Large-Scale Monitoring of Bird Communities along an Altitudinal Gradient in Two Central High Atlas Valleys

Mounir, Mohamed; Dakki, Mohamed; Douini, Ikram; Benka, El-Mostafa; Nouri, Ayoub; Mansouri, Ismail; Hammada, Soumaya

doi:https://doi.org/10.1155/2024/8873008

International Journal of Zoology

On this page

Abstract Introduction Materials and Methods Results Discussion Conclusion Data Availability Conflicts of Interest Acknowledgments Supplementary Materials References Copyright Related Articles

Research Article | Open Access

Volume 2024 | Article ID 8873008 | https://doi.org/10.1155/2024/8873008

Large-Scale Monitoring of Bird Communities along an Altitudinal Gradient in Two Central High Atlas Valleys

Mohamed Mounir,¹Mohamed Dakki,²Ikram Douini,¹El-Mostafa Benka,¹Ayoub Nouri,¹Ismail Mansouri,³and Soumaya Hammada¹

Academic Editor: Edson Gandiwa

Received26 May 2023

Revised26 Feb 2024

Accepted06 Mar 2024

Published14 Mar 2024

Abstract

Altitude is one of the determinant factors that influence the spatial distribution of birds and their species richness. However, few investigations studied its influence on African bird communities over a wide gradient in North Africa. Considering this knowledge gap, 194 sampling points were carried out along altitudinal gradient (773 to 2595 m) in two adjacent mountainous valleys in the Central High Atlas of Beni Mellal in Morocco, Aït Bouguemmaz (AB), and Ahançal (OA). Each valley was divided into three altitudinal intervals (low, medium, and high zones). For each spatial subdivision, we studied the phenological cycle, in the sense that each valley underwent a four-season monitoring, during 2018 and 2019. The results showed 131 species in the study area in 43 families; both valleys had similar community richness, but they differed by the phenological status of their species. Indeed, the increase in altitude led to a decrease in bird species richness, while it does not show any correlation with abundance. In addition, richness and abundance increased during the high-productivity seasons (i.e., spring and summer). Although these results were expected, they provide an opportunity to compare these results with higher latitude communities in Europe and to better focus future large-scale investigations on the combined influence of latitude and altitude on birds.

1. Introduction

Biological diversity has become a matter of high global concern, mainly in regions with high biodiversity [1], due to high human and climate pressures. In the Mediterranean region, Morocco is well known for the high richness of its flora, fauna, and habitats [2–4]. This richness is due to the high diversity of country landscapes, as they vary from Saharan ecosystems to high mountainous ones and include some 3,500 km of marine coast [5–7]. This diversity is well evidenced by both vegetal and animal communities [2, 8, 9], among which birds are excellent indicators of habitats’ health [10–12]. However, this group is still poorly studied in the high mountains of Morocco, in comparison to low altitudes, where several studies have been carried out in forest ecosystems [13, 14], wetlands [15, 16], and man-made landscapes [17]. Indeed, Moroccan mountain ecosystems have received little attention, despite their large extension from the Mediterranean coast to the Southern hamada and desert [18–20].

Bird distribution is influenced by several factors, including altitude [21–23]. Through its influence on the climate features [24, 25], altitude determines the zoning of habitats along the elevational gradient, mainly influencing the vegetation cover [26–28], with consequences on the vertical distribution and abundance of avian species [29–31]. This affects the shifting of the breeding phenology of the species which are distributed along a wide altitudinal range, following the availability of foraging resources [32]. Generally, birds shift their arrival, breeding, and departure dates in highlands to avoid the harsh weather conditions [33–36].

In the Mediterranean area, the effect of the altitudinal gradient on avian communities was largely addressed on the European side, where studies have demonstrated that species diversity declines with increasing altitudes due to the influence of climate and decreasing temperatures that affect productivity, a key factor driving the variations in species richness [37, 38]. In Morocco, few investigations targeted the impact of altitude on mountain bird communities, which in turn indicate a decrease in species richness with increasing altitude: Cuzin [39] in the Western High Atlas, Mounir et al. [20] in the Central High Atlas, Mansouri et al. [36] in the Middle Atlas, and Qninba et al. [40] in the Anti-Atlas.

The present study aims to specifically analyse the variation of avian communities according to altitude in the Central High Atlas (Morocco) during the entire year. This approach is supposed to give new insights into the spatiotemporal patterns of the mountainous bird communities in an important biodiversity hotspot in North Africa.

2. Materials and Methods

2.1. Study Zone

Our research was conducted in the valleys of Oued Ahançal and Aït Bouguemmaz located in the Central High Atlas of Morocco in M’Goun Geopark and designated as Ramsar sites [41, 42] (Figure 1). The study area is located between an altitudinal range of 800 and 2600 m above sea level being characterized by a warm and temperate climate with an average annual temperature of 15°C [43] and high variations (500–800 mm per year) in rainfall throughout the year [44, 45]. The valleys are known for their rich and complex hydrographic networks including rivers, springs, and lakes [41, 42]. The most important rivers are those of Oued Ahançal and Lakhdar-Aït Bouguemmaz whose flows are primarily determined by several permanent springs and tributaries, as well as some creeks that are heavily influenced by seasonal rainfall and snowmelt.

The landscape of both valleys comprises forest formations of broad-leaved and coniferous trees, high-mountain vegetation, and agricultural areas, which depend on the elevation level. The Ahançal Valley is known for its abundance of water resources, the limited expansion of agricultural areas, and the predominance of its forest ecosystems. Notably, Tetraclinis articulata, Quercus rotundifolia, and Juniperus phoenicea dominate the low-altitude section between Bin El Ouidane lake and Tilouguite village. Tamga forest at medium altitudes comprises woodlands of Pinus halepensis mixed with Juniperus phoenicea, along with woody shrubs such as Buxus balearica and Pistacia lentiscus, with Populus nigra forming the riparian vegetation [46]. In the high-altitude section of the valley, Juniperus phoenicea prevails, accompanied by shrubs of Buxus balearica, and Salix sp. dominates the riparian vegetation in Zaouiat Ahançal and Taghia villages.

In Aït Bouguemmaz, from Agouti to Zaouiat Oulmzi village, the valley bottom is dominated by agricultural lands including apple orchards, walnuts, and cereals [47, 48]. The riparian vegetation is dominated by Salix sp., while the foothills of the valley are covered by juniper woodlands Juniperus phoenicea and Juniperus thurifera [49]. In high altitudes above 2200 m, from Zaouiat Oulmzi to Izourar Lake, steppic formations of xerophytic plants colonize the rocky slopes of the mountains [50].

Before starting our field investigations, we divided the study area into three altitudinal sections (Table 1). This altitudinal division was based on topographic features, bioclimatic stages, and an upstream-downstream sectorization of each studied valley [51–53].

2.2. Data Collection

To investigate the avifauna distribution and diversity, we adopted the point-count method with unlimited distance [54, 55] for terrestrial birds. The surveys were carried out during 2018 and 2019, in both breeding and nonbreeding seasons. A total of 194 sampling points were selected in both valleys (120 points in Oued Ahançal and 74 points in Aït Bouguemmaz). For each point, all birds seen or heard were recorded for 10 to 20 minutes and within unlimited distance around each sampling point [56, 57]. We located points 300 meters to 1 km apart from each other to avoid double counting. During the breeding season (March to June), the surveys were carried out within the first five hours after sunrise and in favourable weather conditions, knowing that this period corresponds to the maximum vocal activity of breeding birds. During the nonbreeding seasons (July to February), we extended the survey into the evening, just before sunset. For waterbirds (in Bin El Ouidane reservoir and Izourar lake), we proceeded by exhaustive counts. Species were identified using binoculars or vocal characteristics, while waterbirds were sometimes counted using a spotting scope. We boosted our surveys using other counting techniques to increase bird detectability, especially during the nonbreeding seasons when most species become less detectable and difficult to hear. In order to increase the chance of detecting birds, including secretive species (e.g., moorhens, rails, and wetland songbirds), nocturnal species (e.g., owls and nightjars), and rare birds, we used a mini Bluetooth speaker during the count period of the point count as a playback method [58, 59]. This device was specifically employed within dense habitats and submerged vegetation along the river’s edge, and it was used carefully to minimize the disturbance without affecting bird’s behaviour [60]. In addition, for the need of precise identification, we used a high shooting speed camera with a telephoto zoom lens and a sound recorder for later identification of unrecognized bird calls. For each observation point, the altitude and geographic coordinates were determined using an Android GPS tracker.

2.3. Statistics

For each valley, we recorded the species with their phenological and conservation statuses, and we estimated the representativity of families, in terms of the number of species and abundance. Then, we calculated diversity indices (Shannon–Wiener and Equitability) in each valley. Based on these parameters, we compared communities of the two valleys, using the independent samples t-test and the diversity of seasonal avian assemblages, using the ANOVA one-way test. This same method was also used to compare bird richness and abundance at fixed altitude sections. To evaluate the relationship between altitudinal gradient and both avian richness and abundance, we used a simple linear regression model, where altitudinal sections (ranges) were considered as the independent variable (Factor), while avian richness (number of species per altitudinal section) and population size (abundance of recorded species in each altitude section) were considered as dependent variables. To evaluate the spatiotemporal variation of distribution among studied species, we considered seasons (n = 4) and altitudinal sections as independent variables (factors) and the population sizes of avian species (n = 131) as dependent variables. Then, the data were analysed by factorial correspondence analysis (FCA) [61] using the first two axes. Analyses were carried out in SPSS 21 [62], and significant values were considered at , while graphs were generated using GraphPad prism 8.3.0 [63].

3. Results

3.1. Status, Richness, and Abundance of the Avian Assemblages

During the two years, we recorded 131 bird species in both valleys, belonging to 43 families and 19 orders. Families with the highest richness were Muscicapidae (16 species), followed by Fringillidae (10 species) and Accipitridae (8 species). In contrast, Phalacrocoracidae, Meropidae, Coraciidae, Caprimulgidae, Upupidae, and Podicipedidae had the lowest richness, with one species each. Passeriformes recorded the highest richness, with 78 species, while the Suliformes, Caprimulgiformes, Bucerotiformes, and Ciconiiformes were the less diverse avian orders, with one species each (see Table 2).

Concerning the phenological status of the species, 104 of the recorded species are breeders in Morocco and 27 others are strictly visitors. Among the breeders, 72 species (69%) are residents, with five of them also being breeding migrants and/or passage migrants, with potential winterers, and 23 others are also winterers. The 32 other breeders (31%) are migrants, with passage visitors for nine of them only. Among the 27 strict visitors, seven only are strictly winterers and 20 are passage migrants, 11 of them having also wintering contingents (Figure SM A).

The most abundant species was Fringilla coelebs (4062 individuals), followed by Cyanistes teneriffae, Pyrrhocorax graculus, and Pycnonotus barbatus, with 1379 to 1093 individuals. High abundances were also recorded for seven species (Serinus serinus, Passer domesticus, Pyrrhocorax pyrrhocorax, Ptyonoprogne rupestris, Turdus torquatus, Apus pallidus, and Columba palumbus) (Figure SM B), while 101 species cumulated medium and low abundances (3–500 individuals) and 19 species were considered as accidental with 1-2 individuals (Figure SM C). Four species of conservation concern were recorded: two species are globally vulnerable (Streptopelia turtur and Aythya ferina) and two others are near-threatened species (Lanius senator and Turdus iliacus).

The independent samples t-test showed significant differences in terms of species abundance between the studied valleys (Table 3). In contrast, they were similar in terms of species richness, number of families, orders, and species of conservation concern. In addition, the phenological status varied between the two valleys in terms of resident breeders. However, breeding migrants, passage migrants, and winter visitors were not statistically different, even though Ahançal receives a higher number of visitors during migration periods, and Aït Bouguemmaz has more breeding migrants. Concerning diversity indices, no significant difference was observed, neither for the Shannon index nor for the equitability index.

3.2. Seasonal Variation

Seasonal variation of avian diversity in both studied valleys is displayed in Figure 2. The seasonal monitoring showed that the species richness in Oued Ahançal was significantly higher in spring (76 species), and summer (77 species) compared to winter (71 species) and autumn (54 species). The abundance was significantly higher in spring (4553 individuals), followed by autumn (3342) and winter (3187), while the summer season showed the lowest abundance (2861). Similarly, the species richness was significantly higher in summer (58 species) and spring (64 species) in Aït Bouguemmaz, compared to winter and autumn (47 and 42 species, respectively), while abundance was higher in spring (2405) and winter (2119), but that was lower in summer (792) and autumn (657).

Our comparative analysis with the ANOVA test did not show any significant differences in species richness in the Ahançal Valley (F3.271 = 0.9514, ) nor in species abundance (F3.271 = 0.5984, ). This suggests that the number of observed species and their abundance do not vary significantly from one season to another in this valley. However, in the Aït Bouguemmaz valley, the analysis revealed a difference in species richness between seasons (F3.132 = 8.244, ), while species abundance showed no difference (F3.132 = 0.3055, ).

3.3. Altitudinal Variation

The altitudinal variation of avian diversity in both studied valleys is presented in Figure 3. In Oued Ahançal, species richness was significantly higher in low altitudes (downstream part of the valley) compared to habitats of medium and high altitudes. In contrast, a higher abundance was recorded in high habitats (upstream part), followed by habitats of medium altitudes, and lowlands. In Aït Bouguemmaz, species richness was significantly higher in low altitudes (downstream part) compared to medium and high-altitude habitats, similar to Oued Ahançal Valley. However, the abundance of recorded species was significantly higher in low altitudes compared to medium and high altitudes.

The ANOVA test showed highly significant differences between the altitudinal sections for species richness (Ahançal: F2.117 = 6.234, ; Aït Bouguemmaz: F2.71 = 13.24, ) and for species abundance (Ahançal: F2.117 = 10.89, ; Aït Bouguemmaz: F2.71 = 8.895, ). This suggests that both species richness and abundance of birds vary significantly along the altitudinal gradient in the two studied valleys.

In both valleys, the species richness revealed a significant negative correlation with the increasing altitude, while no significant correlation was shown for the abundance (Figure 4 and Table 4).

3.4. Spatiotemporal Distribution

The distribution of avian species following altitudinal sections and seasons is presented in Figure 5. The first two axes of the FCA diagram accounted for 39.23% of the total variance. The first axis (explained by 20% of the variance) separated two groups of birds at the apex of the parabola (G2 and G3). The group (G3) includes species that are more commonly found at very high altitudes during the summer season, principally Sylvia conspicillata, Rhodopechys alienus, Oenanthe hispanica, Anthus campestris, and Monticola saxatilis. Group (G2) comprises species recorded with higher abundances at high altitudes during the spring and autumn seasons, especially passerines (Saxicola rubetra, Ficedula speculigera, Sylvia cantillans, Sylvia communis, Luscinia megarhynchos, Serinus serinus, Regulus ignicapilla, and Turdus merula), birds of prey (Falco tinnunculus, Falco naumanni, and Accipiter nisus), and others (Upupa epops, Gallinula chloropus, and Spilopelia senegalensis). The second axis accounted for 19.24% of the variance, ordering avian species along an altitudinal gradient, forming a continuum from low to high altitudes showing a distinction of two groups at both ends of the scatterplot (G6 and G1). The group (G6) comprises winter visitors that visit low altitudes in this season, including ducks, shorebirds, and other waterbird species (Anas acuta, Anas crecca, Aythya ferina, Spatula clypeata, Podiceps nigricollis, Gallinago gallinago, Fulica atra, Tringa ochropus, Phalacrocorax carbo, Egretta garzetta, and Circus aeruginosus). The other group (G1) contains species that inhabit high-altitude habitats during winter, including winter visitor passerines such as Fringilla montifringilla, Turdus iliacus, and Turdus torquatus. The groups (G4 and G5) include species found at lower and medium altitudes, which are predominantly observable during spring, summer, and autumn, counting Acrocephalus baeticatus ambiguus, Hippolais polyglotta, Iduna opaca, Oriolus oriolus, Tchagra senegalus, Spinus spinus, Motacilla flava, Coturnix coturnix, and Oenanthe oenanthe. On the other hand, the middle of the diagram shows ubiquitous species such as Fringilla coelebs, Chloris chloris, Emberiza cia, and Columba livia, which occurred indifferently in all altitudinal sections and seasons.

4. Discussion

Here, we presented a pioneering contribution to the elucidation of avian diversity in the central regions of Morocco, where comprehensive investigations into mountain biodiversity are notably scarce. We integrated bird richness and abundance, and spatiotemporal distribution to examine avian zonation across altitudinal ranges in two Valleys of the Central High Atlas. Furthermore, this study provides new data on avian diversity and altitudinal zonation in mountainous habitats of global interest.

Our seasonal monitoring endeavours revealed that the Central High Atlas valleys of Morocco host an important avian diversity. In fact, 131 bird species were recorded in both studied valleys of Aït Bouguemmaz and Oued Ahançal, which represents nearly 23% of the total recorded species in the entire Morocco. This diversity is very similar to that mentioned in Moulouya valley between High Atlas and Middle Atlas of Morocco with 130 species [36] but higher compared to the 85 bird species recorded in the valley of Oued Bouhellou in the Eastern Middle Atlas [64], and 90 species recorded in Sefrou Mountains [65] and in other regions in Algeria: 78 species in Machroha Forest northeastern part and 71 species in Merine forest, north-west of the country [66, 67]. However, it is still lower than the diversity mentioned in other areas in Europe such as a Mediterranean semiarid region in Murcia (SE Spain) with 339 species recorded [68].

The most relevant findings are the records of the globally threatened species, such as the vulnerable Streptopelia turtur and Aythya ferina and the near-threatened Lanius senator and Turdus iliacus. Streptopelia turtur is widely recorded in central Morocco, counting Beni Mellal, in the High Atlas as a summer breeder [17, 20, 35]. Turdus iliacus is a regular winter visitor, typically found in moderate numbers across the Tangier Peninsula, Central Plateau, and Western Middle Atlas. Generally scarce and irregular further east and south, however, during some winters, it is more common in High Atlas valleys up to 2000 m above sea level [9, 69]. Concerning Aythya ferina, this is the first record in this high-altitude zone, but it was previously recorded in human-made reservoirs in the plain [16, 70]. These findings emphasize the need for immediate and thorough research to characterize their habitats in order to implement successful conservation strategies.

Both studied valleys are similar in terms of species richness, number of families, orders, and species of conservation concern, since both ecosystems are located in the same mountainous chain of the High Atlas [43, 71]. In contrast, species abundance and the phenological status of recorded birds were variable between valleys, with a higher number of resident breeders and winter visitors in Oued Ahançal compared to Aït Bouguemmaz Valley. This variation is governed by the features of the studied valleys. In Oued Ahançal, the higher numbers of winterers and resident breeders were closely related to the presence of aquatic ecosystems (springs, rivers, and the reservoir of Bin El Ouidane) and forest stands (mainly Pinus halepensis, Juniperus phoenicea, and Populus nigra) which are known for their roles in supporting European migratory birds during winter in Morocco, as well as providing foraging resources and nesting sites for local bird species that breed in forest ecosystems [20, 72]. In contrast, the existence of sparse and degraded juniper stands as well as the domination of agroecosystems in Aït Bouguemmaz [49, 73], such as apple orchards and cereals are suggested to influence negatively the diversity of birds because of the reduction of breeding and foraging resources which are considered necessary elements for birds. In addition, the concentration of human habitations and the agricultural activities such as the use of pesticides in agricultural fields affect the abundance and diversity of many passerines such as Turdus merula and Serinus serinus [36, 74–76].

This study showed a seasonal variation of avian diversity between both valleys of the Central High Atlas, which was one of the neglected aspects of avian diversity studies in the High and Middle Atlas Mountains of Morocco, as well as in the entire North Africa [20, 64, 76].

In terms of species richness, the higher diversity of birds during spring and summer is possibly due to the abundance of breeding species that nest during spring and summer as mentioned by Mounir et al. [20] in the same valleys. The authors have recorded 92 breeding birds in spring and summer in 2018 and 2019. Equally, Mansouri et al. [77] and Wakass et al. [78] documented 98 breeding species in the spring and summer seasons in the east of High Atlas near Midelt, which is only about 120 km from our study area.

Our results showed significant variation of avian distribution in the Central High Atlas in studied valleys under the combination of altitudes and seasons factors. The first axis of the ordination diagram separates a group of resident and migrant species (G3) that occur in high-mountain xerophytes in summer including Sylvia conspicillata, Rhodopechys alienus, and Monticola saxatilis, from many species (G2) that occur in spring and autumn in the same altitudinal section, principally in juniper stands and agricultural fields of Aït Bouguemez valleys. The very low species richness in the high formations of xerophytic steppes is in agreement with previous studies carried out in the same valleys of the Central High Atlas [20] and in the Western High Atlas [39]. In this context, the stringent environmental conditions of high altitude (low temperature and lack of food resources) combined with the spatial dynamics described by certain theories such as the mid-domain effect hypothesis (MDE) could explain the low species diversity in these mountainous areas [22].

The second axis of the diagram shows that birds follow an altitudinal gradient from low to high altitudes. During winter, the Bin EL Ouidane reservoir situated in the low-altitude section attracts divers number of waterfowl and other waterbird species including Recurvirostridae, Scolopacidae, and Charadriidae (G6), as opposed to the mountain lake of Izourar located in high altitude at 2569 m above sea level, where Tadorna ferruginea was the only observable waterbird with more than 200 individuals. Even though this lake shows tens of visitors of this species following precipitation events, its neighbouring lands seem unfavourable as breeding habitat for this duck, in contrast to the Bin El Ouidane reservoir in lowlands, which contains submergent vegetations in the upstream part, offering favourable breeding or wintering grounds for many species including the globally vulnerable Aythya ferina [79, 80]. The other group (G5) includes more than 20 species with high abundance in low altitudes during spring, summer, and autumn (mainly Spinus spinus, Periparus ater, and Sylvia atricapilla) which were widely abundant in coniferous stands (Pinus halepensis and Juniperus phoenicea) and woody shrubs of Buxus balearica and pistacia lentiscus. This vegetation type has a high coverage in this altitudinal range, offering significant nesting substrates and foraging resources to these species. Similar results were reported by the authors of [81] who documented Spinus spinus in low-altitudinal ecosystems of Barcelona (500−600 m), Catalonia, north-eastern Spain, and [82] who mentioned the occurrence of diving waterbirds including the globally vulnerable Aythya ferina in Oued Fez (400 to 500 m, central Morocco). However, the seasonal variation of these species in this altitudinal section is a new aspect that needs more advanced investigations.

In medium-altitude habitats, 10 avian species (G4), principally Acrocephalus baeticatus ambiguus, Hippolais polyglotta, and Iduna opaca, were recorded during spring and summer. During our study, the three mentioned species of Acrocephalidae were recorded in dense vegetation along the river course (e.g., Salix purpurea, Rubus ulmifolius, and Nerium oleander). The high coverage of this riparian vegetation in such altitudinal range provides important sites for food and nesting for these species. This finding aligns with results mentioned in medium altitudes between the Western High Atlas and the Middle Atlas near Midelt for Hippolais polyglotta [36] during spring and summer. Additionally, similar observations were made for Acrocephalus baeticatus ambiguous, which was reported currently as a breeder in medium-altitudinal habitats of Arroyo Ardachón in southeast of Spain [83].

High-altitude habitats witness the arrival of winter passerines including Fringilla montifringilla, Turdus iliacus, and Turdus torquatus, in addition to the occurrence of other resident species with higher abundance in winter, counting Eremophila alpestris and Aquila chrysaetos (G1). These are in agreement with results reported by Cuzin [39], Sánchez-Zapata et al. [84], Clouet et al. [85], Bautista et al. [86], Mansouri et al. [36], and Shakya et al. [87] who characterized the habitats of these species in Mediterranean mountains including those of Morocco in the Southern Slope.

5. Conclusion

This study highlights for the first time the avian diversity and abundances according to the altitudinal and seasonal variations in two valleys of the Central High Atlas Mountains and Northwest Africa, which host important avian diversity and significant bird communities. However, bird richness and abundance vary seasonally and follow the altitudinal gradient. Despite the significant contribution of this paper to the knowledge of poor-studied mountainous avian communities in Morocco and North Africa, more investigations are needed to clarify the effects of habitat features, human presence, and agricultural practices on avian species in these mountainous areas.

Data Availability

The data used to support the findings of this study are included in the article.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

The authors would like to acknowledge the support of the GIZ for providing an internship opportunity that greatly assisted in the completion of our research.

Supplementary Materials

Figure SM A: phenological status of bird species observed in the two valleys of the Central High Atlas of Beni Mellal (Oued Ahançal and Aït Bouguemmaz). Figure SM B: abundance profile of avian species recorded in Oued Ahançal and Aït Bouguemmaz valleys. Figure SM C: abundance classes of avian species in the global avifauna assemblage of Oued Ahançal and Aït Bouguemmaz valleys. (Supplementary Materials)

References

A. Chandra and A. Idrisova, “Convention on Biological Diversity: a review of national challenges and opportunities for implementation,” Biodiversity & Conservation, vol. 20, no. 14, pp. 3295–3316, 2011.
View at: Publisher Site | Google Scholar
M. Dakki, “Etude Nationale sur la Biodiversité: faune aquatique continentale,” in Rapport de l’etude nationale sur la biodiversité édité par la direction de l’observation, des études et de la coordination, Springer, Berlin, Germany, 1997.
View at: Google Scholar
M. Dakki, M. Menioui, and Z. Amhaouch, Stratégie Nationale et plan d’action 2015-2024 pour les Zones Humides du Maroc, Food and Agriculture Organization, Rome, Italy, 2016.
M. Fennane and M. Ibn Tattou, Flore Pratique du Maroc, Inst Scientifique, Rabat, Morocco, 1999.
M. R. Abelouah, M. Ben-Haddad, A. A. Alla, and N. Rangel-Buitrago, “Marine litter in the central Atlantic coast of Morocco,” Ocean & Coastal Management, vol. 214, Article ID 105940, 2021.
View at: Publisher Site | Google Scholar
I. Agmour, M. Bentounsi, N. Achtaich, and Y. El Foutayeni, “Carrying capacity influence on the incomes of seiners exploiting marine species in the Atlantic coast of Morocco,” Mathematical Biosciences, vol. 305, pp. 10–17, 2018.
View at: Publisher Site | Google Scholar
M. Menioui, M. Dakki, and P. Aguesse, “Une biotypologie des peuplements infralittoraux superficiels de crustaces des cotes rocheuses marocaines,” Vie et Milieu, vol. 40, no. 1, pp. 57–66, 1990.
View at: Google Scholar
S. Hammada, M. Dakki, M. Ibn Tattou, and M. Fennane, “Analysis of the Moroccan wetlands floristic diversity: rare, threatened and halophilous flora,” Acta Botanica Malacitana, vol. 43–66, 2005.
View at: Google Scholar
E. K. Urban, R. Vernon, and P. Bergier, “The birds of Morocco,” The Auk, vol. 122, no. 4, pp. 1303–1305, 2005.
View at: Publisher Site | Google Scholar
A. Sorace, P. Formichetti, A. Boano, P. Andreani, C. Gramegna, and L. Mancini, “The presence of a river bird, the dipper, in relation to water quality and biotic indices in central Italy,” Environmental Pollution, vol. 118, no. 1, pp. 89–96, 2002.
View at: Publisher Site | Google Scholar
S. Larsen, A. Sorace, and L. Mancini, “Riparian bird communities as indicators of human impacts along mediterranean streams,” Environmental Management, vol. 45, no. 2, pp. 261–273, 2010.
View at: Publisher Site | Google Scholar
F. Robledano, M. A. Esteve, P. Farinós, M. F. Carreño, and J. Martínez-Fernández, “Terrestrial birds as indicators of agricultural-induced changes and associated loss in conservation value of Mediterranean wetlands,” Ecological Indicators, vol. 10, no. 2, pp. 274–286, 2010.
View at: Publisher Site | Google Scholar
M. Thevenot, “Contribution a l’étude ecologique des passereaux forestiers du Plateau Central et de la corniche du Moyen Atlas (Maroc),” Oiseau et la Revue Francaise d’Ornithologie, vol. 52, 1982.
View at: Google Scholar
I. Cherkaoui, S. Selmi, J. Boukhriss, R. I. Hamid, and D. Mohammed, “Factors affecting bird richness in a fragmented cork oak forest in Morocco,” Acta Oecologica, vol. 35, no. 2, pp. 197–205, 2009.
View at: Publisher Site | Google Scholar
R. El Hamoumi, M. Dakki, and M. Thévenot, “Composition et phénologie du peuplement D’oiseaux d’eau du complexe lagunaire de sidi moussa-walidia (MAROC): son importance nationale et internationale,” Alauda, vol. 68, no. 4, pp. 275–294, 2000.
View at: Google Scholar
A. Ouassou, M. Dakki, M. A. El Agbani, A. Qninba, and R. El Hamoumi, “Distribution and numbers of three globally threatened waterbird species wintering in Morocco: the common pochard, marbled teal, and white-headed duck,” International Journal of Zoology, vol. 2021, Article ID 8846203, 17 pages, 2021.
View at: Publisher Site | Google Scholar
M. Mounir, I. Mansouri, W. Squalli, S. Hammada, and M. Dakki, “Spatial and temporal monitoring of north african turtle doves Streptopelia turtur arenicola (hartert, EJO, 1894): first migrants arrive early and select nesting trees next to foraging resources while second breeders’ wave breed around earlier nests,” International Journal of Zoology, vol. 2023, Article ID 8863486, 11 pages, 2023.
View at: Publisher Site | Google Scholar
D. Barreau and P. Bergier, “L’Avifaune de La région de marrakech (haouz et haut atlas de marrakech, maroc),” Alauda, vol. 69, no. 2, pp. 261–309, 2001.
View at: Google Scholar
L. Chillasse and M. Dakki, “Potentialités et statuts de conservation des zones humides du Moyen-Atlas (Maroc), avec référence aux influences de la sécheresse,” Secheresse (Montrouge), vol. 15, no. 4, pp. 337–345, 2004.
View at: Google Scholar
M. Mounir, M. Dakki, I. Douini et al., “The avifauna of two High Atlas valleys breeding assemblages in forest stands and open lands,” Journal of Animal Behaviour and Biometeorology, vol. 10, no. 3, pp. 1–10, 2022.
View at: Publisher Site | Google Scholar
D. Chamberlain, M. Brambilla, E. Caprio, P. Pedrini, and A. Rolando, “Alpine bird distributions along elevation gradients: the consistency of climate and habitat effects across geographic regions,” Oecologia, vol. 181, no. 4, pp. 1139–1150, 2016.
View at: Publisher Site | Google Scholar
C. D. Ferreira and G. Perbiche-Neves, “The importance of the standardizing sampling methodology to detect altitudinal gradients in mountains: a study case for the resident bird community in a hotspot (Atlantic forest) and the Middle Domain Effect,” Acta Oecologica, vol. 110, Article ID 103677, 2021.
View at: Publisher Site | Google Scholar
F. Mallet-Rodrigues, R. Parrini, L. M. S. Pimentel, and R. Bessa, “Altitudinal distribution of birds in a mountainous region in southeastern Brazil,” The Zoologist, vol. 27, no. 4, pp. 503–522, 2010.
View at: Publisher Site | Google Scholar
W. W. Immerzeel, L. Petersen, S. Ragettli, and F. Pellicciotti, “The importance of observed gradients of air temperature and precipitation for modeling runoff from a glacierized watershed in the Nepalese Himalayas,” Water Resources Research, vol. 50, no. 3, pp. 2212–2226, 2014.
View at: Publisher Site | Google Scholar
F. C. Rego and M. S. Rocha, “Climatic patterns in the mediterranean region,” Ecologia Mediterranea, vol. 40, no. 1, pp. 49–59, 2014.
View at: Publisher Site | Google Scholar
A. Benabid, “Bref aperçu sur la zonation altitudinale de la végétation climacique du Maroc,” Ecologia Mediterranea, vol. 8, no. 1, pp. 301–315, 1982.
View at: Publisher Site | Google Scholar
S. Gentile, “Zonation altitudinale de la végétation en Italie méridionale et en Sicile (Etna exclu),” Ecologia Mediterranea, vol. 8, no. 1, pp. 323–337, 1982.
View at: Publisher Site | Google Scholar
M. D. Miara, M. Ait Hammou, S. Hadjadj-Aoul, and A. S. Hamerlain, “Bioclimats, etages de vegetation et zonation altitudinale des groupements vegetaux dans les monts de tiaret (exemple des groupements forestiers et preforestiers du massif de guezoul),” Revue Ecologie-Environnement, vol. 9, 2013.
View at: Google Scholar
M. E. Visser, L. J. M. Holleman, and P. Gienapp, “Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird,” Oecologia, vol. 147, no. 1, pp. 164–172, 2006.
View at: Publisher Site | Google Scholar
A. S. Anderson, T. A. Marques, L. P. Shoo, and S. E. Williams, “Detectability in audio-visual surveys of tropical rainforest birds: the influence of species, weather and habitat characteristics,” PLoS One, vol. 10, no. 6, Article ID e0128464, 2015.
View at: Publisher Site | Google Scholar
T. R. Duclos, W. V. DeLuca, and D. I. King, “Direct and indirect effects of climate on bird abundance along elevation gradients in the Northern Appalachian mountains,” Diversity and Distributions, vol. 25, no. 11, pp. 1670–1683, 2019.
View at: Publisher Site | Google Scholar
D. Rubolini, R. Ambrosini, M. Caffi, P. Brichetti, S. Armiraglio, and N. Saino, “Long-term trends in first arrival and first egg laying dates of some migrant and resident bird species in northern Italy,” International Journal of Biometeorology, vol. 51, no. 6, pp. 553–563, 2007.
View at: Publisher Site | Google Scholar
C. Carey, “The impacts of climate change on the annual cycles of birds,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 364, no. 1534, pp. 3321–3330, 2009.
View at: Publisher Site | Google Scholar
L. Halupka and K. Halupka, “The effect of climate change on the duration of avian breeding seasons: a meta-analysis,” Proceedings of the Royal Society B: Biological Sciences, vol. 284, no. 1867, Article ID 20171710, 2017.
View at: Publisher Site | Google Scholar
I. Mansouri, M. Mounir, W. Squalli, L. Elhanafi, M. Dakki, and L. El Ghadraoui, “Migratory dates, breeding phenology, and reproductive success of European turtle doves between lowlands and highest breeding habitats in North Africa,” International Journal of Zoology, vol. 2020, Article ID 8816577, 7 pages, 2020.
View at: Publisher Site | Google Scholar
I. Mansouri, W. Squalli, M. Dakki et al., “Breeding biology, chronology, and reproductive success of the European serin (Serinus serinus) at Moulouya high plain (Morocco),” International Journal of Zoology, vol. 2021, Article ID 8737951, 8 pages, 2021.
View at: Publisher Site | Google Scholar
J. Cusens, S. D. Wright, P. D. McBride, and L. N. Gillman, “What is the form of the productivity-animal-species-richness relationship? a critical review and meta-analysis,” Ecology, vol. 93, no. 10, pp. 2241–2252, 2012.
View at: Publisher Site | Google Scholar
J. L. Tellería, “Long-term altitudinal change in bird richness in a Mediterranean mountain range: habitat shifts explain the trends,” Regional Environmental Change, vol. 20, no. 2, p. 69, 2020.
View at: Publisher Site | Google Scholar
F. Cuzin, “L’avifaune de très haute altitude du Parc National du Toubkal (Haut Atlas, Maroc),” Bulletin de l’Institut Scientifique, Rabat, Section Sciences de La Vie, vol. 32, no. 1, pp. 25–32, 2010.
View at: Google Scholar
A. Qninba, F. Cuzin, M. A. El Agbani, and M. Thévenot, “Breeding avifauna of the jbel saghro (Anti-Atlas, Morocco), a detached mediterranean upland bordering the sahara, 30-31°N/5-6°W,” Section Sciences de La Terre, vol. 35, pp. 119–129, 2013.
View at: Google Scholar
M. Dakki, “Fiche descriptive ramsar pour le Site n° 2372,” 2019a, https://rsis.ramsar.org/ris/2372.
View at: Google Scholar
M. Dakki, “Fiche descriptive Ramsar pour le Site n° 2378,” 2019b, https://rsis.ramsar.org/ris/2378.
View at: Google Scholar
J. Rais, A. Barakat, E. Louz, and A. Ait Barka, “Geological heritage in the M’Goun geopark: a proposal of geo-itineraries around the bine El Ouidane dam (central high atlas, Morocco),” International Journal of Geoheritage and Parks, vol. 9, no. 2, pp. 242–263, 2021.
View at: Publisher Site | Google Scholar
L. Auclair and M. Alifriqui, “Agdal patrimoine socio-écologique de l’Atlas marocain,” 2012, https://www.editions.ird.fr/produit/70/9782709917148/agdal.
View at: Google Scholar
B. Romagny, L. Auclair, and A. Elgueroua, “La gestion des ressources naturelles dans la vallée des Aït Bouguemez (Haut Atlas): la montagne marocaine à la recherche d’innovations institutionnelles,” Mondes en Développement, pp. 63–80, 2008.
View at: Publisher Site | Google Scholar
M. Ibn Tattou and M. Fennane, “Projet de gestion des aires protégées,” 2006, https://action.biopama.org/wp-content/uploads/2021/01/WA187_InfoFiche_RB_final.pdf.
View at: Google Scholar
B. Keita, “Gestion sociale de l’ eau et projet de modernisation hydraulique dans une vallée du haut atlas au Maroc les Aït Hakim (des Aït Bouguemez),” PCSI-4e Séminaire International et Interdisciplinaire, vol. 1–15, 2006.
View at: Google Scholar
J. Riaux, T. Ruf, M.-J. Valony, and A. Herzenni, “Dynamiques des Innovations sociales et institutionnelles de l’irrigation dans une vallée du haut Atlas au Maroc Vallée des Ait Hakim,” Ait Bougmez, vol. 41, 2003.
View at: Google Scholar
M. Rhanem, “Etude phyto-écologique des versants de la vallée des Aït-Bou-Guemmez [Montpellier],” 1985, https://infodoc.agroparistech.fr/index.php?lvl=notice_display&id=135382.
View at: Google Scholar
T. Aude Nuscia, Y. El Khalki, and M. El Hannani, Atlas régional Région du Tadla Azilal Maroc, HCL, Bengaluru, India, 2015.
L. Emberger, “Une classification biogéographique des climats,” Recherches et Travaux des Laboratoires de Géologie, Botanique et Zoologie, Faculté des Sciences Montpellier (France), vol. 7, pp. 1–43, 1966.
View at: Google Scholar
L. Emberger, “La position phytogéographique du Maroc dans l’ensemble méditerranéen,” Position Phytogeographique Du Maroc, vol. 12, pp. 1–15, 1969.
View at: Google Scholar
J. Roche, Les oiseaux nicheurs des cours d’eau du bassin de la Saone: etude ecologique des peuplements le long du gradient amont-aval, L’University de Bourgogne, Dijon, France, 1986.
J. Blondel, C. Ferry, and B. Frochot, “La méthode des indices ponctuels d’abondance (IPA) ou des relevés d’avifaune par stations d’écoute,” Alauda, vol. 38, pp. 55–71, 1970.
View at: Google Scholar
J. Blondel, C. Ferry, and B. Frochot, “Point counts with unlimited distance,” Studies in Avian Biology, vol. 6, pp. 414–420, 1981.
View at: Google Scholar
C. J. Ralph, G. R. Geupel, P. Pyle, T. E. Martin, and D. F. DeSante, “Handbook of field methods for monitoring landbirds,” Director, vol. 144, no. 1, pp. 1–41, 1993.
View at: Google Scholar
C. J. Ralph, S. Droege, and J. R. Sauer, “Managing and monitoring birds using point counts: standards and applications,” Workshop on Monitoring Bird Population Trends by Point Counts, vol. 18, pp. 161–169, 1995.
View at: Google Scholar
J. Haselmayer and J. S. Quinn, “A comparison of point counts and sound recording as bird survey methods in amazonian southeast Peru,” The Condor: Ornithological Applications, vol. 102, no. 4, pp. 887–893, 2000.
View at: Publisher Site | Google Scholar
A. A. Whitman, J. M. H. Iii, and N. V. L. Brokaw, “A comparison of two bird survey techniques used in a subtropical forest,” The Condor: Ornithological Applications, vol. 99, no. 4, pp. 955–965, 1997.
View at: Publisher Site | Google Scholar
R. D. Gregory, D. W. Gibbons, and P. F. Donald, “Bird census and survey techniques,” Bird Ecology and Conservation, vol. 15, pp. 17–56, 2004.
View at: Publisher Site | Google Scholar
J. P. Benzécri, L’analyse des correspondances, Dunod, Paris, France, 1973.
Ibm Corp, Statistics for Windows, IBM, Armonk, NY, USA, 2012.
L. Graphpad software, “GraphPad prism for windows,” 2019, https://www.graphpad.com/.
View at: Google Scholar
H. Achiban, I. Mansouri, W. Squalli et al., “Avifauna of the Oued Bouhellou Valley (Morocco): remarkable diversity, five new breeding cases and mapping of nesting sites,” Zoology and Ecology, vol. 32, no. 1, pp. 36–48, 2022.
View at: Publisher Site | Google Scholar
H. Nekhla, I. Mansouri, A. Zahri et al., “The ecological importance of Chamaerops humilis steppe for animal biodiversity in Northwest Africa (Morocco),” Zoology and Ecology, vol. 32, no. 1, pp. 74–83, 2022.
View at: Publisher Site | Google Scholar
A. Boucif, M. Bara, and M. Houhamdi, “Ecological Diagnosis and Div cological Diagnosis and Diversity Structur ersity Structure of the F e of the Forest Bir est Birds Community in Machr Community in Machroha Forest Souk Ahr est Souk Ahras Nor as Northeastern theastern Algeria,” Journal of Bioresource Management, vol. 9, no. 4, pp. 102–109, 2022.
View at: Google Scholar
M. El Bouhissi, A. Chedad, S. E. Sadine, W. Dahmani, and M. A. Hammou, “Avifaunistic diversity of merine forest, north-west Algeria,” Current Trends in Natural Sciences, vol. 10, no. 20, pp. 61–71, 2021.
View at: Publisher Site | Google Scholar
J. F. Calvo, A. J. Hernández Navarro, F. Robledano et al., “Catalogue of the birds of the province of Murcia (Spain),” Anales de Biología, vol. 39, pp. 7–33, 2017.
View at: Publisher Site | Google Scholar
C. Ryall, K. Briggs, C. Ryalla, and K. Briggs, “Some factors affecting foraging and habitat of Ring Ouzels Turdus torquatus wintering in the Atlas Mountains of Morocco,” Bull ABC, vol. 13, no. 1, pp. 17–31, 2006.
View at: Google Scholar
M. Dakki, B. Riad-Essolh, and M. A. El Agbani, “Recensement hivernal d’oiseaux d’eau au Maroc,” Institut Scientifique Doc, vol. 16, pp. 1–32, 1993.
View at: Google Scholar
S. Hammi, V. Simonneaux, J. B. Cordier et al., “Can traditional forest management buffer forest depletion? Dynamics of Moroccan High Atlas Mountain forests using remote sensing and vegetation analysis,” Forest Ecology and Management, vol. 260, no. 10, pp. 1861–1872, 2010.
View at: Publisher Site | Google Scholar
A. Ahbari, L. Stour, A. Agoumi, and L. Oualkacha, “A simple and efficient approach to predict reservoir settling volume: case study of Bin El Ouidane reservoir (Morocco),” Arabian Journal of Geosciences, vol. 11, no. 19, p. 591, 2018.
View at: Publisher Site | Google Scholar
L. Auclair, “L’appropriation communautaire des forêts dans le Haut Atlas marocain,” Cah. Sci. Hum, vol. 32, pp. 177–194, 1996.
View at: Google Scholar
J. A. Klemens, R. G. Harper, J. A. Frick, A. P. Capparella, H. B. Richardson, and M. J. Coffey, “Patterns of organochlorine pesticide contamination in neotropical migrant passerines in relation to diet and winter habitat,” Chemosphere, vol. 41, no. 7, pp. 1107–1113, 2000.
View at: Publisher Site | Google Scholar
S. Hanane and L. Baamal, “Are Moroccan fruit orchards suitable breeding habitats for Turtle Doves Streptopelia turtur?” Bird Study, vol. 58, no. 1, pp. 57–67, 2011.
View at: Publisher Site | Google Scholar
A. El Hassani, I. Mansouri, W. Squalli et al., “Breeding performances of the European blackbird (Turdus merula) in Morocco: habitat selection, breeding phenology, and breeding success,” International Journal of Zoology, vol. 2021, Article ID 7742894, 8 pages, 2021.
View at: Publisher Site | Google Scholar
I. Mansouri, W. Squalli, A. El Agy et al., “Avifauna diversity in the gate between humid atlas and saharan desert: Midelt province, Morocco,” International Journal of Zoology, vol. 2021, Article ID 5557921, 10 pages, 2021.
View at: Publisher Site | Google Scholar
S. Wakass, M. Mounir, W. Squalli et al., “Diversity of avian species their ecosystems and climate conditions in two zones of High Atlas (central Morocco) for ecotouristic purposes,” Journal of Animal Behaviour and Biometeorolgy, vol. 8, 2023.
View at: Google Scholar
A. Elafri, M. Belhamra, and M. Houhamdi, “Comparing habitat preferences of a set of waterbird species wintering in coastal wetlands of North Africa: implication for management,” Ekológia, vol. 36, no. 2, pp. 158–171, 2017.
View at: Publisher Site | Google Scholar
Birdlife International, “Aythya ferina,” The IUCN Red List of Threatened Species, BirdLife International, Cambridge, UK, 2021.
View at: Publisher Site | Google Scholar
J. Pascual, J. C. Senar, and J. Domènech, “Plumage brightness, vigilance, escape potential, and predation risk in male and female Eurasian Siskins (Spinus spinus),” The Auk, vol. 131, no. 1, pp. 61–72, 2014.
View at: Publisher Site | Google Scholar
W. Squalli, I. Mansouri, M. Dakki, and F. Fadil, “Nesting habitat and breeding success of Fulica atra in tree wetlands in Fez’s region, central Morocco,” Journal of Animal Behaviour and Biometeorology, vol. 8, no. 4, pp. 282–287, 2020.
View at: Publisher Site | Google Scholar
F. Jiguet, P. Dufour, K. J. Kardynal et al., “Identifying the winter grounds of the recently described Barbary Reed Warbler (Acrocephalus baeticatus ambiguus),” Ibis, vol. 165, no. 1, pp. 204–213, 2022.
View at: Publisher Site | Google Scholar
J. A. Sánchez-Zapata, S. Eguía, M. Blázquez, M. Moleón, and F. Botella, “Unexpected role of ungulate carcasses in the diet of Golden Eagles Aquila chrysaetos in Mediterranean mountains,” Bird Study, vol. 57, no. 3, pp. 352–360, 2010.
View at: Publisher Site | Google Scholar
M. Clouet, J. F. Gerard, J. L. Goar et al., “Diet and breeding performance of the golden eagle Aquila chrysaetos at the eastern and western extremities of the pyrenees: an example of intra-population variability,” Ardeola, vol. 64, no. 2, pp. 347–361, 2017.
View at: Publisher Site | Google Scholar
J. Bautista, S. Castillo, J. L. Paz, J. Llamas, and E. David H, “Golden Eagles (Aquila chrysaetos) as potential predators of Barbary Macaques (Macaca sylvanus) in northern Morocco evidences of predation Golden Eagles (Aquila chrysaetos) as potential predators of Barbary macaques (Macaca sylvanus) in northern,” Go-South Bull, vol. 15, pp. 172–179, 2019.
View at: Google Scholar
S. B. Shakya, C. Y. Wang-Claypool, C. Cicero, R. C. K. Bowie, and N. A. Mason, “Neo-sex chromosome evolution and phenotypic differentiation across an elevational gradient in horned larks (Eremophila alpestris),” Molecular Ecology, vol. 31, no. 6, pp. 1783–1799, 2022.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2024 Mohamed Mounir et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies

Views

110

Downloads

90

Citations