Avifauna Diversity in the Gate between Humid Atlas and Saharan Desert: Midelt Province, Morocco

)e analysis of biological diversity at a regional scale is the first step to understand and classify the biological importance of a specific region and therefore the adoption of implementing conservation strategies.We conducted weekly bird counts by using the point count method from January 2015 to December 2017 in Midelt province, Morocco. A total of 130 bird species were observed, among breeding, migrant, and wintering species belonging to 42 families. Accipitridae (15 species), Muscicapidae (9 species), and Alaudidae (9 species) were the most observed families. Order of Passeriformes was the dominant order represented with 16 families and 68 species. Moreover, five species of conservation concern were recorded such as the vulnerable European turtle dove, houbara bustard, and Dupont’s lark; the near threatened ferruginous duck and bearded vulture; and the endangered Egyptian vulture. On the other hand, the results of the diversity analysis (Margalef index, Shannon–Wiener index, and Simpson index) showed the highest diversity in wetlands, forests, steppes, and farmlands, while cliff, landfills, and urban areas were the least diversified habitats. Finally, with its geographic situation between humid Atlas and Sahara desert, as well as the diversity of habitats and avifauna, Midelt region needs advanced analysis in terms of biodiversity and environmental characteristics, in order to provide effective conservation management.


Introduction
e study of biological diversity in a regional pattern is an important step in conservation management [1]. Patterns of geographic distribution, species boundaries, and differentiation taxonomy must be studied and defined for each species [2,3]. Site inventories must be conducted to determine regional levels of diversity and integrated into a regional view of spatial variation in diversity and endemism [4]. en, these patterns can be associated with physical and biological features of the environment to produce a synthetic understanding of determinants of biological diversity patterns [5]. However, this process is difficult in time and field, but the completion of such syntheses, particularly patterns of biological diversity, is crucial for both conservation measures and scientific knowledge regarding the process of biological diversification [6,7].
Morocco is situated in the Mediterranean Basin hotspot, one of Earth's biologically richest and most endangered terrestrial ecoregions [8,9]. Consequently, it hosts the second greatest concentration of animal and vegetation diversity in the Mediterranean Basin and the greatest marine biodiversity [10,11]. Morocco has a significant species diversity of more than 31.000 species of which about 11 % are endemic [12,13]. Morocco shelters approximately 500 bird species among them were breeders, migrants, and wintering species [5][6][7]. is species richness is the result of the diversity of Moroccan habitats [8,9], climate conditions [14], and geographical localisation. In fact, Morocco has 10 national/natural parks, including three that have marine areas within their boundaries, 38 RAMSAR wetlands, and 160 Sites of Biological and Ecological Interest (SBEI) [15] in addition to the Atlantic Ocean, the Mediterranean Sea, and the Sahara influence on the climate [16]. Morocco is the gate between Europe and Africa for many migrant bird species [17]. However, despite this richness and diversity, Moroccan ecosystems are less studied; several of them are under pressure and most are moderately-to-severely degraded. On the other hand, Midelt province was chosen due to its localisation between the humid Atlas considered as castle Morocco and Eastern Saharan Oasis installed in the Daraa-Tafilalet. Furthermore, Midelt houses the Isli, Tislit, and Agoulmame Sidi Ali RAMSAR wetlands [18,19], which are the least wetlands that can be used as a stopover site by migrant species before crossing the Sahara desert. e present contribution thus has two main objectives: (1) we present an inventory of the birds frequenting Midelt province in the high Moulouya plain and (2) we compare the richness and diversity of different habitats dominating this zone. erefore, the understanding of biological diversity in this unique area will be a first step to consolidate conservation strategies.

Study Area.
is study was carried out in the Midelt province, located in the Daraa-Tafilalet region between the Middle and High Atlas Mountains in the North of Morocco (32°40′47.57″N and 4°44′16.28″W), on an elevated plain with altitude ranging between 1300 m and 1500 m on sea level [20,21] (Figure 1). is area contains the last forests and lakes before the Saharan oasis of the desert. Moreover, the province is dominated by the high plain of Moulouya in the east and mountains in the Northwest and the South. e main irrigated crops are fruit trees (mainly apple trees Starking Delicious and Golden Delicious), fodder crops, and vegetables, while the main crops in rainfed farming are barley and wheat (Table 1).
e Midelt area is characterized by a cold arid climate (the annual average temperature and precipitations being about 29°C and 89 mm successively) with a mountainous tendency and the rainfall regime is marked by extremely variable and irregular low rainfall; stormy precipitation brings eroded products upstream. Sometimes the region receives snowfall.
In each site, we collected a number of data associated with the species richness and relative abundance of bird species. From January 2015 to December 2017, birds were surveyed and recorded during the breeding and wintering seasons by using the "point-counts" method with unlimited distance due to the wide area explored [22]. is is an effective method for sampling bird species [23] because it permits an extensive surveying of sample areas and the neighbouring landscape [24,25]. In addition, this method enables collecting a wide range of ecological data on species with cost-effectiveness [26]. During every single visit, which took around 12 hours to walk, from 06.00 to 18.00 hours, the numbers of species, as well as abundance seen and/or heard singing (mainly during the breeding phase), were recorded. Simpson index: lambda � sum{i � 1}^{R}p_{i}{2}, where S is the total number of species; N is the total number of individuals; pi represents the number of birds for species, i/ represents the total number of bird species. Moreover, the index of abundance was estimated as the relative size of an animal population calculated from counts of the number of individuals recorded in each habitat. In parallel, birds were divided into three groups including passerines, water birds, and raptors. e diversity indexes (Shannon-Wiener index, Margalef index, and abundance index) were calculated and compared for all habitats. Similarly, the species richness, families, and relative abundance for habitats and orders were calculated and compared by means of ANOVA (after assessing normality of variances, all data were parametric). Also, species were grouped in passerines, water birds, and raptors and compared via ANOVA during three years. All analyses were performed using SPSS 18 (SPSS IBM, 2009). Table 3 illustrates bird species diversity for the prospected habitats in Midelt province. A total of 130 bird species were recorded, including passerines (92 species), water birds (23 species), and raptors (15 species). ese species were belonging to 42 families. e most important families are Accipitridae (15 species), Muscicapidae (9 species), and Alaudidae (9 species), while Upupidae, Alcedinidae, Coraciidae, and Otididae are the less represented with 1 species for each ( Figure 2). On the other hand, Fringillidae are the abundant family with 280520 individuals. Similarly, the European serin represented by 105000 birds and Common Linnet with 81000 birds were the most abundant species, while the Egyptian vulture and bearded vulture were the less observed species. In addition, passerines were the most dominant species (Table 4) in comparison with water birds and raptors.

Avifauna Diversity.
In terms of presence status at Midelt, we recorded 98 breeding species, 24 wintering birds, and 57 migrants. In parallel, five species have been categorized by the IUCN as a species of conservation concern, including the vulnerable 2 International Journal of Zoology European turtle dove, houbara bustard, and Dupont's lark, the near threatened ferruginous duck and bearded vulture, and the endangered Egyptian vulture. e other birds (125) were a species of less concern conservation status.

Habitats and Distribution.
e results of diversity analysis (Margalef index, Shannon-Wiener index, and Simpson index) and compositional parameters (species richness) are shown in Table 5. Wetlands, forests, steppes, and farmlands were the highest diversity habitats in terms of species, while cliff, dumps, and urban were fewer divers' habitats ( Figure 3) (DF � 6, F � 2378.58, p < 0.001). On the other hand, farmlands and steppes were the highest abundant sites in terms of observed birds, followed by wetlands and forests. On the contrary, birds were less abundant in cliff, urban, and dump sites.

Discussion
Total species richness and habitat specific-birds-diversity (recorded in each habitat) showed that Midelt province avifauna diversity is important. Among the 42 families, Accipitridae, Muscicapidae, and Alaudidae represent 34% of recorded bird species. In an opposite pattern, Upupidae, Ciconiidae, and Oriolidae represent only 3% of recorded bird species. On the other hand, Passeriformes (with 16 families and 68 species) are the most dominant order (in terms of field abundance, species, and family levels) in Mountainous province, followed by Accipitriformes (one family and 13 species) and Charadriiformes (4 families and 6 species) (   concern, including the vulnerable European turtle dove (Streptopelia turtur) [33], houbara bustard (Chlamydotis undulata) [34], and Dupont's lark (Chersophilus duponti) [35]; the near threatened ferruginous duck (Aythya nyroca) [36] and bearded vulture (Gypaetus barbatus) [37]; and the endangered Egyptian vulture (Neophron percnopterus) [38]   International Journal of Zoology 5   International Journal of Zoology were observed regularly, which necessitate important and urgent research to characterise their habitats for effective conservation measures [39]. In wetlands, forests, steppe, and farmlands, the number of species, families, and abundance were higher in comparison to urban, dump, and cliff, which is in agreement with results reported by [40][41][42] and support the diversity of avifauna in forest, farmlands, and wetlands. e abundance of food resources, including water and nutrients in farmlands [31,43] and nesting-trees in forests [44][45][46], are the main reasons behind this diversity. In fact, the water availability (rivers, lakes, and dams) and feeding sources (cereals, wild seeds, and invertebrates) in wetlands, farmlands, and forests at the studied zone confirm this suggestion. e low avifauna diversity in urban and dumps sites is supposed to be controlled by human disturbance. In this point, it is known that bird diversity decreases with the urban gradient [47][48][49] due to increasing human disturbance in cities and buildings that reduce breeding opportunities and resources for bird species [50] which is in agreement with results reported in our study.

Conclusion
e Midelt province presents a variety of natural habitats, agroecosystems, and urban zones, which makes it a gate between the humid world and Saharan desert in Morocco. Midelt province needs a deep analysis in terms of biodiversity and habitat characterisation in order to orient and adopt effective conservation measures at least for the vulnerable habitats and threatened species.

Data Availability
e data used to support the findings of this study are included within the article.

Conflicts of Interest
e authors declare that there are no conflicts of interest regarding the publication of this paper.