The Distribution of Bats ( Mammalia : Chiroptera ) in Syria

1 General Commission for Scientifi c Agricultural Research, Douma. P.O. Box 113, Damascus, Syria; a.shehab(at)mail.sy 2 Department of Biology, Nigde University, 51200 Nigde, Turkey; rousettus(at)hotmail.com 3 Department of Biology, Jordan University of Science & Technology, Irbid, Jordan; amrz(at)just.edu.jo 4 Department of Biology, Zonguldak Karaelmas University, 67100 Zonguldak, Turkey; spalaxtr(at)hotmail.coml


Introduction
Most of our knowledge on the bat fauna of Syria is based on old records (WETTSTEIN, 1913;TROUESSART & KOLLMAN, 1923;HARRISON & LEWIS, 1961;ATALLAH & HARRISON, 1967;ATALLAH, 1977;NADER & KOCK, 1983).Only recently some publications focused on the bats of Syria (BENDA et al., 2003a;SHEHAB et al., 2004 and2006;SHEHAB &MAMKHAIR, 2004 and2006).Since 2004 we organized several fi eld trips covering most of Syria for the purpose of studying the biodiversity and ecology of the bat fauna of Syria.
Within the past few years, much interest among Eastern European zoologists focused on zoogeography, systematics and distribution of bats in the Palaearctic Region and the Eastern Mediterranean (BENDA & HORÁČEK, 1998;HORÁČEK et al., 2000;HANÁK et al., 2001;BENDA et al., 2003b;BENDA & KARATAŞ, 2005).These contributions increased our knowledge concerning the distribution and zoogeographical affi nities for several bat species in Syria.Additionally, the Chiroptera of Jordan was intensively studied over the past two decades (QUMSIYEH et al., 1992(QUMSIYEH et al., , 1998;;AMR et al., 2006), where a total of 24 species were recorded.
In this paper, we present data on distribution and ecology of Syrian bats and on their conservation.

Materials and Methods
A total of 27 localities representing different habitats in Syria were visited (see Appendix -Gazetteer).Bats were netted with mist nets (6 × 3 m) placed on caves entrances, paths among old ruins, and near river banks, Bats were also collected by hand from crevices and fi ssures using hand nets and leather gloves.Cranial remains of bats recovered from owl pellets including skulls and mandibles were also examined.The material of this study was prepared as museum specimens (skin and skull), and housed in the collection of the General Commission for Scientifi c Agricultural Research (GCSAR), Damascus, Syria.The lists of new records are arranged in alphabetical order and each record consists of the following information: number of locality as indicated in the map, name of province (muhafaza) (name of district, town or nahiye), name of the locality; date, number of specimen and/or observed bats with their age (juv: juvenile, sad.: subadult= mean pre-breeding animal, not juvenile or breeding adult., ad.: adult), name of the collector(s) and the collection number of museum material deposited in GZCS: A. Shehab collection in GCSAR.

Geographic Setting of Syria
The Syrian Arab Republic is located within the heart of the Middle East with an area of 185,180 km².It borders Turkey to the north, Jordan to the south, Lebanon to the west, and Iraq to the east.Syria is divided into 14 provinces (Muhafaza), namely; Dar'aa, Deyr ez-Zur, es-Sham (Dimashk), Rif Dimashk, es-Suweyda, Kuneitra, Halep, Hamā, el-Haseke, Humus, Idlib, el-Ladhikiye, er-Rakka and Tartus (Fig. 1).Biogeographically, Syria is divided into two main regions; the coastal zone and the Eastern Plateau.The coastal region consists of a narrow, double mountain belt enclosing a depression in the west.These mountains stretch along the Mediterranean Sea from the Turkish border in the north, reaching the Lebanon Mountains in the south.Nusayriye Mountains, a range paralleling the coastal plain, has an average elevation of 1212 meters; the highest peak is about 1575 meters.The western slopes catch moisture from the western sea winds and are thus more fertile and more heavily populated than the eastern slopes.Inland and farther south, the Anti-Lebanon Mountains rise to peaks of over 2700 meters on the Syrian-Lebanese frontier and spread in spurs eastward toward the plateau region.The eastern slopes have little rainfall and vegetation and merge eventually with the desert.In the coastal zone rain fall ranges between 750-1000 mm annually.
The Eastern Plateau comprises the majority of Syria.The entire eastern plateau region is intersected by a low chain of mountains, extending northeastwards from the Jebel el-Arab to the Euphrates River.South of these mountains lies a barren desert region known as the Hamad.North of the Jebel er-Ruwak and east of the city of Humus is another barren area known as the Humus Desert.Northeast of the Euphrates River, which originates in the mountains of Turkey and fl ows diagonally across Syria into Iraq, is the fertile Jazirah region that is watered by the tributaries of the Euphrates.The area underwent irrigation improvements during the 1960s and 1970s, and it provides substantial cereal and cotton crops.In the Eastern Plateau annual rain fall ranges between 150-250 mm.

List of Bat Species
Family Pteropodidae (Fruit Bats)  Remarks: A large colony of around 2000 individuals was observed in a deep cave along the most northern end of the Orontes River (Fig. 3).The cave is prehistoric.Locally it is called "el-Menfa" or "en-Nashiye", implying its diffi cult access and bad smell.Detailed description of this cave was given by SHEHAB & MAM-KHAIR (2004).Bats were roosting in clusters of hundreds to the ceiling (Fig. 4).This cave harbors the Egyptian fruit bats only.On 6 July 2004, 36 (24 females and 12 males) specimens were collected.Most of the collected specimens were sexually mature; males with large scrotal testes (12-13 mm, N= 4).Of the 24 females, nine were pregnant and each with a single foetus, one with a suckling newborn, and six subadults, while the rest has developed teats.On 6 September 2004, 10 specimens (4 males and 6 females) were collected, measured and 6 were subsequently released.Males were sexually mature; two females were with suckling newborns (Fig. 5) and three females were pregnant and gave birth later on 11-13 September 2004.During 6 August 2006, we observed two lactating females with their young and one pregnant female of 9 examined females, which were subsequently released.The population of the Egyptian fruit bat at el-Menfa Cave estimated to be larger on 2006 in contrast to 2004 estimation.The total population was approximately 2000 specimens.

Discussion
ATALLAH (1977) reported that this species is abundant in Lebanon.It was also reported form many localities in Jordan and Palestine (AMR et al., 1987, QUMSIYEH, 1996, AMR, 2000).The Egyptian fruit bat is an African species that penetrated northwards reaching Cyprus, Syria and Turkey.KARATAŞ et al. (2003) showed the distribution of R. aegyptiacus in southern Turkey, and indicated several large colonies (1000-1500 individuals) from Hatay, Mersin, and Antalya provinces.
Measurements of the Syrian population of the Egyptian fruit bat (Fig. 6; Table 2) agree with those given by HARRISON & BATES (1991) for R. a. aegyptiacus collected from Lebanon and Palestine.However, all measurements for the Syrian specimens were larger than those given by KARATAŞ et al. (2003) for the Turkish specimens with the body weight (88±2.9g; 71-150 g) and length of forearm (90±4.9mm: 81-93 mm).SHEHAB & MAMKHAIR (2004) assumed that some of the Turkish specimens were probably subadults, since the forearm length for adults from Lebanon, Palestine and Syria was not less than 87 mm.But one of the authors (A.K.) re-investigated Turkish specimens and they were determined as adults.There is probably a cline in size.
Previous studies reported that R. aegyptiacus often roosts with other bat species.KARATAŞ et al. (2003) re-ported that Rhinolophus ferrumequinum, Rh. euryale, Rh. mehelyi, Myotis myotis, M. blythii, My. capaccinii, and Miniopterus schreibersii were found roosting in the same caves with R. aegyptiacus in Turkey.On the other hand, AMR et al. (1987) found a large colony of R. aegyptiacus with no other bat species in a cave overlooking the Yarmūk River, Jordan.Farmers of the coastal region observed the presence of a bat feeding on their groves of orange and Loquat (Eriobotria japonica) trees.Thus it was possible to locate the fruit bat along the coastal region (SHEHAB & MAMKHAIR, 2004).Also unpublished reports in the Ministry of Agriculture and Agriarian Reform in Syria mentioned damages by fruit bats from ez-Zebadani (near the Syrian Lebanon borders).

Remarks:
A large population of this bat was observed on 13 August 2006 at Ayn Jum'aa near Deyr ez-Zur.About 200-300 animals were spotted in several crevices located on cliffs on the southern side of the Euphrates.Bats were very noisy when approached and moved deeper in the crevices during attempts to capture them.Faecal remains were in relatively large quantity with strong odor.Also, another population was spotted on 14 August 2006 in 9).This colony was hiding in vertical crevices less than 10 cm wide.Hundreds of bats were observed packed in small fl at narrow crevices that extends deep to the inside.Also, one population was observed in an open cave near Ayn Jum'aa, hanging to the highest point of the cave.Despite the effort to capture specimens by mist nets, the animals were hesitant to leave their crevices.
Under the roosting sites of the naked-bellied tomb bat at Ayn Jum'aa, we observed several individuals of the Barn Owl, Tyto alba, and many pellets were collected.Mandibles (4 left and 4 right) of this species and remains of 14 skulls of Pipistrellus kuhlii were re covered.Seven intact skulls of T. nudiventris were re covered from Barn Owl's pellets collected from Hale biyye in 2001, additionally.

Discussion
The naked-bellied tomb bat is very common along the Euphrates and Tigris (HATT, 1959;HARRISON & BATES, 1991); however, its presence in Turkey was only recently confi rmed (SACHANOWICZ et al., 1999;KARATAŞ & SÖZEN, 2003).The measurements of Syrian specimens prove them to represent the large sized subspe-  et al., 1999).External and cranial measurements for the naked-bellied tomb bat, T. nudiventris magnus from Syria are indicated in Table 3.     1996).

Remarks:
A colony of about of 40-50 animals, including juveniles and some females carrying young was observed on 11 August 2006 in an underground dark large room in Kal'at en-Nejm.This castle is located on the southern side of the Euphrates with several alleys and corridors.This colony consists of mostly subadults and few adult individuals.On 13 August 2006 at el-Mesreb Village, two large colonies (500 and 2500 individuals) were found in two separate caves very close to each other.The caves are natural with low roofs not more than 2 meters height.Thick layers (10-20 cm) of fresh and old guano were accumulated across the caves, mainly in the largest cave.Adults have a brilliant reddish orange coloration on the back while subadults are yellowish gray.Similarly most individuals were subadults (about 90 %).Many females carrying young were observed and photographed (Fig. 11).
We visited both caves on 26 March 2006, but observed only piles of guano and not a single bat was seen.The trident leaf-nosed bat was found roosting with no other bat species in el-Mesreb caves, in con-trast to Kal'at en-Nejm, where Eptesicus serotinus, was found to dwell near the roosting site of the trident leaf-nosed bat, however, in separate cellars.Asellia tridens was also recovered along with Eptesicus bottae, Myotis capaccinii, Pipistrellus kuhlii and Taphozous nudiventris from owl pellets collected in Halebiyye, and in combination with P. kuhlii and T. nudiventris at es-Salihiyye (Dura Europus).The farmers declared that they collected guano from el-Abdūl Cave to fertilize their vegetable crops.

Discussion
The trident leaf-nosed bat is a colonial species that occurs across much of Africa, throughout the Middle East and into southwest Asia (HARRISON & BATES,  1991), and can be found in large numbers.DEBLASE (1980) reported on colonies reaching up to fi ve thousand bats in a cave in Iran.Seasonal abundance of this bat was reported; HARRISON (1957) stated that the number of individuals declined sharply in winter and increased again in summer in caves between Ramadi and Habbaniye in Iraq.We have a similar observation in el-Mesreb, where both visited caves were void of bats in March, and two large colonies reappeared in August.External and cranial measurements for the trident leaf-nosed bat are shown in Table 4. er-Rakka: Khatir "Cater" Cave and Pigeon well "Taubenbrunnen" Cave [4], March 1993, C. Ebenau, leg. (EBENAU, 1996).

Family Rhinolophidae (Horseshoe Bats)
Remarks: A colony of about 75 individuals was observed in a dark cellar in Kal'at es-Sem'ān on 20 July 2004 (Fig. 13 A).It was found along with Myotis emarginatus.Another colony of 100-150 horseshoe bats (Rh.ferrumequinum in combination with Rh. euryale) was found in a large room (6m × 6m × 6m) in Kal'at es-Salahaddin (Salahaddin Citadel) (Figs. 14,17).This castle is situated in a dense Mediterranean forest of pine and oak.The room has two entrances and a narrow window.Two clusters of bats were found hanging separately in the roof crevices; one cluster was larger than the other.A huge amount of bat droppings (more than 50 kg) accumulated on the fl oor of the room's center (SHEHAB & MAMKHAIR, 2006).
Most of the collected specimens were sexually mature females without embryos, although, one female had developed teats (3.5 mm)

Discussion
This bat is widely distributed from northern India, south to northwestern Africa and throughout temperate Eurasia including Great Britain and Japan (HARRISON & BATES, 1991;HORÁČEK et al., 2000).In the Middle East, it inhabits the Mediterranean ecozone especially in the mountains and forested regions and avoids extreme desert habitats (QUMSIYEH et al., 1998).This species shares caves with Rh. euryale as well as Rh.hipposideros (QUMSIYEH et al, 1998).ATAL-LAH (1977) also reported that Rh. ferrumequinum and Rh.euryale were found roosting together in groups of 30-50 bats in Lebanon and Jordan, even in the same cluster.In Turkey, RUDOLPH et al. (2005) found the greater horseshoe bat to share a cave with other 8 bat species including Rh. blasii, Rh. euryale, Rh. mehelyi, M. myotis, M. blythii, M. capaccinii, M. emarginatus, and Miniopterus schreibersii in Balıkesir (Turkey), while KARATAŞ et al. (2003) found Rh. ferrumequinum and Rh.euryale roosting in the same cave with Rousettus aegyptiacus in southern Turkey.Several workers addressed the severe decline of this species across its range (MICKLEBURGH et al., 2002).HARRI-SON & BATES (1991) reported a specimen from Tripoli, Syria, referred to Rh. f. ferrumequinum, in BMNH collection; we omitted this record from the Syrian chiropterean fauna, since Tripoli is presently in Lebanon out of the Syrian borders.
External and cranial measurements for the greater horseshoe bat are indicated in Table 5.   Remarks: A solitary hibernating female, hanging in an underground cave used by locals as a shelter for donkeys and horses was collected from Basufān.The specimen collected from Kal'at el-Merkab was also a solitary hibernating male (Fig. 13 B) in a lateral dark underground tunnel (SHEHAB et al., 2006).On 6 August 2006, at least 15 individuals were observed in a cave near Hamama, 100 m north of el-Menfa Cave, most of these animals were subadults or juveniles.
The lesser horseshoe bat is more common in the northern Mediterranean climatic zone rather than in arid re-   7).The superior connecting process of the sella is pointed in side view, and the lancet is triangular without marked concave edge at its base (Fig. 14).The ears are long, pointed and without tragus.The pelage is long, soft and dense, grayish brown in the back, while lighter on the abdomen.The skull is smaller than that of Rh. ferrumequinum (Fig. 17).The GtL is up to 18.6 mm.The rostrum is elevated behind the nasal orifi ce forming pronounced nasal bulb.The sagittal crest is not well developed.The tympanic bullae are small (SHEHAB & MAMKHAIR, 2006).26 bat mummifi ed specimens were collected from a fumigated small room in Kal'at es-Salahaddin on 8 September 2004. 2 mummies belonging to Rh. euryale and the rest (24 mummies) to Myotis emarginatus.We were informed by custodian of Kal'at es-Salahaddin that a local person came and fumigated that room to collect several bats for the use in folk medicine.At our visit on 23 January 2006, the large room in Kal'at es-Salahaddin was unoccupied by any bat, neither by Rh. euryale nor by Rh. ferrumequinum.This may suggest that these two species have the same emigration behaviour.

Discussion
The Mediterranean horseshoe bat is a European species with a distribution that extends the Mediterranean Region and North Africa (HORÁČEK et al., 2000).As mentioned earlier, this bat is associated with Rh. ferrumequinum and inhabits forested areas across it range in the Middle East (AMR et al., 2006).
HARRISON & BATES (1991) stated that there were no details concerning the measurements or lancet shape for specimens previously assigned to Rh. euryale that have been reported from Halep by WETTSTEIN (1913) and from Jerud by TROUESSART & KOLLMAN (1923).Therefore, they are only tentatively referred to Rh. euryale, following DEBLASE (1972).
Remarks: A large colony of 1500-2000 individuals was found in a cave situated along the Orontes River.
The cave is about 150 m long with a height of 20 m.External and cranial measurements of M. myotis from Syria are given in Table 8.
Remarks: Remains of two skulls, one of them intact, were recovered from owl pellets.All previous records from Syria are from the same locality (HARRISON & LEWIS, 1961;NADACHOWSKII et al., 1990).
Remarks: Two specimens were mistnetted in underground cellars in Kal'at es-Sem'ān.These cellars were also inhabited by Rh. ferrumequinum.Many mummifi ed bats were found scattered on the fl oor inside a small underground room (4 × 2.5 × 2.5 m) in Kal'at es-Salahaddin on 8 September 2004.26 intact mummies were collected, 24 of them were belonged to M. emarginatus and two to Rh. euryale (see remarks under Rh.euryale).
Discussion: Geoffroy's Bat has been reported only from mesic forested habitats in Jordan (QUMSIYEH et al., 1998).It inhabits caverns; a large colony that consisting of females only was observed in Mount Carmel (HARRISON & BATES, 1991).Similar fi ndings were reported by RUDOLPH et al. (2005) from a cave near Havran (Balıkesir Prov.),Western Turkey.They also found a nursery, young and females only.They found Geoffroy's Bat sympatric with several Myotis sp. as well as different horseshoe bats.KARATAŞ & ÖZGÜL (2006) mapped the distribution of this species in Turkey, and indicated several localities close to the north-western Turkish-Syrian borders.According to these authors most records of Geoffroy's Bat are from coastal areas.External and cranial measurements of M. emarginatus from Syria are presented in Table 9.
Remarks: On 6 August 2006, a colony of 30-40 bats was observed in a cave near Hamama Village, and about 1 km south of el-Menfa Cave.It was found along with M. myotis and Miniopterus schreibersii.On 24 January 2006, there were only tens of hibernating bats in the same cave, of which we collected four individuals together with Rh. euryale, whereas no M. myotis    Remarks: One individual was observed roosting solitary in a crevice at Kal'at-u Fakhraddin el-Mani, 3 km W Tadmur (Palmyra) on 15 August 2006.This bat was collected in a mistnet and photographed.Later it escaped into a deep narrow crevice in the wall (Fig. 29).

Discussion:
The species was fi rst recorded for Syria by EBENAU (1966).Subsequent collection of owl pellets

Otonycteris hemprichii PETERS, 1859
Hemprich's long-eared bat Distributional Records (Fig. 33):   myotis and less M. capaccinii was found in the cave with together Miniopterus schreibersii (Fig. 21).This may suggest emigration behavior of this species along with M. myotis in winter.Remarks: A complete skull was recovered from an owl pellet (Fig. 37).This is the fi rst record of the European free-tailed bat to Syria.Its cranial measurements as follow: GtL 23.Vertebrate Zoology ■ 57 (1) 2007

Conclucion
Our records belong to 23 bats species in 11 Syrian muhafazas (provinces) (Table 16).Of these muhafazas, Halep looks like the richest muhafaza with eleven bat species.In el-Ladhikiye we found eight, in Humus and Idlib seven, in Deyr ez-Zur six, in es-Sham fi ve, in Tartus three, in Hamā and el-Haseke two, and in Dar'aa only one species.Of all species, Pipistrellus kuhlii is the most common and was found in all eleven muhafazas.We analysed the records summarized in Table 16 using the software MVSP 3.2.With respect to this cluster analysis (Fig. 38), Syria can be divided into three zones: (1) Mediterranean zone including Idlib, el-Ladhikiye, es-Sham, and Tartus.(2) Dry zone (steppe, desert and semi-desert areas) including Deyr ez-Zur, Halep, Humus, and er-Rakka.(3).Transitional zone including Dar'aa, Hamā, and el-Haseke.
The last zone is transitional zone between fi rst and second zones and has a relatively poor fauna with a low number of bat species.Pipistrellus kuhlii and Myotis myotis were recorded from Hamā, and Plecotus macrobullaris from el-Haseke (Table 16).
The Egyptian Fruit Bat, R. aegyptiacus, seems to be confi ned to one locality on the inner coastal  Tab.16.Syrian bat records with respect to its province (muhafaza).
mountains.It probably never succeeded to penetrate eastwards despite the presence of large water bodies.Similar observations were reported from south western Turkey (KARATAŞ et al., 2003).
The caves along the Orontes River, such as el-Menfa cave should be declared as an Important Mammal Area, since it harbours a large number of bats and also relatively high species richness (one cave with 4 species, and one cave with a large population of the Egyptian Fruit Bat).
Similarly, el-Mesreb caves near the Euphrates harbour a large population of Aselia tridens.The Syrian authorities responsible for nature conservation should adopt a strategy to protect such populations.
cies T. n. magnus.The occurrence of T. n. magnus on the Syrian Euphrates is part of a northwestern extension of the Iraqi population, extending into southern Turkey to near Nizip, Gaziantep Prov.(SACHANOWICZ

Fig. 13 .
Fig. 13.A small colony of the greater horseshoe bat, Rhinolophus ferrumequinum, in a cellar at Kal'at es-Sem'ān (A) and a solitary hibernating lesser horseshoe bat, Rh. hipposideros, in a cave at Kal'at el-Merkab (B).

Tab. 5 .
External and cranial measurements (mm) and weight (g) of the greater horseshoe bat, Rh. ferrumequinum from Syria.

Fig. 17 .
Fig. 17.Dorsal view of the skulls of Rh. euryale (left) and Rh.ferrumequinum (middle) and lateral view of Rh. euryale (right) from northern Syria (the arrow is pointing to the fi rst upper premolar).
from Halep.External and cranial measurements (mm) of the Mediterranean horseshoe bat, Rh. euryale from Syria.

Table 11 .
External and cranial measurements (mm) and weight (g) of Kuhl's pipistrelle, Pipistrellus kuhlii.BENDA & RUEDI (2004)divided the Western Palaearctic P. kuhlii into three distinct subspecies.One corresponds to the nominative subspecies P. k. kuhlii (circum-Mediterranean), one to a desert form P. k. deserti living in the Sahara and P. k. lepidus is distributed in the Middle East (Syria and Iran).