Echolocation calls for 11 species recorded from Jordan.
Abstract
The diversity and the conservation status of bats in Jordan are discussed based on recent studies. The bat fauna of Jordan consists of 26 bat species belonging to nine families (Emballonuridae, Hipposideridae, Pteropodidae, Miniopteridae, Molossidae, Nycteridae, Rhinolophidae, Rhinopomatidae, and Vespertilionidae). Bat echolocation calls for some selected species are included. Conservation status based on regional assessment according to the IUCN standards is amended, along with the current legislative laws for the conservation of bats. Threats affecting the bats of Jordan are highlighted including the recent introduction of wind farms and other mining activities. In addition, the role of bats in disease transmission is included.
Keywords
- bat
- diversity
- threats
- Jordan
1. Introduction
Jordan is situated at a crossroad between three continents and with diverse habitats (Mediterranean, Saharo-Arabian, Irano-Turanian, and Afro-tropical). Although Jordan is a small country, the bat fauna is diverse with 26 species representing nine families. Within the past four decades, our knowledge of the bats of Jordan expanded significantly, adding new records [1, 2, 3], distributional data [4, 5, 6, 7, 8, 9, 10, 11, 12], ectoparasites [13], karyotypic studies [14, 15], activity patterns [16], and conservation [17]. Yet, these studies also pointed out a significant shortage in our knowledge especially about the ecology and conservation of the bat fauna of this country. Benda et al. [18] published the most comprehensive and up-to-date manuscript on the bats of Jordan, including distributional data, ecology, echolocation, ectoparasites, and zoogeographical analysis.
This summary on the bats of Jordan is based on cumulative research and field observation since 1978. Over the past four decades, the senior author was involved in numerous studies on various aspects of the mammalian fauna of Jordan, including bats. As a result, several additional records of the bat fauna were added, and further knowledge on habitat preference and threats affecting bats in Jordan was gained. As a developed country, Jordan witnessed accelerated changes in its natural setting (water resources, agricultural practices, urination, mining, etc.), which, in turn, affected the well-being of several species of animals, including bats.
2. Biogeography of Jordan
Jordan is influenced by four major biogeographic regions (Figure 1). Vegetation cover, soil texture, altitude, and annual rainfall are among the major factors that shaped these biogeographic regions. Several types of habitats are present in Jordan, ranging from extreme desertic to mild-forested Mediterranean (Figure 2). It was agreed on the delineation of these four regions based on vegetation cover as well as animal distribution in Jordan [19, 20].
2.1 The Mediterranean region
This area is represented by mountain ranges extending from Irbid in the north near to the south around Ra’s Al Naqb. This region is characterized by the presence of several types of forests (The Phoenicean juniper,
2.2 Irano-Turanian region
This area surrounds the Mediterranean region from the west and the east. It extends to the Syrian Desert to the northeast. Few scattered trees can be observed, mainly
2.3 Sudanian penetration region
This ecozone extends from southern Jordan near Aqaba Gulf along Wadi Araba reaching the southern part of the Jordan Valley near Dayr Alla northward. It also extends to southeastern Jordan near Wadi Ram, the largest sandstone mountain formation and granite mountains to the east. Altitudes range from 400 m bls around the Dead Sea area to as high as 1734 m asl for Jabal Ram mountain. Precipitation is of less than 50 mm annually. Two species of Acacia occur in this region in varying densities,
2.4 Saharo-Arabian region
This region constitutes the largest biogeographical region, covering about 70% of Jordan. It spreads to the east bordering the Irano-Turanian region from the west and the Sudanian Penetration region from the southwest.
3. Bat diversity in Jordan
The bat fauna of Jordan consists of 26 bat species belonging to nine families (Emballonuridae, Hipposideridae, Pteropodidae, Miniopteridae, Molossidae, Nycteridae, Rhinolophidae, Rhinopomatidae, and Vespertilionidae). Figure 3 shows some representative species.
3.1 Family Pteropodidae
This family of fruit bats includes a single species, the Egyptian fruit bat,
3.2 Family Rhinopomatidae
This family is represented by two species, the greater rat-tailed bat,
3.3 Family Rhinolophidae
This family includes six species inhabiting a variety of habitats. Geoffroy’s horseshoe bat,
3.4 Family Emballonuridae
The tomb bat,
3.5 Family Hipposideridae
The trident leaf-nosed bat,
3.6 Family Miniopteridae
3.7 Family Molossidae
The European free-tailed bat,
3.8 Family Nycteridae
The Egyptian slit-faced bat,
3.9 Family Vespertilionidae
This is the most diverse family in Jordan and is presented by seven genera (
The Asian barbastelle,
Christie’s big-eared bat,
Kuhl’s pipistrelle,
The lesser mouse-eared bat,
4. Bat echolocation calls
Bat echolocation calls for 11 bat species from Jordan are documented. Figure 4 and Table 1 show recorded calls and durations and frequency variables using Song meter from different localities.
Species | No. of calls | D [ms] | SF [kHz] | EF [kHz] | PF [kHz] |
---|---|---|---|---|---|
116 | 28.7 ± 12.3 | 85.8 ± 1.7 | 85.9 ± 1.7 | 86.2 ± 0.8 | |
7 | 23.4 ± 15.2 | 105.3 ± 0.9 | 98.5 ± 7.4 | 105.8 ± 0.5 | |
107 | 42 ± 10.5 | 75.7 ± 4 | 77.9 ± 6.5 | 82.2 ± 0.5 | |
145 | 29.8 ± 13 | 107 ± 4.8 | 107 ± 5.1 | 111 ± 1.39 | |
14 | 3.6 ± 2.25 | 35.2 ± 1.9 | 28.94 ± 0.9 | 31.2 ± 0.85 | |
103 | 8.7 ± 3.3 | 115 ± 2 | 109 ± 6.2 | 116 ± 2 | |
105 | 5.6 ± 2 | 38.1 ± 4 | 30.8 ± 1 | 32.6 ± 1.2 | |
76 | 5.53 ± 1.57 | 50.5 ± 6.3 | 39.3 ± 2.2 | 40.4 ± 2.2 | |
130 | 5 ± 2 | 51.7 ± 5 | 47.9 ± 2.6 | 48.4 ± 2.4 | |
7 | 2.3 ± 0.9 | 46.8 ± 3.5 | 37.2 ± 3.5 | 41.8 ± 3 | |
26 | 66 ± 1.02 | 20.2 ± 2.3 | 15.06 ± 0.12 | 15.2 ± 0.5 |
Species of the genus
All of the calls are within the range of previous studies in the Middle East [21, 22, 23]. Table 2 lists frequencies for bats recorded from the Negev desert on the opposite side of Jordan. It clearly shows that calls reported in our study are similar for most species.
Cave | Type | Number of bat species recorded | Species observed | References |
---|---|---|---|---|
Al Hamma | Karstic | 1 | [7, 18] | |
Al Majdal | Karstic | 2 | [11] | |
Al Wardeh | 5 | [18] | ||
Al-Mahhatta | Pressure ridge | 1 | [1] | |
Ar Raddass | 1 | [18] | ||
Arjan | 2 | [18] | ||
Bir Hamma cave | Lava | 1 | [18] | |
Dhana village caves | Sandstone | 2 | [18] | |
Dibbin Forest caves | 4 | [1, 11, 14, 18] | ||
Iraq Al Amir | Artificial | 6 | [18] | |
Iraq Al Wahaj | Karstic | 6 | [18] | |
Jabal Al Bayda | Sandstone | 2 | [18] | |
Jesus’ cave | 1 | [18] | ||
Lot’s cave | 1 | [18] | ||
Mahjub cave | Sandstone | 3 | [18] | |
Malka cave | Artificial | 1 | [18] | |
Mgharet Issa | 1 | [18] | ||
Mogharet Al-Roum Cave | 1 | [1] | ||
Mukawir | 1 | [18] | ||
Qaraiqira cave | 1 | [11] | ||
Tabaqat Fahl | Artificial | 5 | [14, 18] | |
Umm Al Iraq | 1 | [18] | ||
Wadi Al Hasa | 1 | [18] | ||
Wadi Ben Hammad | Limestone | 1 | [20] | |
Wadi Dhana | Sandstone | 1 | [18] | |
Wadi Dharih | Karstic | 1 | [18] | |
Wadi Shu’ayb | 1 | [18] | ||
Zubiya | Karstic | 6 | [18] |
5. Bat caves in Jordan
A total of 142 caves and dwelling areas suitable for bats have been mapped (Figure 5). Caves are classified, as lava tunnel, pressure ridge, artificial, limestone, karstic, and sandstone caves. Most of the caves are located along the mountainous ridge extending from the north to the south on the western side of the country. Other sites include historical castles, mine-shafts, man-made tunnels, and rock crevices.
Based on previous studies over the past 30 years, the bat faunae for 28 caves are summarized in Table 2. The number of bat species per cave ranged from six to one, whereas Al Wardeh, Iraq Al Amir, Iraq Al Wahaj, and Zubiya caves harbored six species. It seems that cave size is related to the number of bat species recorded; Zubiya, Al Wardeh, Dibbin Forest caves, and Iraq Al Wahaj are large caves extending over 300–500 m, while smaller caves usually are inhabited by a single bat species (Table 2). Other bat species such as
Our current projects on the bats of Jordan are to study the bat fauna associated with caves and identify threats that can affect bat populations. On the other hand, a campaign to protect bat important cave areas through legislative authorities is among high-priority issues.
6. IUCN conservation status of bats in Jordan
Eid et al. [24] compiled the national red list for the mammals of Jordan. Of the 26 bat’s species, one, nine, and three species were listed as critically endangered, endangered, and near threatened, respectively (Table 3). At the global level,
Species | Common name | National IUCN status | Global IURCN status |
---|---|---|---|
Mehely’s horseshoe bat | CR | VU | |
Mediterranean horseshoe bat | EN | NT | |
Greater horseshoe bat | EN | LC | |
Greater mouse-tailed bat | EN | LC | |
Egyptian tomb bat | EN | LC | |
Naked-rumped tomb bat | EN | LC | |
Egyptian slit-faced bat | EN | LC | |
Pale bent-wing bat | EN | LC | |
Lesser mouse-eared bat | EN | LC | |
Geoffroy’s bat | EN | LC | |
Trident leaf-nosed bat | VU | LC | |
Egyptian fruit bat | NT | LC | |
Lesser horseshoe bat | NT | LC | |
Asian barbastelle | NT | LC | |
Long-fingered bat | DD | VU | |
Blasius’s horseshoe bat | LC | LC | |
Geoffroy’s horseshoe bat | LC | LC | |
Egyptian mouse-tailed bat | LC | LC | |
European free-tailed bat | LC | LC | |
Botta’s serotine | LC | LC | |
Desert pipistrelle | LC | DD | |
Natterer’s bat | LC | LC | |
Desert long-eared bat | LC | LC | |
Kuhl’s pipistrelle | LC | LC | |
Common pipistrelle | LC | LC | |
Christie’s big-eared bat | LC | DD |
Jordan is a member of several conventions, treaties, and agreements related to the provide protection for wildlife (Convention on Biological Diversity, Convention on International Trade in Endangered Species of Wild Fauna and Flora, Treaty of Conservation of Migratory Species of Wild Animals, Convention on the Protection of Marine Pollution by Preventing the Disposal of Waste and other Materials, RAMSAR, United Nations Convention to Combat Desertification). Several national laws have been enacted at the national level. In addition, the Agriculture Law No. 13 of 2015 addresses to a large extent Jordan obligations related to the protection of wildlife under these conventions [20].
Regulation No. Z/2 for the year 2021 regulates wildlife protection, hunting, and trade. This bylaw was issued in accordance with article No. 56, of the Agriculture Law No (13) for the year 2015. Bylaw No. 43 for the year 2008 categorized mammals and other wildlife banned from hunting according to its level of protection (Table 4). This bylaw was issued in accordance with article No. 56, paragraph (H) of the Agriculture Law No (13) for the year 2015. In addition, Regulation No (Z/2) for the year 2021 includes instructions of regulating the International Trade in Endangered Species of Wild Fauna and Flora under Article (56) of the Agriculture Law No (13) for the year 2015 [20].
Common name | Scientific name |
---|---|
Egyptian Fruit Bat | |
Long-fingered Bat | |
Natterer’s Bat |
7. Threats affecting the bats of Jordan
7.1 Deforestation
7.2 Urbanization
Over the past 70 years, the population of Jordan increased 17-folds during reaching 10,320,000 by 2021. A great burden on the natural and wild habitats due to this accelerated population increase became evident with the expansion of cities, towns, and villages. Construction style using cement was by far the most important factor that affected bat populations. Previously, old houses were built using mud, wood, or stone, creating suitable habitat for bat roosting. Many of these old houses are by now demolished and replaced by modern buildings [17]. Al Mahatta cave in Amman that used to harbor a population of the Egyptian Fruit Bat is by now void of bats due to housing projects that changed its integrity.
Noise and light pollution and heavy traffic disturbed many bats populations that are sensitive to human activity. One of the most evident examples of the disturbance that affected bat habitats is the disappearance of a healthy population of
7.3 Tourism and vacationing
Tourism and outdoor activities in wild habitats (e.g., Dibbin Forests, Wadi Ram, and Zubiya) have a direct impact on the roosting populations of bat species living in such habitats. For example, large colonies of
The Egyptian Fruit Bat populations declined or disappeared from several sites where it used to be in abundance. Al Hemma cave is a classic example, where it used to harbor thousands of bats [7]. By now, only a few hundreds of the fruit bats were present and continued to decline. Also, the population of the Egyptian Fruit Bat in Wadi ben Hammad is declining due to extensive tourism activities within the vicinity of this site. The Zubiya cave, one of the largest karstic caves in Jordan, whereas seven bat species were previously recorded (
Recently, many caves were turned into restaurants and coffee shops. This was observed in Asef cave where it was remodeled as a recreation site, and all bats were exterminated (Figure 7A).
7.4 Mining
In recent years, mining for extraction minerals for the cement industry and rocks for buildings expanded in many parts of the country. This in turn brought many bat populations to their demise. For example, Al Wardeh cave located near Ajlun was inhabited by large colonies of
Another cave used to harbor a significant population of over 500 individuals of
7.5 Wind power projects
In the past decade, windmills projects increased to reach up to six operational sites mostly in the southwestern part of the country, with a total of 151 turbines (Figure 8). Cumulative effect assessment was developed for Al Tafilah site to help in determining bat species that are at the highest risk and to identify potential mitigations and monitoring measures that should be considered by investors [26]. Eight species of bats were identified of major or moderate risk ratings (Table 5).
Species | Species sensitivity | Eurobats level of collision risk | Likelihood of effect score | Risk rating |
---|---|---|---|---|
Low | Unknown | Low | Minor | |
Medium | Low | Negligible | Negligible | |
High | Low | Negligible | Minor | |
Low | Unknown | Low | Minor | |
Low | Medium | Medium | Minor | |
Medium | High | High | Major | |
Medium | Low | Negligible | Minor | |
Low | Unknown | Low | Negligible |
Carcasses of bats are surveyed on a monthly basis in the operational sites. We are aware of bat mortality in these sites; however, data remain undisclosed for the meantime.
7.6 Folk medicine and other practices
Bat blood is prescribed for female infants so no hair will grow under their armpits [27]. Fresh bat’s blood is applied to the newborn body. This belief was adopted from the Roman culture and remained practiced by the local people in many parts of the Middle East that were under the Roman Empire, but is not practiced on a large scale.
Search for red mercury became a threat to bats in Jordan in the past 10 years. Many locals strongly believed that red mercury can be found in bat’s nests. Caves and colonies in many parts of the country were disturbed in pursue of the red mercury to sell it at a high price. A campaign to educate the public that bats do not form nests through all forms of public media was undertaken.
7.7 Bats caves as animal barns
Scattered caves in the country have been used as sheep or goat’s barns. Caves were sat on fire first to remove all kinds of wild animals such as snakes, scorpions, birds, and bats. This practice was observed in the caves of Jarash and Ajlun mountains (Figure 7B).
8. Bats and diseases in Jordan
Since the emergence of the Middle East Respiratory Syndrome Coronavirus (MERS-CoV) in Jordan in 2012 [28], health authorities and research institutes collected blood samples from the Egyptian fruit bat,
Although human rabies is considered very rare in Jordan, six isolates of rabies were found in wild animals (badger and squirrel) and domestic animals (cow, dog, donkey, and goat) [31]. No information is available on rabies caused by bats in Jordan. Further studies should evaluate the role of zoonotic infections that could be possibly transmitted by bats.
9. Conclusion
This study shed the light on the urgent need to conserve the bats of Jordan, taking into consideration the alarming decline in bat populations observed over the past decades affecting their natural habitats. Further studies on the ecological requirements and habitat selection for the bats of Jordan are needed. Such studies will provide baseline data to implement conservation strategies for each species. Other avenues of future research include identification, both quantitatively and qualitatively, the impacts of various man-made changes and threats to the existing bat population.
Acknowledgments
We would like to thank Qamar Almimi (RSCN) for map preparations. Also we thank Thabit Al Share, Sameh Khatatbeh, and Mohammad Al Zoubi (The Royal Society for the Conservation of Nature) for their help in the field studies. This study was supported in part by the Deanship of Academic Research, Jordan University of Science & Technology.
References
- 1.
Qumsiyeh MB. New records of bats from Jordan. Säugetierkundliche Mitteilungen. 1980; 28 :36-39 - 2.
Darweesh N, Al-Melhim WN, Disi AM, Amr ZS. First record of the naked bellied tomb bat, Taphozous nudiventris Cretzschmar 1830, from Jordan. Zoology in the Middle East. 1997;15 :13-14. DOI: 10.1080/09397140.1997.10637732 - 3.
Al-Omari K, Abu Baker M, Amr Z. First record of the Egyptian slit-faced bat, Nycteris thebaica E. Geoffroy, 1818, from Jordan. Zoology in the Middle East. 2000;21 :5-7. DOI: 10.1080/09397140.2000.10637826 - 4.
Atallah SI. Mammals of the Eastern Mediterranean region: Their ecology, systematics and zoogeographical relationships. Säugetierkundliche Mitteilungen. 1977; 25 :241-319 - 5.
Atallah SI. Mammals of the Eastern Mediterranean region: Their ecology, systematics and zoogeographical relationships. Säugetierkundliche Mitteilungen. 1978; 26 :1-50 - 6.
Nader IA, Kock D. Notes on some bats from the Near East (Mammalia: Chiroptera). Zeitschrift für Säugetierkunde. 1983; 48 :1-9 - 7.
Amr ZS, Woodbury SC, Disi AM. On a collection of mammals from Jordan. Dirasat: Series B. 1987; 14 :131-136 - 8.
Bates PJJ, Harrison DL. New records of small mammals from Jordan. Bonner Zoologische Beiträge. 1989; 40 :223-226 - 9.
Amr ZS, Disi AM. Jordanian Mammals Acquired by the Jordan University Natural History Museum. Amman: Publication of the University of Jordan; 1988. 32 pp - 10.
Qumsiyeh M, Disi A, Amr Z. Systematics and distribution of the bats (Mammalia: Chiroptera) of Jordan. Dirasat. 1992; 19 :101-118 - 11.
Qumsiyeh MB, Amr ZS, Al-Oran RM. Further records of bats from Jordan and a synopsis. Turkish Journal of Zoology. 1998; 22 :277-284 - 12.
Benda P, Sádlová J. New records of small mammals (Insectivora, Chiroptera, Rodentia, Hyracoidea) from Jordan. Časopis Národního Muzea Řada Přírodovědná. 1999; 168 :25-36 - 13.
Amr ZS, Qumsiyeh MB. Records of bat flies from Jordan, Libya and Algeria. Entomological News. 1993; 104 :43-46 - 14.
Qumsiyeh M, Schlitter D, Disi A. New records and karyotypes of mammals from Jordan. Zeitschrift für Säugetierkunde. 1986; 51 :139-146 - 15.
Karatas A, Weydan M, Sozen M, Shehab A, Amr Z. Karyotypes of bats (Chiroptera: Rhinolophidae, Vespertilionidae) from Jordan. Arab Gulf Journal of Scientific Research. 2008; 26 :193-198 - 16.
Abed OA, Abu Baker MA, Amr ZS. Seasonal habitat selection and temporal activity patterns determine the structure of Mediterranean bat assemblages. Zoology in the Middle East. 2019; 65 :11-19. DOI: 10.1080/09397140.2018.1540151 - 17.
Amr Z, Abu Baker M, Qumsiyeh M. Bat diversity and conservation in Jordan. Turkish Journal of Zoology. 2006; 30 :235-244 - 18.
Benda P, Lučan RK, Obuch J, Reiter A, Andreas M, Bačkor P, et al. Bats (Mammalia: Chiroptera) of the Eastern Mediterranean and Middle East. Part 8. Bats of Jordan: Fauna, ecology, echolocation, ectoparasites. Acta Societas Zoologicae Bohemicae. 2010; 74 :185-353 - 19.
Al-Eisawi D. Vegetation in Jordan. In: Haotot A, editor. Studies in the History and Archeology of Jordan. Vol. 1. Amman: Department of Antiquities; 1985. pp. 45-57 - 20.
Amr ZS. The Mammals of Jordan. 2nd ed. Amman: Al Rai Press; 2012. p. 308 - 21.
Hackett TD, Korine C, Holderied MW. The importance of Acacia trees for insectivorous bats and arthropods in the Arava Desert. PLoS One. 2013; 8 (2):e52999. DOI: 10.1371/journal.pone.0052999 - 22.
Hackett TD, Holderied MW, Korine C. Echolocation call description of 15 species of Middle-Eastern desert dwelling insectivorous bats. Bioacoustics. 2017; 26 :217-235. DOI: 10.1080/09524622.2016.1247386 - 23.
Benda P, Dietz C, Andreas M, Hotový J, Lučan RK, Maltby A, et al. Bats (Mammalia: Chiroptera) of the Eastern Mediterranean and Middle East. Part 6. Bats of Sinai (Egypt) with some taxonomic, ecological and echolocation data on that fauna. Acta Societas Zoologicae Bohemicae. 2008; 72 :1-103 - 24.
Eid E, Abu Baker M, Amr Z. National Red Data Book of Mammals in Jordan. Amman, Jordan: IUCN Regional Office for West Asia, Amman; 2020. p. 130. DOI: 10.2305/IUCN.CH.2020.12.en - 25.
Harrison DL. Footsteps in the Sand. London: Ernest Benn Limited; 1959. p. 256 - 26.
International Finance Corporation. Tafila Region Wind Power Projects Cumulative Effects Assessment. Washington, DC, USA; 2017 - 27.
Aldebsawi AA, Al-Najdawi MM, Jarrar QB, Saleh MM, Moshawih SF. Middle Easterns’ knowledge about bat blood use and effectiveness in preventing hair growth: A questionnaire survey. Archives of Pharmacy Practice. 2021; 12 :29-33. DOI: 10.51847/XdT8clmkcV - 28.
Al-Abdallat MM, Payne DC, Alqasrawi S, Rha B, Tohme RA, Abedi GR, et al. Hospital-associated outbreak of Middle East respiratory syndrome coronavirus: A serologic, epidemiologic, and clinical description. Clinical Infectious Diseases. 2014; 59 :1225-1233. DOI: 10.1093/cid/ciu359 - 29.
Kandeil A, Gomaa M, Nageh A, Shehata MM, Kayed AE, Sabir JMS, et al. Middle East Respiratory Syndrome Coronavirus (MERS-CoV) in dromedary camels in Africa and Middle East. Viruses. 2019; 11 :717. DOI: 10.3390/v11080717 - 30.
Shehata MM, Chu DKW, Gomaa MR, AbiSaid M, El Shesheny R, Kandeil A, et al. Surveillance for Coronaviruses in Bats, Lebanon and Egypt, 2013-2015. Emerging Infectious Diseases. 2016; 21 :148-150 - 31.
David D, Hughes GJ, Yakobson BA, Davidson I, Un H, Aylan O, et al. Identification of novel canine rabies virus clades in the Middle East and North Africa. Journal of General Virology. 2007; 88 :967-980. DOI: 10.1099/vir.0.82352-0