The bat fauna ( Mammalia : Chiroptera ) of the United Arab Emirates : a review of published records and museum specimens with conservation notes

The bat fauna of United Arab Emirates (UAE) has so far received very little attention. This paper presents a review of published records and voucher specimens in museum collections. We reviewed 39 references and identified 116 records concerning nine species belonging to five families. Fifteen of these records mention 71 specimens of six species in collections. Distribution maps of known locations are provided for each species. Most records (70%) date back more than 10 years and two species have not been recorded for more than 40 years. Based on the bat fauna of Oman, a more thoroughly investigated neighbouring country, the presence of at least nine other, still unrecorded, species is expected. The status of bats in UAE and their conservation concerns are discussed. We encourage further field studies of the bat fauna of UAE.


INTRODUCTION
Rare are the reports of naturalists' observations and wildlife records in the United Arab Emirates before the 1950s.Only a few foreign early travellers took note of the most noticeable fauna and flora species or initiated some wildlife specimen collection (Thomas 1932;Thesiger 1959).Only in the mid 20 th century, the fauna of the territory that would become the United Arab Emirates in 1971, began to receive attention from foreign expatriates or visitors.Bats were no exception, but even today, have still received very little attention, presumably in relation to their cryptic life, difficulties of field investigations, and the apparent low species diversity and abundance compared to other parts of the world.Most knowledge on bat species diversity comes from the surveys conducted by David Harrison in 1953-1955and 1975(Harrison & Bates 1991;Harrison 1955).Only few additional records have been published in the following decades and only the Particolored Bat Vespertilio murinus has been lately added to the species list of bat fauna established by Harrison (Monadjem et al. 2016).
Despite growing concern for environmental conservation in national institutions, the consequences of economic development on wildlife populations are still either not recognized or under-estimated.Field surveys data, well-designed long-term population monitoring programmes and a centralized biodiversity database at the country scale are still largely deficient.Given the data scarcity on the bat fauna of UAE, their population status and trends, how they are impacted by environmental changes is unknown.Bat species diversity might even be greater than currently assessed.

MATERIAL AND METHODS
We reviewed museum specimens and published records (including journals, articles, books and internet pages) to collect species occurrences, map distributions, highlight the gap in data, and stimulate further field investigations in order to better assess the conservation status of the species concerned.We considered as a record every mention of a species per site.Information on the sites and period of collection of museum specimens was also included in counts of record: a site of collection during the period of survey or study, as indicated in the literature, was counted as a single record for each species.All records were geo-referenced with as much precision as allowed by the information provided by authors.
Species distributions were mapped, distinguishing locations already considered by Harrison & Bates (1991) from newer locations, collected in the last 25 years (Fig. 1.).The main natural history museums holding a bat collection have been approached to inquire about their possession of specimens from UAE. Voucher specimens collected from UAE are preserved or deposited in the Harrison Institute (HZM) -Sevenoaks, United Kingdom; Natural History Museum (BMNH) -London, United Kingdom; Zoologisches Forschungsmuseum Alexander Koenig (ZFMK) -Bonn, Germany; Hungarian Natural History Museum (HNHM) -Budapest, Hungary.References of museum specimens were obtained from literature (Harrison 1964;Harrison & Bates 1991;van Cakenberghe & de Vree 1994) or communicated by the HNHM.
The taxonomic nomenclature used follows Wilson & Reeder (2005) with the exception of Rhyneptesicus nasutus after the revision of Juste et al. (2012).

RESULTS
The review of published observations and specimens in collections allowed the identification of 116 records concerning nine species (Table 1).Of these, 60 (51%) were original records; all others being quotes or repetitions of previously published records.For example, six publications mentioning the presence of Triaenops persicus in UAE (Harrison & Bates 1991;Duckworth 1996;Aspinall et al. 2005;Drew et al. 2005;AGEDI 2008;Tourenq et al. 2009), cite the same single original record represented by eight voucher specimens (Harrison 1955).Among the 117 records, 15 referred to 71 specimens of six species that are kept in museum collections.Of the 60 original records, 42 (70%) dated more than 10 years back with an average of 7.5±6.7 records per 10 years (n=8) since the 1940s.This review brings an addition of 43 new records (Table 1) to the synthesis published by Harrison & Bates (1991).

List of species Egyptian Rousette Rousettus aegyptiacus (E. Geoffroy, 1810)
A total of 13 original records of the Egyptian Fruit Bat (Image 1) in UAE have been published.Except for two sightings in Abu Dhabi City in 1998, all other records are from the broad border or in the Hajar Mountains on the eastern part of the country.In these locations, Egyptian Fruit Bats are recorded in gardens, orchards or other plantations, that they frequent for feeding, like in Al Ain, 11381 but benefit from the vicinity of the mountains, where they can shelter in caves or rock clefts.

Persian Leaf-nosed Bat Triaenops persicus (Dobson, 1871)
The Persian Leaf-nosed Bat is only known from a single record of few individuals by Harrison (1955) in the falaj of Al Ain, where it was observed in association with Geoffroy's Trident Leaf-nosed Bat, but in much lower numbers.The species has never been recorded again in UAE for more than 60 years.

Naked-rumped Tomb Bat Taphozous nudiventris (Cretzschmar, 1830)
This might be more widely distributed in UAE, in the Hajar Mountains in particular, than suggested by the five published records.Only one permanent colony is definitely known in the Qarn Nazwa Protected Area of Dubai, where its presence is well known by UAE naturalists.The subspecies present in eastern UAE, was originally referred to T. n. zayidi Harrison, 1955(Harrison & Bates, 1991), currently considered rather a synonym of T. n. nudiventris (Benda et al. 2006), while the specimen found on Das Island has been identified as T. n. magnus, known from Iraq, Iran, Syria and Turkey (Benda et al. 2006).

Particolored Bat Vespertilio murinus (Linnaeus, 1758)
The Particolored Bat is the most recent and only addition to the bat fauna of UAE, since the surveys of Harrison (1955).The dead specimen found in Sharjah was presumably a migrant (Image 4).This species has a large palearctic distribution and known as long distances migrant.The closest records from UAE are in the Zagros Mountains of Iran, attributed to migrating individuals (Benda et al. 2012).

Sind Bat Rhyneptesicus nasutus (Dobson, 1877)
The seven records of Sind Bat are spread all over UAE from the western region of Abu Dhabi to the Hajar Mountains on the eastern coast, and down to Liwa oasis at the border of the Rub-Al Khali Desert (Image 5).The occupied habitats are diverse, including desert oasis, coastal outcrops, artificial tree lines and mountain wadi.

Kuhl's Pipistrelle Pipistrellus kuhlii (Kuhl, 1817)
Kuhl's Pipistrelle is presumably the most widespread species in UAE, and one of the most abundant.Most records were obtained in coastal areas of all emirates except Ajman, including islands (Image 6), but the species is also present inland as illustrated by the records in Al Ain.

Hemprich's Desert Bat Otonycteris hemprichii (Peters, 1859)
The species was recorded only once in UAE in Ras Al Khaimah, and identified from skulls collected in the pellets of a bird of prey.

DISCUSSION
Published records are not systematically well georeferenced and the information provided by authors varied from very accurate description of the sites to mention only of the approximate area in which the species was recorded, limiting the accuracy of the location to more than 10km in some cases.An important part of the records from Harrison's collections in 1953 that initiated the characterization of the bat fauna of UAE, were referred to Buraimi -Al Ain oasis, which was at that time in Oman in its broader sense.Since this expedition, the area has seen profound environmental changes along with urban development, and with the establishment of the United Arab Emirates in 1971, was split between UAE and the Sultanate of Oman, which questions in which present country the records were obtained.Most recent authors have considered these records being from UAE, except van Cakenberghe and de Vree (1994), who placed them in Oman.
This review includes 116 records of nine species, of which 60 are original records, others being citations of previously published accounts.Three species are known from only one record: the records of Persian Leaf-nosed Bat Triaenops persicus, the Hemprich's Long-eared Bat Otonycteris hemprichii date back from 63 and 44 years respectively, whereas the Particolored Bat Vespertilio murinus was found only recently (Monadjem et al. 2016).Their actual presence in UAE cannot currently be ascertained.
This paper overviews the records collected over a period of 70 years, the first one from 1946, and highlights.the poor knowledge we still have on the bat fauna of UAE.Considering distribution data and occurrence in neighbouring countries (Nader 1990;Harrison & Bates 1991;Davis 2007;Benda et al. 2012), other species are expected to be present in UAE.Rhinolophids are likely to be found in Al Ain, since undated bones were discovered in a cave of Jebel Hafeet (Fogg et al. 2002), and an unconfirmed record of a Lesser Horseshoe Bat Rhinolophus hipposideros recently contacted with a bat detector was raised to our attention (J.Smithson, pers. comm. 2015).Geoffroy's Horseshoe Bat Rhinolophus clivosus is also known to occur in eastern Yemen and eastern Saudi Arabia.Blasius's Horseshoe Bat Rhinolophus blasii, the Egyptian Mouse-tailed Bat Rhinopoma cystops, the Egyptian Tomb Bat Taphozous perforatus, the Common Slit-faced Bat Nycteris thebaica, Botta's Serotine Bat Eptesicus bottae, Geoffroy's Myotis Myotis emarginatus, and the Egyptian Free-tailed Bat Tadarida aegyptiaca are all known from Oman in similar habitats found in UAE.The Arabian Pipistrelle Hypsugo arabicus, described in 1979 from specimens caught in wadis of northern Oman, initially considered as an endemic of the Hajar Mountains but subsequently recorded in Baluchistan, southern Iran (Benda et al. 2002) likely also occurs in the UAE.
All bats species recorded in UAE are listed as Least Concern at the international scale on the IUCN Red List of Threatened Species (IUCN 2017).Their status, however, distribution and trends at the regional scale stayed largely unknown and unassessed.In the first Red List of Mammals of UAE (Hornby 1996), all species were listed as Data Deficient except the Egyptian Fruit Bat which was listed as Vulnerable.This list included the Arabian Pipistrelle Hypsugo arabicus, indicating that although lacking any confirmed record, its presence was suspected.In a further national Red List status assessment for the Emirate of Abu Dhabi, all species were still listed as Data Deficient, except Kuhl's Pipistrelle, which was listed as Least Concern (Drew & Tourenq 2005).Knowledge on bats' distribution and abundance has improved little since the publication of these national red lists, and in the absence of additional dedicated surveys, the status of all bat species in UAE should still be considered as Data Deficient.
In UAE, the wealth brought by oil revenues resulted in substantial development of infrastructures and agriculture, along with dramatic changes of life style and human population increase in just a few decades (Tourenq & Launay 2008).With the numerous threats and major direct impacts this fast pace of development brings to bear on the natural environment (habitat loss, fragmentation, over-grazing, occasional hunting, pollution, physical disturbance), bat populations of UAE are most probably threatened and decreasing.In relation with their ecological, behavioural and physiological characteristics, bats might be more sensitive than other taxa to climate changes and habitat loss and are generally in decline due to their sensitivity to environmental stress and slow reproductive rates (Sherwin et al. 2013).Bats are generally recognized as important component of terrestrial ecosystems, providing important ecological services.In UAE and Oman, except the frugivorous Egyptian Fruit Bats, all other species are insectivorous, contributing to regulation of insect populations.Due to their high position in the trophic chain, insectivorous bats are sensitive to accumulations of pesticides and other toxins, and their population might be affected by changes in arthropod preys availability.This makes bats excellent candidates to be used as bio-indicators of the ecosystems in which they live, by measuring their response to climate change and habitat loss (Jones et al. 2009).Bats might also raise economic or human health concerns that are worth investigating.The impact of the Egyptian Fruit Bat on orchards and date palm plantations has not been assessed in UAE, while there are strong suspicions that they are being poisoned in some places.Additionally, bats have been suspected to play a role in human infection by Middle East Respiratory Syndrome (MERS) coronavirus (Memish et al. 2013).
Despite an increasing number of records in the last five years, species distribution, status and trends still remain largely poorly understood.Much remains to be done about the bat fauna of UAE.We encourage and urge naturalists and field ecologists to conduct field surveys on the bat fauna of the United Arab Emirates, and to contribute in the characterization of the echolocation calls of UAE species.Accurate references of echolocation calls and acoustic identification methodology would facilitate the use of bat detectors in identifying species, which can substantially contribute in increasing the number of bats records and knowledge of their status.The efficient use of bat detectors will however be dependent on preliminary captures in order to confirm the species identification.
All bat records reviewed for this paper have been put into a database currently managed at the Emirates Wildlife Society, Dubai.