Bats of the Safi-Essaouira Provinces (Morocco): New Inputs to the Knowledge of Bat Populations of the Atlantic Littoral

Dbiba, Youssef; Dakki, Mohamed; Mansouri, Ismail; El Mouden, El Hassan

doi:https://doi.org/10.1155/2023/6624548

International Journal of Zoology

On this page

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

Research Article | Open Access

Volume 2023 | Article ID 6624548 | https://doi.org/10.1155/2023/6624548

Bats of the Safi-Essaouira Provinces (Morocco): New Inputs to the Knowledge of Bat Populations of the Atlantic Littoral

Youssef Dbiba,¹Mohamed Dakki,²Ismail Mansouri,³and El Hassan El Mouden¹

Academic Editor: Zerihun Girma

Received07 Jun 2023

Revised30 Aug 2023

Accepted26 Sept 2023

Published12 Oct 2023

Abstract

In Morocco, investigations of bats are limited and fragmentary. The majority of studies were done in northern provinces close to the Mediterranean Sea and focused on the geographical distribution of bats. With the aim of overcoming these gaps, we used diurnal caves visits, hand nets and mist nets, and acoustic surveys to make an inventory of the Atlantic littoral of Safi-Essaouira provinces, which is considered one of the most neglected regions in the country. In total, five caves and nine foraging habitats were surveyed from 2020 to 2022. Our surveys highlighted the distribution of eleven bat species belonging to five families, of which Rhinolophus blasii and Tadarida teniotis species were newly recorded in the study area. Three caves, namely, Sbaa Fam, Haouya, and Sidi Benkrara were newly discovered and hosted medium-sized colonies of five species. They were important for bats during the daytime, hibernation, and breeding. In foraging habitats, 2650 passes of 10 species were recorded. Pipistrellus pipistrellus and Pipistrellus kuhlii were the most active, followed by Miniopterus schreibersii and Eptesicus isabellinus, while Rhinolophus ferrumequinum, Hipposideros tephrus, Rhinolophus mehelyi, T. teniotis, Myotis punicus, and R. blasii were less active. Olive groves were the most diverse habitat with 8 species, followed by Safi pinewood and degraded Argane forest with 4 species each and Sidi Abderrahmane lake with 3 species. The other habitats hosted only two species each. This paper is the first to highlight data on bats in the coastal areas of Morocco and North Africa. Our results contribute to improve knowledge of the annual cycle of these bats and fill the gaps related to their distribution in the coastal area of the Safi-Essaouira provinces.

1. Introduction

The geographical position and landscape of Morocco, with 3500 km of seacoasts, four mountain chains, large plains, and low plateaus, generated a high diversity of ecosystems and wildlife [1, 2]. This diversity appeared during the late Tertiary and Quaternary periods when Morocco was exposed to high climate variations and insularity factors that created many original ecosystems [3].

Mammals reflect this diversity and originality well, as their species number reached 105, with a high rate of rare or endemic taxa estimated at 40% [4]. Among this group, 31 bat species have been discovered until now in Morocco [4–7]; this group is supposed to deserve a high priority in the national strategies of research and conservation, as bats have a great socioeconomic importance. Indeed, they constitute major agents of insect pest control [8–14] and a source of infectious diseases [15–18]. In addition, bats are good indicators of environmental quality and climate change [19–24].

In Morocco, 31 bat species belonging to eight families were currently recorded. These species represent 29.5% of the total mammalian fauna in Morocco. In comparison with neighboring countries, Algeria hosts only 26 bat species, while Tunisia records only 20 bat species. Similarly, only seven families of Chiroptera are mentioned in Algeria and Tunisia [4–7, 25–28]. These findings demonstrate the high value of Moroccan landscapes for bat species.

Similar to other mammals, Moroccan bats are exposed to high losses, as eight species are endangered or vulnerable taxa, despite the fact that eleven bat species are not evaluated [30]. Human interference in their roosts, the use of pesticides, and misinformation about bats [31] are the most significant threats impacting their existence. The recurrent drought crises and the increasing number of wind farms have certainly had great effects on Moroccan bats but these effects are still unknown.

In Morocco, the first scientific investigations on Chiroptera, mainly focused on the Northern and Atlas regions, were generally based on traditional techniques, such as daily visits to caves, hand capture, roost counts, and mist-net trapping [32–48]. Despite the weakness of the available data, these investigations revealed 24 species among seven families.

In more recent works, some researchers [49] reported bats in the diet of nocturnal raptors, while others [50–55] used ultrasonic detectors [56–59]. This latter technique, considered as the nondestructive method, is generally combined with the aforementioned techniques. These works added five species to the former list of Moroccan Chiroptera. Furthermore, the use of both craniodental characteristics and genetic (mitochondrial and nuclear DNA) methods provided taxonomic precision for some species, such as Miniopterus maghrebensis [6] and Myotis zenatius [5].

Despite the several studies and notes dedicated to Moroccan bats [60], the distribution data gathered remain sparse and mainly focused on the northern half of the country, some of which are outdated. Some bat species, such as Taphozous nudiventris, Myotis capaccini, Nyctalus lasiopterus, and Nyctinomus aegyptiacus, have been identified from a few sites [33, 53, 61–65]. Furthermore, bats’ health, their annual cycle, and their migration routes remain poorly studied. With this in mind, this work was definitely worth undertaking. Indeed, great monitoring efforts are needed in the whole country over the four seasons.

The development of acoustic tool detection, supported by other conventional techniques, promises new advances in bat investigations, notably in their distribution. In this study, we aimed to make an inventory of bat species in the coastal area of Safi-Essaouira provinces, west of Morocco. We investigated the diversity of bat species in caves and foraging habitats dominating the sampling sites. Equally, we noted the importance of the habitats for the recorded bat species to evaluate their roles in feeding and breeding activities of species.

2. Materials and Methods

2.1. Study Areas and Sites

Our study was carried out in the Atlantic littoral of Safi-Essaouira provinces (Figure 1), which is under a Mediterranean climate [66–68], more precisely semiarid (thermo-Mediterranean to sub-Mediterranean), with a protracted dry season (late spring to early autumn). More specifically, the two provinces have quite similar climates as follows: in Safi, the annual rainfall is 274 mm and the annual average of temperatures is 18.4°C, while these parameters are, respectively, 295 mm and 18.7°C in Essaouira (https://climate-data.org). In this latter area, the oceanic winds are quite permanently refreshed by the upwelling currents that mark the sea waters in this area and reduce the summer temperature in the littoral.

This climate, with its different variants, fosters diverse terrestrial plant communities dominated by a few species, the most important of which are Argania spinosa, Tetraclinis articulata, Juniperus phoenicea, Olea europaea, Pistacia atlantica, Euphorbia regis-Jubae, and Senecio anteuphorbium.

Bat investigations were conducted at fourteen sites (Figure 1, Table 1) and were identified for their potential importance as bat habitats as follows: five caves, one agricultural land, one artificial reservoir, and seven foraging habitats. Half of these sites are on the ocean coast or very close to it, and the others are more or less continental (up to 30 kilometers from the coastline).

2.2. Data Collection

This work started in September 2020, with the identification of potential bat habitats in the study area, using existing documentation, mainly Boualla et al. [69] and Camus and Lamouroux [70], satellite images, and in-person interviews. This permitted us to locate potential sites (caves, chasms, and forests) and potential foraging habitats (agricultural fields, surface waters, and farms). Four common methods were used to undertake the bat survey as follows: detecting echolocation calls, mist netting, diurnal visits to the accessible caves, and hand netting. All night visits took place during the three first hours since sunset, where we recorded echolocation calls at fixed places and/or along foot transects.

The survey was made in suitable weather conditions (no rain and wind speed less than 20 km/h). In foraging habitats, we used acoustic detection at fixed points or along foot transects of 300–400 m with a constant speed of 2 km/h. Two bat detectors are used as follows: (1) the Song Meter 4 FS ultrasonic recorder (Wildlife-Acoustics, USA) coupled to a 5-meter microphone (SMM-U2 Ultrasonic Microphone) and (2) the time expansion bat detector, the Pettersson D240X (Uppsala, Sweden), coupled to a portable digital recorder (Edirol R-09HR, Roland Corporation, China). In caves, the closest bats were hand netted, but we also used mist nets (3m × 12m; 16 mm × 16 mm) that are installed in front of known roosts (Table 2).

2.3. Species Identification

Recorded calls were displayed using the Kaleidoscope program version 5.4.8 (Wildlife-Acoustics Inc., USA) as oscillograms and spectrograms concurrently. The settings utilized were as follows: the window size is 128, FFT size is 512, and cache size maximum is 256. The time period of recorded sequences was defined according to the bat detector as follows: every 34.7 s of recording with the D240X and every 5 s of recording with the SM4BAT-FS. One echolocation call from each bat pass was manually identified to the species level, using shape and other call parameters described in the sound library of Barataud [70]. Echolocation calls of recorded species were identified using regional acoustic characteristics [72, 73] and North-African data [74, 74]. In addition, we used unpublished reference calls that we gathered from several Moroccan locations. Captured individuals of bats were identified using different systematic resources [75–77].

During the 15 days of the internship, it aims to revise, reidentify, and draw up the story of the knowledge of described bats in Morocco and to assess the state of preservation of specimens deposited in the National Museum of Natural History of the Scientific Institute of Rabat. We have found 17 species divided into 6 families, and we noticed that no specimens were collected from the study area [78].

3. Results

During our survey along the coast of Safi-Essaouira provinces, we identified 11 bat species, representing 35.5% of the total registered species in the entire country (Table 3). They belong to five families, namely, Rhinolophidae, Vespertilionidae, Molossidae, Miniopteridae, and Hipposideridae. The species are as follows: greater horseshoe bat Rhinolophus ferrumequinum, lesser horseshoe bat Rhinolophus hipposideros, Mehely’s horseshoe bat Rhinolophus mehelyi, Blasius’ horseshoe bat Rhinolophus blasii, Maghrebian mouse-eared bat Myotis punicus, common Pipistrellus pipistrellus, Kuhl’s pipistrelle Pipistrellus kuhlii, Isabelline serotine bat Eptesicus isabellinus, common bent-wing bat Miniopterus schreibersii, European free-tailed bat Tadarida teniotis, and Maghreb leaf-nosed bat Hipposideros tephrus. Eight species have a Mediterranean character, three species are Palearctic, and one species is a Saharan species.

3.1. Cave’s Bat Assemblages

Using conventional techniques, we identified four species in four caves. The most diverse assemblage is in the caves of Haouya and Gora’an, with three species each. In Sidi Benkrara and Sbaa Fam caves, we found, respectively, two and one species, while no species was recorded near the Maâden cave. At the Haouya cave, we hand netted on November 14th, 2021, three males belonging to three different species of Rhinolophidae, namely, R. hipposideros, R. mehelyi, and R. blasii. The ambient temperature was around 21.4°C and the relative humidity was 74.9%. While using echolocation calls and visual aids, we identified 75 individuals belonging to three species of Rhinolophus in Haouya cave, namely, R. hipposideros (15), R. blasii (37), and R. mehelyi (23).

On July 4th, 2021, in front of the Gora’an cave, we recorded 481 passes belonging to 4 species, namely, R. blasii (354), R. mehelyi (75), M. punicus (49), and P. kuhlii (3). However, on March 31^st, 2022, at a lower temperature (16.5°C) and humidity (66.1%), we mist netted only 24 individuals, belonging to two species only, i.e., M. punicus (15 specimens: 9 males and 6 females) and R. blasii (9). Captured females were pregnant at the first stage. In the cave of Sidi Benkrara, visited in both winter (December 5th, 2021) and summer (August 24th, 2022), six individuals of M. punicus were found in winter (at a temperature of 21°C and humidity of 73.3%) and five of them (adult males) have been captured. The summer visit, with a temperature of 25°C and a humidity of 74%, revealed a small mixed colony composed of M. punicus (37 individuals) and M. schreibersii (23 individuals, among which one female was hand netted). In the Sbaa Fam cave, we identified visually five specimens of M. punicus on April 26, 2022.

3.2. Noncave Bat Assemblages

Bat echolocation calls were recorded at nine sites out of the 14 prospected (Table 4). A total of 2650 passes were recorded during 27 cumulated hours. Within the 10 identified species, P. pipistrellus and P. kuhlii were the most active (42.5% and 35.85% of passes, respectively). Two other species (M. schreibersii and E. isabellinus) were less abundant (15.7% and 4.22% of passes, respectively). The rarest species were R. ferrumequinum, H. tephrus, R. mehelyi, T. teniotis, M. punicus, and R. blasii, as they were represented in 0.83% to 0.07% of passes. The most diversified assemblages were found in olive groves located in the SW Jbel Lahdid habitat (8 species in a private farmland near a pine forest), followed by Safi pinewood and degraded Argane forest with 4 species each, followed by Sidi Abderrahmane lake with 3 species. The other sites showed a maximum of two species.

4. Discussion

Our three-year monitoring provides new data on the occurrence and richness of bat species in the littoral area of Safi-Essaouira, mainly in comparison with those reported by Benda et al. [56, 72] in the littoral zone of Morocco. Indeed, before our study, five species were reported from Safi province, namely, R. euryale, R. ferrumequinum, M. punicus, R. mehelyi, and M. schreibersii. They were cited without precise coordinates [4, 79, 80], while M. punicus and R. mehelyi were reported from corpses in Gora’an cave [81]. Previously, in Essaouira province, nine species of bats (R. euryale, R. hipposideros, H. tephrus, N. thebaica, M. schreibersii, E. isabellinus, P. pipistrellus, P. kuhlii, and M. punicus) were described by Aulagnier et al. [4], Aulagnier and Thévenot [79], and Biollaz et al. [82]. Our investigations permitted us to enrich this inventory with 13 bat species, which represent 41.93% of the bat fauna known in Morocco [4–7, 10]. Globally, two species are new to the fauna of Safi-Essaouira provinces. This enrichment is due to a better coverage of the sampling program in both time and space, as we studied for the first time three caves in the Safi province (the caves of Haouya, Sbaa Fam, and Sidi Benkrara), with the Haouya cave being the richest in bats in the region. Indeed, it houses a small colony of three Rhinolophus species, namely, R. hipposideros, R. blasii, and R. mehelyi.

In Gora’an cave, where three species have been recorded, the mist net permitted the confirmation of the existence of M. punicus, while R. blasii was recently discovered in the cave and R. mehelyi was identified using ultrasound methods. For R. blasii, it was recorded for the first time in two caves in Safi province. In the Moroccan littoral, R. blasii was announced in only four places limited to the Souss-Massa coast [4, 73]; therefore, our findings expand its geographic distribution far to the north.

The presence of R. mehelyi has been confirmed by hand-net and with the use of echolocation calls in the province of Safi, especially in Haouya and Gora’an caves. However, R. euryale has not been confirmed in both provinces yet, while R. mehelyi is present in both provinces. These taxa have a wide distribution throughout the northern part of Morocco [4, 79, 83], while R. euryale shows some affinity to the Saharan area. Previously recorded in Safi, R. ferrumequinum was not recorded in this province during our monitoring, maybe because of its ability to migrate during seasons between roosts, notably in Tazarine cave (a breeding colony disserted the cave in late September), while others use Zaara and Zegzel caves during winter [32, 51, 83]. However, we recorded a few passes in Essaouira, where the species is found for the first time, even though it has a wide distribution [44, 57, 84].

On March 31st, 2022, from 24 mist-netted individuals in the front of Gora’an cave, 14 females were pregnant (5 M. punicus and 9 R. blasii), which coincide with gestation periods that start in late spring in North Africa [74, 85]. However, we observed a transitory flight of one P. kuhlii just before sunset in front of the cave, but we consider that it does not use the cave. Indeed, P. kuhlii has anthropophilic mores and has never been found in caves or subterranean sites; however, it has been reported under old trees’ bark [44], over water courses, and at cave entrances [56, 72]. It was also found in rock crevices and building slots [27, 86].

In reference to the period of surveillance of Haouya cave (14/11/2021), the suitable climate condition of the cave and due to the deep torpor observed in bats, this cave is used as a hibernaculum by the three recorded Rhinolophus species [87]. In Morocco, Rhinolophus species use caves, mines, or even khettara and share roosts with other dwelling bats, such as M. punicus, M. schreibersii, Plecotus gaisleri, and Asellia tridens [32, 51, 57, 79, 83]. Few works focused on the hibernation of this group; for R. mehelyi, hibernation was documented in Ain Sfa cave [88]; for R. blasii, it was studied in Tazzouguert cave [51]. In contrast, R. hipposideros is known to winter in caves or mines in small numbers [4].

In August 2022, at the artificial cave of Sidi Benkrara (newly discovered), we observed a small colony of the gregarious species M. punicus and M. schreibersii. Similar results were shown in Morocco and Algeria [56, 88, 89]. Contrary to other Moroccan regions, in the Safi area, M. punicus and M. schreibersii do not form large colonies such as those discovered in the caves of Win-Timdwine and Wad Imi n”Ouggoug (Agadir region), in Kahf Lakhal (Jbel Moussa in the North), and in the irrigation ditch of Wad Tessaout [56, 58, 81]. In our case, these species are suggested to be dispersed in several caves and crevices at the study sites.

Contrary to the other caves, the Maâden cave, which we visited during the day, did not have any bats. The absence of bats in this cave is suggested to be governed by anthropic disturbance since we noticed many fire plots and branches of Argania thorns inside the cave. These tools are probably used by local residents to catch bats.

In the nine foraging habitats, we recorded 2650 passes (based on ultrasonic methods), belonging to 10 species of bats. In such a subarid landscape, this species richness is similar to those reported in Algerian and Tunisian monitoring [74, 86, 90, 91].

Among these species, P. pipistrellus and P. kuhlii showed the highest number of passes. P. pipistrellus, discovered for the first time in Safi province, was recorded in four places; it is particularly active in agricultural lands where an artificial water basin was installed, where this bat was more attached [92]. It seems that it does not like arid areas where there is no water [57]. For that reason, the distribution of P. pipistrellus through the country showed a relative limitation to the mountainous regions, the Mediterranean basin, and a few sites in the low Draa [4, 72, 79]. In contrast, P. kuhlii is widely distributed in the Atlantic littoral of Morocco, as it was reported from Tangier to Mohammedia and from Essaouira to Boujdour [36, 72, 79]. Our study permitted us to expand this distribution further, as we recorded the species for the first time in the Safi province. A similar wide distribution has also been noticed for this species in Algeria and Tunisia [74, 93].

Concerning E. isabellinus, it was recorded in eight sites in the study area. It has a wide distribution throughout the country, with relative preference towards arid zones [39, 72, 79, 94]. In contrast, the rarest species, T. teniotis and H. tephrus, were only recorded in olive groves located in SW Jbel Lahdid. Furthermore, H. tephrus lives in caves and channels, and its distribution in Morocco extends from the coastal region of Essaouira to the Oued Noun in the south [59, 79]. Moreover, T. teniotis is widely dispersed throughout the country, including desert habitats [4, 57, 58]. However, our observation of T. teniotis presents the first record for the species in the study area.

Despite the difficulties that this study faced, mainly the impossibility of achieving a complete spatiotemporal sampling program, we estimate that the 13 species recorded represent all the bat fauna of the study area. This richness indicates the great importance of the Atlantic littoral of Safi-Essaouira for bats. Furthermore, we discovered two new bat species for this littoral and registered new occurrence in each of the two provinces.

In Morocco, bats are legally protected under Dahir no. 1-11-84, prohibiting the commercialization of endangered wild animal and plant species. However, the implementation of this conservation measure is hampered by lack of information and execution. Therefore, the key to conservation remains raising local awareness of the ecological (economic) services provided by these animals instead of tons of pesticides.

These results are mainly due to the discovery of three caves (Gora’an, Haouya, and Sidi Benkrara), which constitute both important maternity roosts and hibernacula and are inhabited during swarming grouping by two vulnerable species and two near-threatened species, according to UICN (2023). Therefore, these habitats need more protection against environmental and anthropogenic factors. Indeed, caves were used to bury the corpses of animals for treasure hunting (Dbiba pers. obs.) and/or for the intentional catching of bats for witchcraft, while some of them were illuminated by fire plots [31, 74]. These activities and others have potential negative effects on bat communities [95–97]. Similar results were mentioned by Tanalgo et al., [98] who recorded the urgent need to protect caves due to their richness in bats worldwide. These authors mentioned that 48% of the known bat species habit caves for parts of their life histories and 15% of them are currently threatened. In our case, the protection of the caves is suggested to protect their associated fauna (i.e., chiropteran species) and to contribute to the local economy via the ecotouristic activities such as speleology and geotourism. All these elements will constitute a basis for sustainable activities looking for balance between the incomes and the use of natural resources.

5. Conclusion

In this study, we revealed new data on bats in coastal areas of Safi-Essaouira provinces. Recorded data demonstrated the importance of coastal habitats for bats on the western coasts of Morocco and North Africa. Our study highlighted the distribution of eleven bat species belonging to five families. Two species, R. blasii and T. teniotis, are newly recorded in the study area. Equally, this survey discovered for the first time three caves that hosted medium-sized colonies of five species, including Gora’an, Haouya, and Sidi Benkrara caves. The caves of Safi province showed significant importance for bats during the daytime, hibernation, and breeding compared to those visited in Essaouira. In parallel, 10 bat species were identified in foraging habitats with variable dominance. Olive groves were the most diverse site, followed by Safi pinewood and degraded argane forest, followed by Sidi Abderrahmane Lake. The other sites showed a maximum of two species each. The recorded results underline the importance of coastal regions for flying mammals. Equally, this work provides new data on the species richness of bats, reports the importance of caves, sheds light on the annual cycle of insectivorous bats for the first time in the coastal area of Morocco, and informs the concerned sectors and the scientific community of the current situation regarding bat caves and foraging habitats. However, more research is required in these key coastal regions all year round to assess the bioecology of Moroccan bats.

Data Availability

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

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

The authors would like to express their gratitude to the Water and Forest Department for delivering permits to capture bat specimens. The authors are also grateful to Mr. Othmane Boualla, president of the Ocean Association of Speleology (AOS) in Safi, for providing the caving equipment and thanks to Amine Rada and Badar Eddine Souab for accompanying us during cave visits. We are also indebted to several volunteers who helped us in the field and cave visits (Mohammed Khartoumi, Larbi Bakraoui, Hicham Akale, Youness Loudini, Idriss Matar, Abdelatik Gardam, Hamza Labrid, Nabil Louidani, and Zakaria Ellehah).

References

S. Berred, D. Fadli, F. Di Gregorio, and K. Berred, “Geological and landscape particularities of Issafen-style chevron pattern in Tata region (Anti-Atlas, South Morocco),” Arabian Journal of Geosciences, vol. 13, no. 15, p. 689, 2020.
View at: Publisher Site | Google Scholar
W. Squalli, I. Mansouri, I. Douini et al., “Diversity of avian species in peri-urban landscapes surrounding fez in Morocco: species richness, breeding populations, and evaluation of menacing factors,” Diversity, vol. 14, no. 11, p. 945, 2022.
View at: Publisher Site | Google Scholar
F. Médail and K. Diadema, “Glacial refugia influence plant diversity patterns in the Mediterranean Basin,” Journal of Biogeography, vol. 36, no. 7, pp. 1333–1345, 2009.
View at: Publisher Site | Google Scholar
S. Aulagnier, F. Cuzin, and M. Thévenot, “Mammifères sauvages du maroc,”, 2017, https://mammiferesafricains.org/2018/12/mammiferes-sauvages-du-maroc/.
View at: Google Scholar
J. Juste, M. Ruedi, S. J. Puechmaille, I. Salicini, and C. Ibáñez, “Two new cryptic bat species within the Myotis nattereri species complex (Vespertilionidae, Chiroptera) from the western palaearctic,” Acta Chiropterologica, vol. 20, no. 2, pp. 285–300, 2019.
View at: Publisher Site | Google Scholar
S. J. Puechmaille, B. Allegrini, P. Benda et al., “A new species of the; species complex (Chiroptera: Miniopteridae) from the Maghreb Region, North Africa,” Zootaxa, vol. 3794, no. 1, pp. 108–124, 2014.
View at: Publisher Site | Google Scholar
J. Šrámek, V. Gvoždík, and P. Benda, “Hidden diversity in bent-winged bats (Chiroptera: Miniopteridae) of the Western Palaearctic and adjacent regions: implications for taxonomy,” Zoological Journal of the Linnean Society, vol. 167, no. 1, pp. 165–190, 2013.
View at: Publisher Site | Google Scholar
U. Baroja, I. Garin, J. Aihartza et al., “Pest consumption in a vineyard system by the lesser horseshoe bat (Rhinolophus hipposideros),” PLoS One, vol. 14, no. 7, Article ID e0219265, 2019.
View at: Publisher Site | Google Scholar
A. Costa, B. Silva, G. Jiménez-Navarro et al., “Structural simplification compromises the potential of common insectivorous bats to provide biocontrol services against the major olive pest Prays oleae,” Agriculture, Ecosystems & Environment, vol. 287, Article ID 106708, 2020.
View at: Publisher Site | Google Scholar
I. Garin, J. Aihartza, U. Goiti, A. Arrizabalaga-Escudero, J. Nogueras, and C. Ibáñez, “Bats from different foraging guilds prey upon the pine processionary moth,” PeerJ, vol. 7, pp. 71699–e7214, 2019.
View at: Publisher Site | Google Scholar
E. M. Olimpi and S. M. Philpott, “Agroecological farming practices promote bats,” Agriculture, Ecosystems & Environment, vol. 265, pp. 282–291, 2018.
View at: Publisher Site | Google Scholar
M. Riccucci and B. Lanza, “Bats and insect pest control: a review,” Vespertilio, vol. 17, pp. 161–169, 2014.
View at: Google Scholar
D. Russo, L. Bosso, and L. Ancillotto, “Novel perspectives on bat insectivory highlight the value of this ecosystem service in farmland: research frontiers and management implications,” Agriculture, Ecosystems & Environment, vol. 266, pp. 31–38, 2018.
View at: Publisher Site | Google Scholar
T. C. Wanger, K. Darras, S. Bumrungsri, T. Tscharntke, and A. M. Klein, “Bat pest control contributes to food security in Thailand,” Biological Conservation, vol. 171, pp. 220–223, 2014.
View at: Publisher Site | Google Scholar
H. Han, H. Wen, C. Zhou, F. Chen, L. M. Luo, and J.X. J. Liu, “Bats as reservoirs of severe emerging infectious diseases,” Virus Research, vol. 205, pp. 1–6, 2015.
View at: Publisher Site | Google Scholar
D. Lelli, A. Prosperi, A. Moreno et al., “Isolation of a novel Rhabdovirus from an insectivorous bat (Pipistrellus kuhlii) in Italy,” Virology Journal, vol. 15, no. 1, pp. 37–7, 2018.
View at: Publisher Site | Google Scholar
J. Serra-Cobo, M. López-Roig, R. Lavenir et al., “Active sero-survey for European bat lyssavirus type-1 circulation in North African insectivorous bats,” Emerging Microbes & Infections, vol. 7, no. 1, pp. 1–4, 2018.
View at: Publisher Site | Google Scholar
K. Van Brussel and E. C. Holmes, “Zoonotic disease and virome diversity in bats,” Current Opinion in Virology, vol. 52, pp. 192–202, 2022.
View at: Publisher Site | Google Scholar
F. Festa, L. Ancillotto, L. Santini et al., “Bat responses to climate change: a systematic review,” Biological Reviews, vol. 98, no. 1, pp. 19–33, 2022.
View at: Publisher Site | Google Scholar
G. Jones, D. S. Jacobs, T. H. Kunz, M. Willig, and P. A. Racey, “Carpe noctem: the importance of bats as bioindicators,” Endangered Species Research, vol. 8, no. 1–2, pp. 93–115, 2009.
View at: Publisher Site | Google Scholar
H. Rebelo, P. Tarroso, and G. Jones, “Predicted impact of climate change on european bats in relation to their biogeographic patterns,” Global Change Biology, vol. 16, no. 2, pp. 561–576, 2010.
View at: Publisher Site | Google Scholar
D. Russo, V. B. Salinas-Ramos, L. Cistrone, S. Smeraldo, L. Bosso, and L. Ancillotto, “Do we need to use bats as bioindicators?” Biology, vol. 10, no. 8, pp. 693–715, 2021.
View at: Publisher Site | Google Scholar
D. Russo and L. Ancillotto, “Sensitivity of bats to urbanization: a review,” Mammalian Biology, vol. 80, no. 3, pp. 205–212, 2015.
View at: Publisher Site | Google Scholar
H. A. Sherwin, W. I. Montgomery, and M. G. Lundy, “The impact and implications of climate change for bats,” Mammal Review, vol. 43, no. 3, pp. 171–182, 2012.
View at: Publisher Site | Google Scholar
M. Ahmim, Les Mammifères sauvages d’Algèrie: Répartition et Biologie de la Conservation, les Editions du Net, Saint-Ouen, FR, USA, 2019.
M. L. Bendjeddou, I. Bouam, and F. Khelfaoui, “First photographed record of the naked-rumped tomb bat, taphozous nudiventris cretzschmar, 1830 (Chiroptera: emballonuridae), in the grand Maghreb,” African Journal of Ecology, vol. 58, no. 4, pp. 852–854, 2020.
View at: Publisher Site | Google Scholar
R. Dalhoumi, P. Aissa, and S. Aulagnier, “Taxonomie et répartition des chiroptères de Tunisie,” Revue Suisse de Zoologie, vol. 118, pp. 265–292, 2011.
View at: Publisher Site | Google Scholar
S. J. Puechmaille, W. M. Hizem, B. Allegrini, and A. Abiadh, “Bat fauna of Tunisia: review of records and new records, morphometrics and echolocation data,” Vespertilio, vol. 16, pp. 211–239, 2012.
View at: Google Scholar
K. Djilali, M. Sekour, K. Souttou et al., “Diet of short-eared owl asio flammeus (pontoppidan, 1763) in desert area at hassi el gara (el golea, Algeria),” Zoology and Ecology, vol. 26, no. 3, pp. 159–165, 2016.
View at: Publisher Site | Google Scholar
IUCN, “The iucn red list of threatened species,” 2023, https://www.iucnredlist.org.
View at: Google Scholar
S. Aulagnier, A. Bayed, F. Cuzin, and M. Thevenot, “Mammals of Morocco: extinctions and declines during the XX th century,” Travaux de l’Institut Scientifique, vol. 8, no. 8, pp. 53–67, 2015a.
View at: Google Scholar
A. Brosset, “Observations sur la biologie des chiroptères du Maroc oriental,” Bull. Soc. Sci. Nat. Phys., vol. 35, pp. 295–306, 1955.
View at: Google Scholar
A. Brosset, “Note sur Myotis capaccinii et sur Myotis emarginatus, chiroptère nouveau pour le Maroc,” Bulletin of the Russian Academy of Sciences: Physics, vol. 38, pp. 85–98, 1958.
View at: Google Scholar
A. Brosset, “Myotis nattereri, Chiroptère nouveau pour l’Afrique du Nord,” Mammalia, vol. 27, pp. 440–443, 1963.
View at: Google Scholar
A. Brosset and B. Caubères, “La colonie d’Asellia tridens de l’oasis de Figuig,” Mammalia, vol. 24, pp. 222–227, 1960.
View at: Publisher Site | Google Scholar
A. Cabrera, “Los mamíferos de Marruecos,” Trabajos Del Museo Nacional De Ciencias Naturales, vol. 57, 1932.
View at: Google Scholar
H. Foley, “Contribution à l’étude de la faune saharienne,” Bulletin of the Society History, vol. 13, pp. 70–76, 1922.
View at: Google Scholar
H. Heim de Balsac, “État actuel de nos connaissances concernant la faune des Mammifères du Maroc,” Bulletin De La Société Des Sciences Naturelles De, vol. 52, pp. 289–303, 1948.
View at: Google Scholar
J. E. Hill, “Notes on a collection of bats from figuig, Morocco,” Mammalia, vol. 28, no. 1, pp. 83–87, 1964.
View at: Publisher Site | Google Scholar
P. Laurent, “Une forme nouvelle du genre Asellia: A. tridens pallida subsp. nov,” Mammalia, vol. 1, no. 3, pp. 111–116, 1936.
View at: Publisher Site | Google Scholar
P. Laurent, “Présence au Maroc d’une chauve-souris ibérique: Rhinolophus mehelyi carpetanus Cabrera, à Tanger,” Bulletin de la Societe Sciences Nat, vol. 17, pp. 151–153, 1937.
View at: Google Scholar
P. Laurent, “Une chauve-souris nouvelle pour le Maroc: la noctule, Nyctalus noctula Schreber, à Rabat,” Bulletin de la Societe Sciences Nat, vol. 17, pp. 145–150, 1937.
View at: Google Scholar
J. B. Panouse, “Les chauves-souris du Maroc,” Institute Support for Travel, vol. 1, 1951.
View at: Google Scholar
J. B. Panouse, “Observations sur les chauves-souris du Maroc et addition d’une nouvelle espèce Myotis mystacinus (Kuhl,1819) à la faune marocaine,” Bulletin of the Russian Academy of Sciences: Physics, vol. 33, pp. 89–107, 1953.
View at: Google Scholar
J. B. Panouse, “Contribution à l’étude des Chauves-souris du Maroc: Pipistrellus savii et Barbastella barbastellus,” Bulletin of the Russian Academy of Sciences: Physics, vol. 35, no. 3, pp. 259–263, 1955.
View at: Google Scholar
J. B. Panouse, “Présence au Maroc de Nycteris thebaica (Chiroptera),” Bulletin of the Russian Academy of Sciences: Physics, vol. 38, pp. 91–98, 1958.
View at: Google Scholar
J. B. Panouse, “Une nouvelle localité marocaine pour Nycteris thebaica,” Une nouvelle localité marocaine pour Nycteris thebaica, vol. 25, p. 82, 1959.
View at: Google Scholar
W. E. D. Winton, “On a collection of mammals from Morocco,” Proceedings of the Zoological Society of London, vol. 65, no. 4, pp. 953–962, 1897.
View at: Publisher Site | Google Scholar
M. Thévenot, P. Bergier, and P. Beaubrun, “Repartition actuelle et Statut des Rapaces nocturnes au Maroc,” Bievre, vol. 5, pp. 27–39, 1983.
View at: Google Scholar
S. Aulagnier and C. Denys, “Presence du Taphien ventre nu, Taphozous nudiventris, (Chiroptera, Emballonuridae) au Maroc,” Mammalia, vol. 64, no. 1, pp. 116–118, 2000.
View at: Google Scholar
S. Aulagnier and R. Destre, “Introduction à l’étude des Chiroptères du Tafilalt (sud-est marocain),” Mammalia, vol. 49, no. 3, pp. 329–338, 1985.
View at: Publisher Site | Google Scholar
S. Aulagnier and P. Mein, “Note sur la présence d’Otonycteris hemprichii Peters, 1859 au Maroc,” Mammalia, vol. 49, no. 3, pp. 582–584, 1985.
View at: Google Scholar
C. Denys, W. Bogdanowicz, and S. Aulagnier, “First record of Tadarida aegyptiaca (Chiroptera, Molossidae) from Morocco,” Mammalia, vol. 2, pp. 266–268, 1995.
View at: Google Scholar
C. Ibáñez, “Notes on bats from Morocco,” Mammalia, vol. 52, no. 4, pp. 278–281, 1988.
View at: Google Scholar
J. Palmerim, “On the presence of Nyctalus lasiopterus in North Africa,” Mammalia, vol. 46, pp. 401–403, 1982.
View at: Google Scholar
P. Benda, M. Ruedi, and S. Aulagnier, “New data on the distribution of bats (Chiroptera) in Morocco,” Vespertilio, vol. 8, pp. 13–44, 2004.
View at: Google Scholar
T. Dieuleveut, V. Lieron, and H. Yves, “Nouvelles données sur la répartition des Chiroptères dans le Maroc oriental (années 2007 à 2009),” Bulletin de l'Institut Scientifique, Section Sciences de la Vie, vol. 32, no. 1, pp. 33–40, 2010, http://www.israbat.ac.ma/IMG/pdf/05-Dieuleveut.pdf.
View at: Google Scholar
V. Lieron, E. Poulouin, M. Amezian, A. Qninba, and M. Thevenot, “Inventaire des Chiroptères de l ’arrière-pays du port,” Bulletin de l'Institut Scientifique, Section Sciences de la Vie, vol. 30, pp. 53-54, 2008.
View at: Google Scholar
R. Moores and D. Brown, “A range reinforcement of Lesser Leaf-nosed Bat Hipposideros (caffer) tephrus to the lower reaches of the Oued Noun and further mammal records from the Lower Draa,” Go-South Bull, vol. 11, pp. 19–30, 2014.
View at: Google Scholar
S. Aulagnier, “Zoogeographical notes on Moroccan bat fauna,” Myotis, vol. 29, pp. 83–90, 1991.
View at: Google Scholar
P. Bergier, M. Thévenot, and A. Qninba, “Notes naturalistes au Sahara Atlantique marocain-8,” Go-South Bull, vol. 16, pp. 193–249, 2019.
View at: Google Scholar
F. Cuzin, “Au sujet de quelques nouvelles données ultrasonores sur la Grande Noctule (Nyctalus lasiopterus Schreber, 1774) au Maroc Some new ultrasonic data about Greater Noctule bat (Nyctalus lasiopterus Schreber, 1774) in Morocco,” Bulletin de l'Institut Scientifique, Section Sciences de la Vie, vol. 39, pp. 27–35, 2017.
View at: Google Scholar
R. Moores and D. Brown, “New records of bats from southern Morocco (Atlantic Sahara) and notes on echolocation,” Mammalia, vol. 81, no. 6, pp. 611–614, 2017.
View at: Publisher Site | Google Scholar
V. Prié, “Nouvelle donnée de grande noctule Nyctalus lasiopterus (Schreber, 1780) au Maroc,” Vespère, vol. 1, pp. 66–68, 2008.
View at: Google Scholar
E. A. Sehhar, “Diagnostic en mammalogie (Sibe du Jbel Moussa),” Projet Gef De Gestion Des Aires Protegees Tf – 023494 – Mor, vol. 10, 2006.
View at: Google Scholar
A. Benabid, “Les écosystèmes forestiers pré forestiers et pré-steppiques du Maroc: diversité, répartition biogéographique et problèmes posés par leur aménagement,” Forêt Méditerranéenne, vol. 8, no. 1, pp. 53–64, 1985.
View at: Google Scholar
C. Carruesco, Genèse et évolution de trois lagunes du littorale atlantique depuis l’Holocène: Oualidia, Moulay Bou Salham (Maroc) et Arcachon (France), Bordeaux I, Bordeaux, France, 1989.
M. Ferré and J. Ruhard, “Ressources En Eau Du Maroc, Tome 2 Plaines Et Bassins Du Maroc Atlantique,” Editions du Service Geologique du Maroc, vol. 41, 1975.
View at: Google Scholar
O. Boualla, K. Mehdi, and B. Zourarah, “Collapse dolines susceptibility mapping in Doukkala Abda (Western Morocco) by using GIS matrix method (GMM),” Modeling Earth Systems and Environment, vol. 2, no. 1, p. 9, 2016.
View at: Publisher Site | Google Scholar
J. Camus and C. Lamouroux, “Inventaire spéléologique du Maroc,” Direct, Hydraul, vol. 44, 1981.
View at: Google Scholar
M. Barataud, in Écologie acoustique des Chiroptères d’Europe, Muséum National d’Histoire Naturelle, Paris, France, 4th edition, 2020.
P. Benda, J. Červený, A. Konečný et al., “Some new records of bats from Morocco (Chiroptera),” Lynx, vol. 41, pp. 151–166, 2010.
View at: Google Scholar
T. Disca, B. Allegrini, and V. Prié, “Caractéristiques acoustiques des cris d’écholocation de 16 espèces de chiroptères (Mammalia, Chiroptera) du Maroc,” Le Vespère, vol. 3, pp. 209–229, 2014.
View at: Google Scholar
M. Ahmim, R. Dalhoumi, and D. S. Măntoiu, “First data on the acoustic characteristics of some Chiropteran species from northern Algeria,” Bioacoustics, vol. 29, no. 5, pp. 499–517, 2019.
View at: Publisher Site | Google Scholar
S. Aulagnier, P. Haffner, F. Moutou, A. Mitchell-Jones, J. Zima et al., in Guide de mammifères d’Europe, d’Afrique du Nord et du Moyen-Orient, Delachaux et Niestle, Paris, France, 2015.
C. Dietz, O. von Helversen, D. Nill et al., in L’encyclopédie des chauves-souris d’Europe et d’Afrique du Nord: biologie, caractéristiques, protection, Delachaux et Niestle, Paris, France, 2009.
C. Dietz and O. von Helversen, “Illustrated identification key to the bats of europe,” Europe, vol. 1–72, 2004.
View at: Publisher Site | Google Scholar
Y. Dbiba, “Inventaire et révision taxonomique de la collection des chiroptères de l’institut scientifique de rabat: principales familles, richesse spécifique et distribution géographique des sites prospectés,” Travaux de l’Institut Scientifique, vol. 8, 2023.
View at: Google Scholar
S. Aulagnier and M. Thévenot, Catalogue des mammifères du Maroc, Travaux de l’institut scientifique de Rabat, Rabat, Maroc, 1986.
P. Romero Zarco, “Quiropteros de andalucia y marruecos,” Universidad de Sevilla, Sevilla, Spain, 1990.
View at: Google Scholar
S. Aulagnier, “Les chauves-souris cavernicoles du Maroc,” Bullet Spécial Spéléo Maroc, vol. 20, pp. 141–179, 1987.
View at: Google Scholar
F. Biollaz, N. Bruyndonckx, G. Beuneux, M. Mucedda, J. Goudet, and P. Christe, “Genetic isolation of insular populations of the Maghrebian bat, Myotis punicus, in the Mediterranean Basin,” Journal of Biogeography, vol. 37, no. 8, pp. 1557–1569, 2010.
View at: Publisher Site | Google Scholar
V. Aellen, “Rhinolophus blasii Peters (1866), chauve-souris nouvelle pour l’Afrique du Nord,” Mammalia, vol. 19, no. 3, pp. 361–366, 1955.
View at: Publisher Site | Google Scholar
A. E. Morales, “Algunos datos y observaciones sobre mamiferois marroquies,” Bullet Society Española de Historia Natural, vol. 41, pp. 37–47, 1943.
View at: Google Scholar
R. Dalhoumi, P. Aissa, H. Beyrem, and S. Aulagnier, “Annual cycle of bats in a cave of Jebel Errwa, a sub- desert zone of central Tunisia,” Tropical Zoology, vol. 32, no. 3, pp. 155–165, 2019.
View at: Publisher Site | Google Scholar
M. Ahmim and B. Oubaziz, “New data on the distribution of bats (Mammalia: Chiroptera) in Algeria,” Acta Societatis Zoologicae Bohemicae, vol. 81, pp. 17–30, 2017.
View at: Google Scholar
K. J. Park, G. Jones, and R. D. Ransome, “Torpor, arousal and activity of hibernating greater horseshoe bats (Rhinolophus ferrumequinum),” Functional Ecology, vol. 14, no. 5, pp. 580–588, 2000.
View at: Publisher Site | Google Scholar
A. Brosset, “Les mammiferes du Maroc oriental. Leur repartition, leur statut actuel,” Bullet Society Scicence Natural Physical, vol. 40, pp. 243–263, 1960.
View at: Google Scholar
K. Kowalski, J. Gaisler, H. Bessam, C. Issaad, and H. Ksantini, “Annual life cycle of cave bats in northern Algeria,” Acta Theriologica, vol. 31, no. 15, pp. 185–206, plate 7, 1986.
View at: Publisher Site | Google Scholar
R. Dalhoumi, A. Hedfi, P. Aissa, and S. Aulagnier, “Bats of jebel mghilla national park (central Tunisia): first survey and habitat-related activity,” in Tropical Zoology, vol. 27, pp. 53–62, Taylor & Francis, 2014.
View at: Publisher Site | Google Scholar
H. E. Loumassine, N. Bonnot, B. Allegrini, M. L. Bendjeddou, F. Bounaceur, and S. Aulagnier, “How arid environments affect spatial and temporal activity of bats,” Journal of Arid Environments, vol. 180, Article ID 104206, 2020.
View at: Publisher Site | Google Scholar
F. Lisón and J. F. Calvo, “Ecological niche modelling of three pipistrelle bat species in semiarid Mediterranean landscapes,” Acta Oecologica, vol. 47, pp. 68–73, 2013.
View at: Publisher Site | Google Scholar
R. Dalhoumi, N. Morellet, P. Aissa, and S. Aulagnier, “Seasonal activity pattern and habitat use by the Kuhl’s pipistrelle (Pipistrellus kuhlii) in an arid environment,” European Journal of Wildlife Research, vol. 64, no. 3, pp. 36–12, 2018.
View at: Publisher Site | Google Scholar
J. Dorst and J. B. Panouse, “A propos des sérotines du Maroc,” C.R. Society Science Natural Physics, vol. 23, p. 83, 1957.
View at: Google Scholar
W. F. Frick, T. Kingston, and J. Flanders, “A review of the major threats and challenges to global bat conservation,” Annals of the New York Academy of Sciences, vol. 1469, pp. 5–25, 2019.
View at: Publisher Site | Google Scholar
T. J. O’Shea, P. M. Cryan, D. T. S. Hayman, R. K. Plowright, and D. G. Streicker, “Multiple mortality events in bats: a global review,” Mammal Review, vol. 46, no. 3, pp. 175–190, 2016.
View at: Publisher Site | Google Scholar
C. Reusch, M. Lozar, S. Kramer-Schadt, and C. C. Voigt, “Coastal onshore wind turbines lead to habitat loss for bats in Northern Germany,” Journal of Environmental Management, vol. 310, Article ID 114715, 2022.
View at: Publisher Site | Google Scholar
K. C. Tanalgo, H. F. M. Oliveira, and A. C. Hughes, “Mapping global conservation priorities and habitat vulnerabilities for cave-dwelling bats in a changing world,” Science of the Total Environment, vol. 843, Article ID 156909, 2022.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2023 Youssef Dbiba 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

303

Downloads

228

Citations