Phytoecological study of a Biosphere Reserve in arid climate in Tunisia

Anthropic effects and global change threaten biodiversity and genetic resources. Thus, their conserva - tion becomes a primary necessity. This work aims to assess the conservation conditions for vegetation and causes that limit the progressive dynamics of the vegetation cover after a long period of defense. Using the quadrat point method, this work was conducted in two fenced zones and an unfenced zone of the Biosphere Reserve of BouHedma in a Tunisian arid climate. A total of 66 transects were inves - tigated. In each transect species richness and, a and b indices were determined. The a and b diversity showed a low similarity in family and species composition in the studied zones. The Poaceae and Aster - aceae families were the most representative in the studied zones and the most used for grazing. These results highlight that long-term conservation contributes to minimizing the reduction of biodiversity in the reserve. It is necessary to minimize grazing and deforestation, especially in the unfenced zone. Thus, the setup of barriers and fences is highly recommended to retain the soil. In addition, finding an effective communication plan with the local population and visitors seems to be crucial.


INTRODUCTION
Tunisia is located in northern Africa.According to Emberger (1955), the country ranges from the most arid to the wettest with five bioclimatic zones (Saharan, arid, semi-arid, sub-humid, and humid floor).The Biosphere Reserve of BouHedma represents the last ecosystem of the steppe of Vachellia (=Acacia) tortilis (Forssk.)Galasso & Banfi subsp.radiana (Savi) Kyal.& Boatwr. of the arid climate (Chaieb and Boukhris 1998;Jaouadi et al. 2013).This gum tree covered all southern Tunisia in Roman times, and its excessive exploitation was the cause of its scarcity from 1881 to 1986 (Jaouadi et al. 2013).The Biosphere Reserve of BouHedma constitutes a transition environment between semi-arid and desert vegetation in Tunisia (Schlesinger et al. 1990).It is a genetic and biological resource threatened by anthropogenic activities, mainly grazing and climatic pressure (drought), to which are added recent global changes (Floret and Pontanier 1982;Ouled Belgacem et al. 2013).The protection and conservation of natural habitats is becoming a global concern (Dupuy et al. 1999;Noumi 2010).Despite its positive impact on biodiversity, recorded in several regions, this protection had a negative impact on other, which recorded an increasing number of extinct or threatened species (Dupuy et al. 1999).In North Africa, defenses and grazing have been shown to cause degradation of steppe vegetation and hinder the reconstitution of major characteristics (cover, composition, and production) of pre-existing vege-tation from three to six years of defense (Bourbouze 1997).Studies of Abdallah et al. (2008); Ouled Belgacem et al. (2013) reported that heavy grazing make palatable species replaced by less desirable ones.Nevertheless, defending can turn out to be harmful, and can lead to a drop in productivity, the recovery and externalization of interspecific competition and a blockage of the biological recovery after more than ten years (Noumi 2010).The setting in defense (between five and 25 years) has a beneficial effect on the vegetation cover (Foudil et al. 2015), and allows a return to formations with high wealth, but with lower pastoral value compared to plantations (Amghar et al. 2012).In this context, this work aims to assess the effect of the protection of the Biosphere Reserve of BouHedma on its biodiversity, after 40 years of conservation.Two objectives were set for this work: (i) to determine species composition and (ii) to study a and b diversity among different zones of the Biosphere Reserve of BouHedma.

Study area
The Biosphere Reserve of BouHedma (BRB) is a part of the South Eastern Saharan Atlas (Orbata chain) with a total area of 16488 ha (Noumi 2010), located in both the Gafsa and Sidi Bouzid Governorates.According to Karem et al. (1993), the BRB includes three fenced zones: Borj Bou-Hedma (BBh.) on the east side, the Corridor (Co.) in the center, and Haddej (Ha.) in the southwest.In 2011, over-

RESUMEN
Los efectos antrópicos y el cambio global son una amenaza para la biodiversidad y los recursos genéticos.Así, su conservación se convierte en una necesidad primordial.El objetivo de este trabajo es evaluar las condiciones de conservación de la vegetación y las causas que limitan la dinámica progresiva de la cubierta vegetal tras un largo periodo de defensas.Este trabajo se realizó en dos zonas cercadas y una zona no cercada de la Reserva de la Biosfera BouHedma en el clima árido de Túnez, utilizando el método de punto cuadrado.Se investigó un total de 66 transectos.En cada transecto se determinaron la riqueza de especies y los índices de similitud y diversidad.La diversidad a y b mostraron una baja similitud en la composición familiar y de especies en las zonas estudiadas.Las familias Poaceae y Asteraceae fueron las más representativas en las zonas y la más utilizada para el pastoreo.Estos resultados destacan que la conservación a largo plazo contribuye a minimizar la erosión de la biodiversidad en la reserva.Es necesario minimizar el pastoreo y la deforestación especialmente en la zona no cercada.Así, se recomienda encarecidamente la instalación de barreras y cercas para retener los suelos.Además, encontrar un plan de comunicación eficaz con la población local y con los visitantes parece ser fundamental.
grazing occurred in the corridor that now has become an unfenced zone (personnel observ.).Thus, investigations were conducted in two fenced zones (zone I, Borj BouHedma and zone II, Haddej) and an unfenced zone III, the corridor (Fig. 1; Table 1).BBh. and Ha. are protected by fences against anthropic activities and grazing.These two zones are linked by the Co. located in the neighboring pastures and heavily grazed by herbivores, mainly sheep and goats (Abdallah et al. 2008).
The region is characterized by an arid Mediterranean climate with moderate winter (Emberger 1955).The average annual rainfall is 180 mm on the plain and 250 mm on the mountain crest.The average temperature varies from 32° to 36°C in summer and from 4° to 7°C in winter (Floret and Pontanier 1982).

Methods
Surveys were carried out over three years, during the periods of full plant growth (March and October 2018; April and December 2019; January 2020).We used the quadrat point method, according to Daget and Poissonet (1971).
Each transect consisted of a straight line 50 m in length and 1 m in width (50 cm on the left and 50 cm on the right side of the line).This protocol was used to consider all plant species to the left and to the right of the transect.In each transect, the total number of plant species was determined and identified using Maire et al. (1955), Ozenda (1977), and Pottier-Alapetite (1979, 1981) keys.The soil map (Fig. 2) was produced using ArcGis software (10.3.1) based on data from the agricultural map of Sidi Bouzid (2003) available from the General Direction of Forests.

Plant community structure
In order to define the important role of the protection in the conservation of this ecological heritage (BRB), a comparison among the three zones using biodiversity indices was used.

Relative frequency
The relative frequency was used to check the homogeneity of the studied sites.It was calculated according to the formula: F % pi P* ( )= / 100; pi=the number of transects with the species observed, P=66 (total number of transects).

Beta diversity
The Jaccard index (1901) was used to determine the similarity between the three zones with ; where a is the number of common species between two zones; b is the number of species specific to the first zone; and c is the number of species specific to the second one.This index varies from zero (specific richness is low) to one (a significant number of species are found in both zones).

Alpha diversity
The Alpha diversity was calculated per transect and then means per zone.The Shannon and Weaver (1948) index was calculated to establish the specific diversity.
where pi is the proportion of the total sample belonging to the species in the same zone.H varies between zero (a single species) and S (number of species; 109, 23 or 41).This index represents a measure of the species composition of an ecosystem including rare species, considering their distribution and relative occurrence; it is usually referred as diversity.
The distribution of occurrences was calculated according to the Pielou (1966) formula: E H Hmax = / .
With Hmax = ln (S).This index varies between zero and one (0 all the numbers are concentrated on one species; 1 all the species have the same occurrence).
The Simpson diversity index does not consider rare species.The Simpson diversity (1949) index was calculated to measure the dominance of a species, expressed as 1-D; ) ; where Ni is the occurrence of individuals of a given species and N is the total number of individuals.D varies between zero (maximum diversity) and 1 (minimum diversity).

Statistical analysis
The statistical analysis was performed using the SPSS-

Richness of the Biosphere Reserve of BouHedma
In the three study zones, 115 species belonging to 93 genera and 41 families were identified.Among these families, The a and b diversity among zones of the Biosphere Reserve of BouHedma The Jaccard index (b diversity) varied between 0.189 and 0.316 (Table 3).Statistical analysis showed a non-significant difference of H and D indexes among the three zones with (F (2, 63) =2.629, P=0.08) and (F (2, 63) =3.022, P=0.056), respectively.Nevertheless, Pielou evenness index was significant (F (2, 63) =4.127, P=0.021).For the a diversity, the BBh.zone was the most diverse showing a Shannon and Weaver index of 3.922 bits, a Simpson diversity index of 0.970 and a Pielou evenness index of 0.836.However, the least diverse was Ha. with 2.190, 0.706 and 0.811, respec-tively (Table 3).A highly significant Pearson's correlation coefficient was observed between species richness and altitude (R 2 = 0.36, p=0.003), while it was significant between species richness and longitude (R 2 = 0.58, p=0.037).

DISCUSSION
The severe natural conditions (drought, lack of rainfall, and high temperature during summer) in BRB have made it a very particular landscape (Schlesinger et al. 1990).Although, the three zones of the BRB differ floristically but some species occur in two or all three zones are similar.
The three study zones share nine families: Apiaceae, Asteraceae, Chenopodiaceae, Cistaceae, Fabaceae, Lamiaceae, Poaceae, Solanaceae, and Zygophyllaceae.The b diversity among the three zones was low in the families and species composition.In fact, 23 families were represented at least by only one species.Three families were represented by eight to ten species.Poaceae was the richest family with 21 species: 19 species in BBh., 8 species in Co. and 4 species in Ha.These results are consistent with those found in southern Senegal (Cornet and Poupon 1977) and in the wooded savannah of Côte d'Ivoire (Mitja and Puig 1990).According to these authors Poaceae tolerates high temperatures, resists drought and grazing.In addition, the work of Le Houérou (1986)   In the corridor, Vachellia tortilis colonizes erosion claws and wadis and compete with other plant species.It exerts an allelopathic effect inhibiting the natural germination of the seeds of competing species and consequently the evolution of herbaceous and woody trees (Noumi 2010).Nevertheless, the corridor is located at an altitude of 200 m and characterized with the limestone glacis and wadis with a complex substrate (silt, rocky and sandy).In this zone, the Poaceae family is represented by 10 species able to resist to deforestation and overgrazing.The Lamiaceae family, known for its aromatic and medicinal virtues (Lardry and Haberkorn 2007), occupies the three study zones; it is represented by 10 species in Borj BouHedma, 3 species in Haddej and 5 species in the corridor.The common species among the three zones are Teucrium polium L. and Salvia aegyptiaca L. These two species are the most resistant to the ecological conditions in the region (Ozenda 1977).
Marrubium deserti (de Noé) Coss., a species characteristic of stony plains (Regs) (Bouallala 2013), was only found in Haddej, where the Gum tree is more frequent than in the two other zones.(Chedli et al. 2016).The occurrence of this species is maybe due to its spreading by these herbivores.In fact, works of Neffati (1994) demonstrated that the occurrence of certain species is probably due to their germination stimulated by grazing.
This result is in concordance with that of Abaza and Hanafi (2018) who found these three species in the sandy environ- ment of Mednine in southern Tunisia.The diversification of the Chenopodiacae family in Borj BouHedma is mainly due to the depth of the soil, the absence of watercourses and the salinity of the soil.
This result is consistent with that of Boughani et al. (2009) in the Ghouffi gorges, near Biskra in Algeria (North Africa).Indeed, the limited area of Haddej and the sandy nature of the substrate and the low altitude make this environment different from two others.The Borj BouHedma area is characterized by different reliefs of a diverse substrate nature and streams making this environment favorable to host many families and species.

CONCLUSION
This work deepens our knowledge concerning the restoration of threatened ecosystems.It allowed a data updating of the state of conservation of the BRB.Cigolani et al. (2005) found that the increase in grazing pressure can lead to a reduction in palatable species, which is the case for the corridor, an area subject to free grazing and considered to be the most threatened.To better conserve the flora of the BRB, it would be important to minimize grazing and deforestation, especially in the corridor.It is essential to install barriers to retain the soil, and a fence to minimize grazing.It is also fundamental to build a communication plan with the local population and visitors to explain the importance of this BRB.Additional works are required with an exhaustive inventory of the vegetation to allow a precise monitoring of the long-term protection impact on the restoration of this heritage.In addition, implementation of policies for the protection and restoration of this threatened ecosystem is needed.

Figure 1 .
Figure 1.Localization of the Biosphere Reserve of BouHedma 20.0 software package for Windows.Average of a diversity (H, Pielou evenness and 1-D) was statistically evaluated by using analysis of variance (ANOVA) and complemented by multiple comparisons of means by Duncan test.Pearson's correlation coefficient was tested between species richness, altitude, longitude, and latitude.The two-proportion z-test was used to compare species frequency per zone.
in North Africa confirms that Chamephytic steppes protected for a long time (> 4 years) have contributed to the expansion of this family.The a diversity represented by the Shannon and Weaver index varied among zones, the lowest was recorded at Haddej.The Pielou evenness was low in the BRB.On one hand, the index was high in BBh.(0.836) showing the occurrence of different species in this zone.On the other hand, it was low in Co. (0.706) and in Ha. (0.698) indicating evenness in the distribution of species.The Simpson diversity index showed minimal diversity in the three zones.This difference is probably linked to the geology characterized by the presence of plains, glacis, and wadis in Borj BouHedma, also to the diversity of the soil texture (sand, silt, and gypsum) and to the altitude (173 m).However, Haddej is composed by a simple relief (plain), a sandy soil and a low altitude (114 m).In addition, the occurrence of Vachellia tortilis is greater in the region of Haddej than that of Borj BouHedma, which gives a landscape of wooded savannah in Haddej and a complex landscape in Borj BouHedma(Tarhouni 2003).

Figure 2 .
Figure 2. Edaphic characteristics of the Biosphere Reserve of BouHedma.a. depth; b. texture *Numbers from 1 to 66 indicated in figures a and b represent the transects

Table 2 .
Flora diversity expected by relative frequency (%); BBh.Borj BouHedma (43 transects), Ha.Haddej (9 transects), Co. corridor (14 transects) Atractylis serratuloides characterizes degraded environment and occupies the old facies of Lygeum spartum L. (Kadi Hanifi 2003), which explains its presence in the overexploited zone by grazing.Haddej is a zone of accumulation of fine mobile sands and is occupied by Rhanterium suaveolens Desf., Atractylis serratuloides and Artemisia campestris L. According to Abdallah et al. (2008) and Ouled Belgacem et al. (2013), Hammada scoparia (Pomel) Iljin, Salvia aegyptiaca, Astragalus armatus Willd., Pergularia tomentosa L. are not used for grazing.Contrariwise, Cenchrus ciliaris L. is abundant in the three zones of the BRB and grazed by Oryx dammah, Addax nasomaculatus, Gazella dorcas, Cten-Odactylus gundi, Jaculus deserti The two threatened species Lavandula coronopifolia Poir.and L. multifida L. are found in Borj BouHedma and the corridor, with a very low density and are absent in Haddej.Ballota hirsuta Benth.has been observed only in the Borj BouHedma.Its presence characterizes wadis and high altitudes (> 120m).Teucrium ramosissimum Desf.was weakly dense or even very rare and was found in Borj BouHedma (only one tree).The two Asteraceae, Artemisia herba-alba Asso and Atractylis serratuloides Sieber ex Cass.were encountered in the corridor.Indeed, A. herba-alba is widely distributed in pre-Saharan Tunisia and occupies a silty soil.