequencing of I.T.S (Internal Transcribed the inventoried species appear is joined by Spacer) will be exploited. We used MEGA an introduction of four-letter codes in software v.5.05 to align the sequences and lower case, taken from the vernacular perform a phylogenetic tree through the name of each species. Example: Limonium Neighbor-Joining [28]. furfuraceum (lifu) (Tab. 1). This approach will facilitate the processing of the 2.5. Treatment of ecological variables variable at the level of the variable matrices [2].For each taxon, we will also In each of the studied sites, Algerian and consider the biological type Raunkier Spanish, the different parcels were selected for [19], and its adaptation [20]. analysis, in which we studied several variables that constructed four tables (Fig. 2).

Figure 2 : Tables of matrices

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GUEZLAOUI et al. Revue Agrobiologia (2018) 8(2): 1145-1154 Table 1: Coding of taxa listed by station

Loc. 2 Messerghine (Algérie) Loc. 1 Saladar de Mata (Espagne) Code Taxons Code Taxons dagn Daphne gnidium arma Arthrocnemum macrostachyum tepo Teucrium polium safr Sarcocornia fruticosa Amma Ampelodesma mauritanicum hapo Halimione portulacoides cial Cistus albidus frco Frankenia corymbosa Lade Lavandula dentata lica Limonium caesium civi Cistus villosus lysp Lygeum spartum aval Avena alba suve Suaeda vera parh Papaver rhoeas lyin Lycium intrincatum sami Sanguisorba minor arba Artemisia barrelieri mavu Marrubium vulgare lipa Limonium parvibracteatum ermo Erodium moschatum lisa Limonium santapolense brni Brassica nigra lifu Limonium furfuraceum alro Allium roseum lico Limonium cossonianum homu Hordeum murinum plcr Plantago crassifolia brdi Brachypodium distachyum icri Inula crithmoides brru Bromus rubens juma Juncus maritimus Aetr Aegilops triuncialis spme Spergularia media Alca Alyssum campestre elel Elymus elongatus memi Medicago minima scni Schoenus nigricans avst Avena sterilis juac Juncus acutus euun Eurucaria uncata agla Atriplex glauca sasi Salsola sieberi sapa Salicornia patula salo Salsola longifolia susp Suaeda spicata sate Salsola tetragona hypr Hymenolobus procumbens saka Salsola kali spdi Sphenopus divaricatus sufr Suaeda fruticosa pain Parapholis incurva haam Halopeplis amplexicaulis liec Limonium echioides atha Atriplex halimus arsc Arthrophytum scoparium lipr Limonium pruinosum save Salsola vermiculata atdi Atriplex dimophostegia lysp Lygeum spartum hasa sativus peha Peganum harmala maae Malva aegyptiaca aspen Astragalus pentaglottis taaf Tamarix africana taca Tamarix canariensis

The choice of the variables was made on the - A second ecological matrix that treats parcels basis of the characteristics that determine a and electrical conductivity. saline environment. It has been demonstrated in - A third matrix of abundance that opposes the literature by numerous authors [29, 20]. The parcels to species. variables are: The electrical conductivity of the - A final matrix called the matrix of traits soil (C.E). The presence of the species. The which treats species and adaptation to salinity. biotype [19]. Adaptation to salinity [30] and The processing of all these matrices was treats abundance (according to the Braun-Blanquet in an analysis of the multiple correspondences method [31]. The matrices formed are: with the SPSSv.15. software. - A first matrix called forms life matrix, which treats the life of the species and the biotype.

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GUEZLAOUI et al. Revue Agrobiologia (2018) 8(2): 1145-1154 RESULTS it fluctuates between 26 and 110 dS / m, characterizing a saline soil. 1. Electrical conductivity The salinity of the soil has a certain influence on the development of vegetation. The At each station, two samples were taken presence of large quantities of salts in the soil at the feeder horizon of the taxa inventoried solution lowers the water potential and greatly (Tab. 2). reduces the availability of water for .

Table 2: Electrical conductivity This is called a physiologically dry medium [32]. Loc. 1 :Saladar de Mata Loc. 2 : Messergine We note that the salinity is high. The organic (Espagne) (Algérie) matter content is very low, it does not exceed N° Conductivity N° Conductivity 1.2%. This is certainly due to the low Ech. C.E.(dS/m) Ech. C.E.(dS/m) vegetation cover [33]. 1.1 120 1.1 130 1.2 110.5 1.2 130 2. Floristic diversity 1.3 108.5 1.3 120 1.4 88.6 1.4 160 The plant stands at the two stations are 1.5 65 1.5 170 halophytic. Adaptation to high levels of salts is 1.6 26 1.6 180 largely explained by the dominance of 1.7 18.7 1.7 200 euhalophytes in the Spanish zone with 33%, 1.8 71.5 1.8 200 followed by glandular crinohalophytes and 1.9 20.6 1.9 120 1.10 18 1.10 130 glycohalophytes respectively with 30%. 1.11 15.4 1.11 140 Downy crinohalophytes account for only 7%. 1.12 12.8 1.12 160 In the Algerian zone the euhalophytes and 1.13 11.7 1.13 130 glycohalophytes dominate with a percentage of 1.14 10.9 1.14 100 30% each. They are followed by the 1.15 8.5 1.15 70 crinohalophytes with glands 23% and lastly the crinohalophytes with down 17%. The biotype The pH is alkaline it oscillates between 07.20 aspect in the Saladar de Mata (Spain) knows and 8.00 at the level of the two stations. The the dominance of the nanophanerophytes 41%, electrical conductivity is higher in the Sebkha followed by the chamephytes 19% and the of Messerghine where it varies between 70 and therophytes 18%. Inthe last comes the 200 dS / m. On the Saladar de Mata, geophytes and the hemicryptophytes with 11% (Fig. 3).

Figure 3 : Floristic diversity

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GUEZLAOUI et al. Revue Agrobiologia (2018) 8(2): 1145-1154 The influence of stress phenomena in these aridity of the climate and in particular the zones is felt on species with a long life summer water stress that provides this expectancy [8].The strong expression of the speciation [35]. nanophanerophytes and the chamephytes in This phenomenon favors short cycle species particular at this station is reinforced by the (therophytes) and accelerates the rate of disjunction of area, by the formation of genetic exchange. It is indeed one of the most endemo-vicariants in the Mediterranean zone important factors in the process of taxon (schisoendemism) [34]. formation in these ecosystems [8]. Therefore, in the Sebkha of Messerghine (Oran), the therophytes are the most dominant 3. Phylogenetic characterization with a percentage of 54%. They are followed The results obtained show that the by the chamephytes 21%, the phanérophytes phylogenetic structure of the two ecosystems 11%, the hemicryptophytes 8%, and lastly the offers a strong correlation between botanical geophytes and the nanophanérophytes 3%. families that are part of saline ecosystems with Thus, one reason for the dominance of a type of adaptation that occurs (Fig. 4). therophytes in these areas, in the Mediterranean region and in the Maghreb, seems to be the

Figure 4: Structure of the phylogenetic tree

The family that has the greatest presence is the It should be noted that for both stations on both Amaranthaceae followed by the Poales which is sides of the Mediterranean, we note a the phylogenetic group (sensu APGIII), which similarity in the genera and species that includes the families Poaceae, Cyperaceae and colonize the two sites. The diversity centers for Juncacea. the Amaranthaceae are more oriented towards Despite the recent interest in the south-western Africa and south of the Sahara and classification of the desert. Most species occur in tropical Africa Amaranthaceae family. There is always a and North America [39]. need to study phylogeny. Previous studies of the Amarantheceae have shown that 4. Multi-varied analysis this is the sister group of Chenopodiaceae As a result of multiple factorial analysis in the order [36], and of correspondence. We obtained measures of should be merged [37, 38]. APG (Group discrimination between the variables of the Angiosperm Phylogeny) 1998 and 2003. study of the two sites (La Mata and Oran) (Fig. 5 and 6).

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GUEZLAOUI et al. Revue Agrobiologia (2018) 8(2): 1145-1154 This linkage of different variables selected On the basis of the results obtained, the for the study provides a model of a unified variables that have more weight in the saline environment structure that includes analysis and explain more the structure of ecosystem analyzes in general. the community are the species, adaptation and biotype.

Figure 5 : Discrimination measures of the variables studied

Figure 6: Diagrams of centroides of ecological variables

Repeating this pattern in both places. It proves view of the various adaptations of halophyte that the variables that are not discriminated are species to the saline environment [40]. The the electrical conductivity of the soil and the variables that have more weight in this analysis abundance of species (Fig. 5). Moreover, the are adaptation, species and biotype. From this factor analysis of the multiple correspondences analysis, two dimensions were obtained for performed shows two joint diagrams of each of the studied sites, each of which are centroids of variables, each belonging to explained so far by the mean of the variance different localities. and represent the amplitude of this variance. A In both diagrams several groups of halophyte sample of degree of importance of this species are clearly visible and differentiated dimension in the overall solution. separately (Fig. 6). We obtained a total of three For Loc; 1 (Spain) these dimensions are 60.9% groups of species at both sites, this explains a and 53.4%, respectively, with an average

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GUEZLAOUI et al. Revue Agrobiologia (2018) 8(2): 1145-1154 reliability index of 0.82.Whereas for Loc 2 It should also be noted that many studies work (Algeria), the dimensions are 54.1% and only in relation to the fluctuation of the 49.7% respectively, with an index alpha of conductivity spectrum as a function of the Cronbach of 0.77 (Tab. 3). seasons. Measurements are made throughout the year [29, 42]. Table 3: Discrimination measures models of Using the measured conductivity as a variable both localities may also explain the structure of this type of vegetation. But that would not be enough to Loc 1 :Saladar de Loc2 : Messerghine make it the unique determining variable. And Mata (Algérie) the observation is clear in this work. It is worth (Espagne) noting the use of the Cronbach alpha % de Alfa de % de Alfa de coefficient which is indicated as a control variance Cronbach variance Cronbach Dimention 1 60.9 0.84 54.1 0.79 index to evaluate these analyzes. The average Dimention 2 53.4 0.78 49.7 0.75 coefficient obtained for Loc. 2 is greater than Avreage 57.2 0.82 51.9 0.77 0.7, whereas that obtained for Loc. 1 is greater than 0.8. We observe that the two dimensions are of It can therefore be considered that the fidelity approximately the same importance since the of this model is acceptable for the lagoon of two eigen values are very beside in both cases. Oran, and good for the lake of La Mata, since Thus the Cronbach alpha coefficients for the the more the value of this index tends to 1, the different dimensions laguna of La Mata (Loc; more it acquires a high reliability [43]. 1) are 0.84 for dimension 1 and 0.78 for On the basis of these results, it can also be dimension 2. However, a fidelity index of 0.79 concluded that in all the variables studied, the is related to the dimension 1 of the Oran adaptation of the species to the clean saline lagoon (Loc. 2) and one of 0.75 is related to environment is the one that has the most the dimension 2 of the same locality. weight in the development of the halophilic community, compared with other ecological DISCUSSION AND CONCLUSION variables, including electrical conductivity. This does not appear to be considerably This study established a global constant, as it varies seasonally throughout the approximation of halophile communities in year. It also depends heavily on periods of order to determine the main variables flooding, drought and heavy rainfall [44]. governing the spatial succession of this type of vegetation. There are many studies on plant ACKNOWLEDGMENTS communities in salt ecosystems. But very few who take these ecosystems as a whole without This work was conducted as part of a establishing a bias band [20]. project of the Spanish Agency for International With the results obtained in this study, we Development Cooperation. A.E.C.I.D No. AP / demonstrate that the coverage of a particular 042 501/11. Thanks to all the staff of the Ibero- species does not determine the structure of the american biodiversity center of Alicante ecosystem. Taking into account the results, and (Spain) taking into account the distribution of these species, which have a similar presence REFERENCES according to the presence of the salts, with average adaptations. This parameter seems to [1]. Médail F. & Diadema K. (2009). Glacial have the greatest weight in the structure of this refugia influence plant diversity patterns in the méditerranean Bassin. J .Biogogr. plant community. Thus, the appearance of the 36:1333-1345. different forms that halophyte species have [2]. Ghezlaoui B-A., Benabadji N., Benmansour developed to adapt to the salt concentration is D., Merzouk A. (2011). Analyse des itself a determining factor in the spatial peuplements végétaux halophytes dans le structure of the ecosystem. Consequently, Chott El-Gharbi (Oranie-Algérie). Acta other works give more importance to the Botánica Malacitana, 36: 113-124. conductivity of the soil in this strand [41]. [3]. Farina A. (1993). L’ecologia d’El Systemi Ambiantali ,CLEUP, Padova.

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