Resumen
Treinta estaciones en el Parque Nacional El Kala (Noreste de Argelia) fueron objeto de un inventario florístico que se centró en el estudio de la ecología de geófitos bulbosos y tuberosos. La flora se caracteriza por una alta proporción de taxones raros y/o endémicos, entre ellos, 6 especies son endemismos algero-tunecinos pertenecientes a la familia Orchidaceae. En este trabajo, se da a conocer la presencia de una nueva especie para la flora argelina, Ophrys fusca subsp. lupercalis. Los análisis multivariantes revelaron, ciertas variables ambientales que determinan la distribución de los geófitos. Los lugares de interés son particularmente sensibles a las amenazas, particularmente las de origen antrópico.
Palabras clave: Especies raras; Endemismo; Flora.
Abstract
Thirty stations at the El Kala National Park (North Eastern Algeria) were the subject of a floristic focused on the study of the ecology of bulbous and tuberous geophytes. The floristic analysis was used to draw up a checklist of 67 species belonging to 36 genera and 14 families, among of which 19 species a high proportion of rare and /or endemic taxa; among them six signed taxa are endemic to algerian-tunisian mainly represented by family of Orchidaceae. In this work, we recorded the presence of a new species for the Algerian flora which is Ophrys fusca subsp. lupercalis. Multivariate analyses revealed certain environmental variables determining the distribution of geophytes. The visited sites show an alarming vulnerability and subject to threats, particularly anthropogenic ones.
Key words: Rare species; Endemism; Flora.
Introduction
The Mediterranean plant biodiversity is commonly known in the world, as one of the most three remarkable ecosystems, regarding species richness, and endemism (Myers et al. 2000). The geographic analysis of the high plant diversity (Barthlott et al. 1999) and the areas of high endemism rate (Verlaque et al. 1997) have shown an important complimentary tool for, classifying the whole Mediterranean basin as a "hot-spot" through the world (Médail & Quézel 1997).
Although, the flora of the southern- Mediterranean basin remains unknown, in particular the Algerian-Tunisian coastal mountainous, historically named "Kabylies-Numidia-Kroumirie", a phytogeographical name basically used by Quézel & Santa (1962-1963), and having a great floristic richness and a very high endemism rate (Véla & Benhouhou 2007).
The coastal of Numidia, "K3" in term biogeographical divisions as proposed by Quézel & Santa (1962) makes at the east a precise biogeographic unit and an Important Plants Areas (IPA) (Yahi & Benhouhou 2010) around the El Kala National Park (Marre 1992). In an ecological view point, this region is considered as highly important, considering its geographical location, climate, and its lakes and forests (de Bélair 1990). The yearly rainfalls are moderated in the coast, however they become abundant with the altitude (614 mm from El Kala city, 1.213 mm to the top of El Ghora soil) (Seltzer 1946), the ideal conditions for the development of bulbous and tuberous geophytes, tuber and rhizome (Danin & Orshan 1990). The perennial subterranean organs promote the plant survivals in periods of serious climatic conditions (Procheş et al. 2015). This form of life is more common in Monocots, including families of Orchidaceae, Asparagaceae, Amaryllidaceae and Liliaceae, as well as some Eudicots taxa (Vesely et al. 2012).
In Algeria, very recent limited data are available on the bulbous geophytes, meanwhile some other studies have been carried out on Orchidaceeae (de Bélair 2000, de Bélair & Boussouak 2002, de Bélair et al. 2005, Hadji & Rebbas 2013, Babali et al. 2013, Kreutz et al. 2013, 2014, Bougaham et al. 2015, Beghami et al. 2015; Hamel & Meddad-Hamza 2016, Hamel et al. 2017, Madoui et al. 2017, Boukehili et al. 2018) and Asparagaceae (Véla et al. 2016, Boubetra et al. 2017).
On top of that, the knowledge of the bulbous plants in Algeria and their distribution is mainly based on historical observations (Maire 19591987, Quézel & Santa 1962), and consequently several new species of Algeria (not found in the historic references) and some taxa "synonyms" established in the distinct species have been discovered in the last few years (Rebbas & Véla 2008, 2013, de Bélair et al. 2013).
* Geophytes are a group of flora whose ecology is not very well known. To this end, this article aims:
* To establish the inventory of geophytes at the El Kala National Park (North Eastern Algeria) and proceed to their identification and classification in order to draw up a floristic Checklist.
* To study the environmental factors influencing the ecological distribution of inventoried species.
* To enrich our database of authoctonous plants in the region in order to understand the phenomena encountered in the southern shore of the Mediterranean.
* To draw attention to the importance of protecting the flora of the region with a view to preserving it by putting in place conservation measures in order to develop a flora that is very important for biodiversity and the dynamics of forest ecosystems.
Materials and methods
Study region
The present study was conducted at El Kala National Park (EKNP), with a total surface area of 78438 ha (Fig. 1). Stands as one of the best landscape diversities, its biological heritage was found as one of the most diversified western Mediterranean basin (Stevenson et al. 1988, Benyacoub & Chabi 2000, Brahmia et al. 2002). This site is located in the extreme North-Eastern Algeria, and boarded to the north by the Mediterranean Sea, to the east by the Algerian-Tunisian borders, to the west by the city of El Tarf and vast marshes of Mekhada, and to the south by the mountain of Medjerda (Benyacoub & Chabi 2000).
According to the Emberger climagram (1955), the El Kala region is located within the bioclimatic sub-humid level of hot winter, to the limit of the humid level. The geological study showed that the study region mainly belongs to the Tertiary sector (Marre 1987), and it is represented by Numidian clays and sandstones, as well as deposits of sands, conglomerates, and banks of red or grey Pontian clay (Marre 1992).
Sampling of plants
Floristic Study
This study was carried out on 30 sites for the phytoecological monitoring, in which vegetation was studied for four years (2015-2018) with two seasons (Spring and Autumn) per year. The taxa have been identified accordingly to the new flora of Algeria and southern desert regions (Quézel and Santa 1962-1963), Flora of North Africa (Maire 1952-1987) and Italian Flora (Pignatti 1982).
The new nomenclature of the inventoried species were updated, taking into account recent works collected in the synonymic index, the bibliography of the North-Africa flora (Dobignard & Chatelain 2010, 2013), and the Electronic African plant database, accessible at [http://www.villege.ch/musinfo/bd/cjb/africa/recherche.php].
In addition, the listed species were documented and indicated following their biogeographical type, as described by Pignatti (1982), Blanca et al. (2009), Dobignard & Chatelain (2010-2013) and Euro+Med Plant Base (http:// ww2.bgbm. org/EuroPlusMed/).
Numerical analysis of the floristic data
All the floristic reports were subjected to two analyses: Canonical analysis of correspondences (CAC), and Linear Discriminant Analysis (LDA). The linkage between the flora data and the environmental variables was obtained by the CAC. The patch resulting in CAC leads to visualize the explanatory percentage of a variable on another (Ter Braak 1995). Moreover, the data of site table were subjected to the LDA (Legendre and Legendre 2012) to obtain a segregation of the main groups of the studied sites. Both of these analysis tests were performed using R software (Core Team 2013) for basic statistical analysis (package ade4, version 3.0.2) (Dray et al. 2018).
Results
Floristic composition
The floristic sampling allowed us to list 67 species belonging to 36 genera and 14 botanical families. The distribution of families by number of species is presented in (Table 1).
According to table 1, the family Orchidaceae dominates with 21 species (31.3%), second are the Amaryllidaceae and Asparagaceae with respectively 28.35% and 18% of the total number of taxa recorded, followed by Iridaceae with 6 species as 9%. Whereas, Araceae and Liliaceae were found with 3 species (4.4%), and thus the Colchicaceae family presented by a rate of 3% with two species. The Apiaceae, Aristolochiaceae, Crassulaceae, Oxalidaceae, Primulaceae, Ranunculaceae and Xanthorrhoeaceae participate in it by a low rate of 1.5% with only one species for each family.
The majority of species found in the study area are greatly presented in two places, namely Oued Djenan (28 species) and Brabtia (17 species), while the site Point of Chacal is the poorest site, containing just two species. Some species are widely distributed through the observation site and within the same site; this is the case of Drimia numidica (Fig. 4e) found in 24 sites with a frequency higher than 50 individuals per site, meanwhile others exist only in one site, case Moraea sisyrinchium (Djebel El Korsi), with a very low frequency (5 individuals). According to the global list of determined species, the composition of the global biological spectre (Table 1) showed that bulbous geophytes along with their 38 taxa (56.7%) were found to be predominant on the tuberous geophytes (29 taxa presenting 43.3%).
Phytogeographical diversity
The determined species belong to several chorological groups (Table 1):
Mediterranean set: this group dominates with 49 species, presenting 73.13% of the classified flora, including 26 species for the Mediterranean link element (sensu stricto), 11 species for the CircumMediterranean link element, 9 species for the Steno-Mediterranean link element, 2 species for the Euro-Mediterranean link element and 1 species for the Atlantic Mediterranean link element. In this set, the richest families are those of the best ones represented in the studied flora. The families; Orchidaceae, Amaryllidaceae, Asparagaceae and Iridaceae, respectively show 17 taxa, 12 taxa, 7 taxa, and 5 taxa, since other families may present 2 or 1 taxa.
Eurosiberian set: This set represents 5.97% of the studied flora (4 taxa), and it is represented by two European taxa (Colchicum autumnale L. and Gladiolus dubius Guss.), and two Eurasian taxa (Neotinea maculata (Desf.) Stearn and Gagea villosa (Parl.) Parl.).
Allocthonous set: This set includes only one taxa of Oxalidaceae (Oxalis pes-caprae L.) family.
Endemic set: It is important set in the studied flora, and it includes 13 species (28.35%). Noteworthy, the great number of species was recorded in five sites; each one contains 3 species (Bougous, Chemin des Oiseaux, Djebel El Korsi, Feid El Allag and Oubeira). The Mellah site is considered as a poor site. It contains just one species. It has been observed that the Asparagaceae family is the richest in endemic species (five out of twelve taxa), followed by the Orchidaceae with 3 species, Amaryllidaceae, Apiaceae, Aristolochiaceae, Araceae and Primulaceae with respectively one taxa.
The genus Hyacinthoides Heist. ex Fabr. is represented by two taxa; while the rest of the genera are monospecific.
Rarity
The studied flora counted 19 rare species. This important number would due to the habitat diversity, especially the cork oak forests Quercus suber L., which include several rare and/or endemic species, like Allium duriaeanum J. Gay and Romulea ligustica Parl. subsp. ligustica. The species do not usually have the same heritage value; meanwhile some of them are endemic and rare, such as Serapias stenopetala Maire & T. Stephenson and Aristolochia navicularis E. Nardi. Additionally, all these species are in the IUCN Red List (2017) along with different status (CR for S. stenopetala, LC for A. navicularis) (Table 2). Rare species of the region could be found in other countries, like the species of the northern element (Neotinea maculata) and the Mediterranean element (Allium commutatum Guss., Ophrys iricolor Desf.). Nevertheless, three species of this flora are protected according to the Algerian legislation (Executive decree N°12/03, 2012) providing the list of protected non-cultivated plant species): Anacamptis papilionacea (L.) R. M.Bateman, Pridgeon & M. W. Chase, Bunium crassifolium (Batt.) Batt., Cyclamen africanum Boiss. & Reut.
Canonical Analysis of Correspondences (CAC)
This analysis joins the 67 plant species and environmental variables. The outline drawn by the first and second axes has an inertia rate of 68.70% (Fig. 2). It evidenced the distribution of the sites as a function to the variables of the environment and the physiognomy of vegetation.
The two sites of marine fringes (R20 and R23) appear relatively isolated on the positive side of the axis 2, and are characterized by their height position. The site R20 occupies a sandy substrate, and is distinguished by the species Pancratium maritimum L. (X13). Although, the site R23 is linked to the maritime cliff of the town of Vielle Calle and is distinguished by the species Allium subvillosum Salzm. ex Schult. & Schult. f. (X9).
Sites (R1, R10, R5, R9, R28, R29, R7, R4, R8, R3, R6 and R13) are associated with five dominant factors of the negative part of the Axis 2: herbaceous cover rate (Trhe), tree cover lignified rate (Trli), slope and bulb overlap area. The altitude (Alti) also mediates for the Bougous site (331 MASL) and El Ghora (445 MASL), and so these two sites limit the distribution of two endemic species; Bellevalia mauritanica Pomel (X20) and Platanthera bifolia L.) Rich. (X58). These fourteen sites were found to include a great number of listed species.
The three sites R18, R21 and R2, containing Romulea bulbocodium (L.) Sebast. & Mauri (X37), Colchicum cupanii Guss. (X32), Arum italicum Mill. (X17) and Serapias stenopetala (X61) were found isolated, in relation to the Numidian sandstone substrates.
The thirteen sites (R24, R14, R22, R25, R30, R26, R15, R12, R11, R17, R19, R27 and R16) were found grouped, in relation with the NorthEastern exposure. They include the species linked to overgrazing as Asphodelus ramosus L. (X67), Ophrys bombyliflora Link (X47) and Ophrys tenthredinifera subsp. tenthredinifera (J.A. Guim.) M.R. Lowe et D. Tyteca (X56).
Typology of sites
The Linear Discriminant Analysis performed on a total of 30 sites and 7 environmental variables has evidenced the existence of an altitude gradient in the direction of axis 1 (Fig. 3). The plan made through the first and the second axes summarize an inertia rate of 84.94%.
The group ?G5? includes the two sites (R20 and R23), characterized by a variable substrate, and located in the maritime beach of the studied region.
The group ?G4? includes the six sites (R8, R10, R11, R12, R18 and R22), organized around a high rate of herbaceous associated with a weak representation of the lignified plants.
The group ?G1? contains two sites (R1 and R27), and it solely includes lignified species on calcareous substrata.
The group ?G2? stretch throughout the negative part of axis 2, and it is formed by two sites of medium and high altitude (R2, R3, R4, R5, R6, R13, R14, R15, R16, R17, R19, R21, R24, R25, R26, R28, R29 and R30). These sites are absolutely characterized by high rates of herbaceous and lignified, along with large areas of bulbous plants.
Lastly, the group ?G3? is constituted by two sites R7 and R9, and it occupies a ridge at high altitude. These two sites are characterized by high rates of lignified, and mainly by strong slopes (45%).
Discussion
Floristic composition
The inventory of bulbous and tuberous species at the El Kala National Park evidenced the presence of 67 taxa with specific or sub specific ranks. Three families (Orchidaceae, Amaryllidaceae and Asparagaceae) are principally represented within the inventoried area, and they are highly dominant in the monocotyledon flora geophytes of the Mediterranean basin (Parsons & Hopper 2003).
Moreover, the orchid flora of the studied area could be considered as quite interesting when compared with that obtained in region of Souk Ahras by Boukehili et al. (2018), who have estimated 27 species, and that reported by Hamel & Meddad-Hamza (2016), showing 20 species in Edough peninsula site, as well as the previous results of Martin et al. (2015), regarding 50 species recorded in Tunisia.
This dominance of orchids in the determined flora would be strongly related to edaphic and climatic factors, as indicated by de Bélair et al. (2005), Kreutz et al. (2013, 2014) and Hamel et al. (2017).
The First-order diversity is high in the other remaining families; they do not only present large number of species, but also a high family numbers (Daget & Gaston 2001). These results are concord with those obtained by the work carried out on the vascular flora of the Edough Peninsula by Hamel (2013), and the work of de Bélair (1990) on the vegetation of the lacustrine zones of El Kala National Park.
In this study, we have noticed the presence of a new species belonged to Algerian flora Ophrys fusca subsp. lupercalis (Fig.4a). Though, the species was indicated as widely distributed in the Mediterranean basin (Devillers & Devillers-Terschuren 1994), since the flora of Algeria (Quézel & Santa 1962-1963) and that of the North-Africa (Maire 1952- 1987) ignore its presence. This is alike to Tunisia flora (Le Floc'h et al. 2010). The recent literature works done on the North-Africa flora (Dobignard & Chatelain 2010) indicate probably the presence of the species in Tunisia.
Hence, El-Kala is believed to be a biogeographical crosslink for its fauna and flora (de Bélair 2005).
Additionally, the unexpected discovering of this species, too far from its classical sites of the western Mediterranean (Spain) (Blanca et al. 2009), auguring the existence of other populations, leading to searching within potential area of the populations.
The studied flora showed a set of heterogeneous biogeographical value, whose establishment in fact responds to the extreme palaeogeographical and paleoclimatic complexities of the Mediterranean region (Quézel & Médail 2003). Indeed, the Mediterranean element dominates with 73.13%, and this is in line with those reported by Quézel (1983), showing an increase in the Mediterranean species in the flora of NorthAfrica. Our study area includes 13 endemic species of rate 28.35%, as 17.1% of the regional endemic species of sector "K3" (Numidia) found in our study area. This percentage is higher than that given by Hamel et al. (2013) for the endemic geophytes of Edough Peninsula (3.8%).
Whilst, the Eurosiberian species exhibits a low percentage (5.97%), and it overall represents the remnants of a flora found in North Africa during the glacial periods, and it appears almost exclusively from the Iberian Peninsula (Quézel 1978).
Habitat diversity of the studied flora
The cork oak forest and lawns of the study area was found as rich in species, containing more than 40 species for each (Table 3), while the maritime cliffs and Zenaie oak include, respectively 12 and 11 species (poorest site), and that eucalyptuses occupy the intermediate position with 14 species.
These results confirm that the Numidia region (where indicate our site) and other areas, such as Kabylie and Kroumirie in Tunisia, presenting a high floristic richness, are classified as new hotspots, along with the ten other regional hotspots of Mediterranean biodiversity (Médail & Quézel 1997, Médail & Diadema 2006, Véla & Benhouhou 2007). As for endemism, it is the most common in the cork oak forests, with 9 taxa, followed along with Zenaie oak forests and lawns, respectively 5 and 3 species.
Eucalyptaie and sea cliffs are the poorest sites with 2 taxa for each, which explains that the floristic accompanying the cork oak forests possesses coping mechanisms throughout the summer dry season (nearly 4 months) that characterizes the Eastern Numidia (Bennadja et al. 2013).
In contrast, the distribution of the endemic species does not occur spontaneously. They were found in regions, whose flora has to do with the recent or previous geographical reasons (Boulos 1997, Verlaque et al. 1997). According to Barbéro et al. (2001), this richness of endemic herbaceous forests accounts for the variability of biogeographic,ecological states and the fragmentation of the continental areas in relation with anthropogenic actions.
Heritage Value of the listed species
The recorded flora was found to be very rich by endemic taxon (13 taxa), which are either endemic of the regional hotspots ?Kabylies-Numidia-Kroumirie? (Véla & Benhouhou 2007) or sub endemic of this sector with a supplementary separated area (Table 4):
Algerian-Tunisian endemics include six species: Allium duriaeanum, Bunium crassifolium, Hyacinthoides aristidis, Ophrys numida (Fig. 4h), Platanthera bifolia (Fig. 4g) and Serapias stenopetala (Fig. 4d). Véla & Benhouhou (2007) and Hamel et al. (2013) argue that these endemic borders with Tunisia correspond less to areas of specialized hyperendemism than to large areas of biogeography where endemic species are locally rare or even abundant.
Algerian-Tunisian/Spain endemics include mainly one taxon (Drimia numidica) which is commonly known in north-eastern of Algeria with less important distribution areas (Quézel & Santa 1962);
Maghreb endemics include three taxa: Cyclamen africanum (Fig. 4c), Hyacinthoides lingulata (Fig. 4b) and Bellevalia mauritanicae.
Algerian-Tunisian endemic, Boreal / Libya include only one taxa: Barnardia numidica.
Sub-endemics: include two taxa (Ambrosinia bassii and Aristolochia navicularis). The presence of endemic Tyrrhenian strain (2 taxa) could be explained by the terrestrial connections passed through the Algerian coast Tell with the Tyrrhenia (Quézel 1964, Hamel & Boulemtafes 2017).
Compared to the work of Hamel et al. (2013), carried out on the rare and endemic flora of Edough Peninsula, the endemic numbers found in our region could be considered as important, and showed about 17.1% of endemic flora of sector "K3", including 76 taxa (Véla & Benhouhou 2007). Nevertheless, two endemic plants are classified as typical species in the identification of Algerian ZIP (El Kala 1): Serapias stenopetala and Bunium crassifolium (Yahi et al. 2012).
The rare or threatened taxa amount to 19, as 28.35% of the studied flora. These rare species are therefore of great value and have a high value in terms of conservation, either for heritage reasons or because of their risk of extinction (Pimm et al. 1988, Gaston 1991, Hamel et al. 2013, Miara et al. 2017).
In fact, three recorded species are listed among the authoctonous and protected plant species, and three others are listed in the red list of IUCN (2017). This flora requires strict protection.
Mosaic of the studied vegetation
The plant mosaic of the studied area was found to be structured by three dominant environmental gradients; the rainfall, altitude and anthropogenic disturbances.
The habitat features are helpful to determine the plant distributions, and this is due to reason to their usually complex interactions with organisms (Gaston 1991). It seems that the precipitation abundance in the study area promoted the appearance of 38 bulbous species and 29 tuberous species, leading to population variation of every observed taxon.
The altitude determines the distribution of the observed species, since the low and the high altitudes are relatively poor in species, although average altitude stations were proved to be quite rich in floristic biodiversity. The presence of new populations of Allium commutatum in the maritime cliffs of Vielle Calle distanced 3 km from the first site ?Medjez Ecchair? (de Bélair et al. 2012), leads us to suggest that the other leek populations could be found in the western-coast, and even to the eastern of El-Kala city. The site of El-Ghora, distanced 820 m, is the highest one among our sites, and thus it is indicated as the sole site of Hyacinthoides aristidis and Platanthera bifolia. The later has already been indicated in the same site by de Bélair et al. (2005). This AlgerianTunisian endemic taxon was observed in Edough peninsula found in high maquis at 594 MASL, in Pinus pinaster Aiton forests (Hamel et al. 2013, Kreutz et al. 2014, Hamel & Meddad-Hamza 2016). Its presence on the Babor Mountain (North-Eastern of Algeria) with altitude of 1,935 MASL is being confirmed (Madoui et al. 2017).
Threats and conservation
As reported by Verlaque et al. (2001), the therophytes and the geophytes (bulbous and tuberous) are highly damaged either by the harvests or pastoral pressure. Indeed, the damages on the habitats are significantly high. These damages are frequently due to the humans and his expansion (flocks). According to Allem et al. (2017) these effects are direct, damaging habitats and species and they modified their groups of associated species.
The total elimination of pasturage in the longterm period, could lead to the removal of the environment and the development of competitive mono-specific communities (Belouahem et al. 2011), and this is not desirable.
Therefore, an integrated strategy for the conservation of threatened taxa or showing heritage interest must absolutely be based on a good knowledge of the auto-ecology and biology of rare species (Quézel & Médail 2003).
Conclusions
The results obtained reveal a high species richness (67 species), characterized by a relatively high rate of endemism (28.35%), a large number of rare, endangered and endemic species (19 species, 10 of which are rare to very rare) and a great biogeographical diversity, marked by the coexistence of elements of Mediterranean, Nordic, endemic and introduced origin.
This inventory allowed us to discover and refer new stations of geophytes by indicating a new species for the region in question (Ophrys fusca subsp. lupercalis).
In terms of conservation, it is necessary to recall the need to rapidly implement measures to protect the stations of the species observed in the study area, by announcing the degraded state of the bulbous habitats and to be concerned about threats to these plants, because indeed human activity modifies and restricts the environments in which the geophyte species develop spontaneously and thus jeopardizes the diversity of these taxa, for that a control of overgrazing and fires is necessary.
Finally, an important step must be taken in the protection of species. The lists of protected species need to be revised to include newly described taxa that are already in danger and those that are newly threatened.
Acknowledgements
The authors gratefully thank M. Boucheker Abdennour for the valuable assistance.
Received: 18 November 2018
Accepted: 13 March 2019
Published on-line: 8 May 2019
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Abstract
Treinta estaciones en el Parque Nacional El Kala (Noreste de Argelia) fueron objeto de un inventario florístico que se centró en el estudio de la ecología de geófitos bulbosos y tuberosos. La flora se caracteriza por una alta proporción de taxones raros y/o endémicos, entre ellos, 6 especies son endemismos algero-tunecinos pertenecientes a la familia Orchidaceae. En este trabajo, se da a conocer la presencia de una nueva especie para la flora argelina, Ophrys fusca subsp. lupercalis. Los análisis multivariantes revelaron, ciertas variables ambientales que determinan la distribución de los geófitos. Los lugares de interés son particularmente sensibles a las amenazas, particularmente las de origen antrópico.