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Systematic Review

Bats of Bangladesh—A Systematic Review of the Diversity and Distribution with Recommendations for Future Research

by
Md Ashraf Ul Hasan
* and
Tigga Kingston
Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409, USA
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(12), 1042; https://doi.org/10.3390/d14121042
Submission received: 2 October 2022 / Revised: 20 October 2022 / Accepted: 27 October 2022 / Published: 28 November 2022
Browse Figures
Review Reports Versions Notes

Abstract

:
Bangladesh is at the ecological transition between the Indo-Himalayan and Indo-Chinese subregions. The country also has one of the highest human population densities in the world and only 6% remaining natural habitat, putting much of its biodiversity at risk. With more than 1455 species worldwide, bats are an important, but threatened, component of global biodiversity and provide critical ecosystem services. Yet, there is no comprehensive work on species occurrence, diversity, or richness of bats of Bangladesh. Here, we collated data on the bats of Bangladesh and states in neighboring countries from the available literature, the Global Biodiversity Information Facility, and museum databases to assess the probability of occurrence of bat species in Bangladesh and created distribution maps for each species. We confirmed 31 species from 8 families, of which 22 were associated with voucher specimens and 9 recorded based on photographs, or human observation. A further 81 species were categorized as Highly Probable (38 species), Probable (33), and Possible (10) in Bangladesh based on the distribution in neighboring states and habitat preferences. The shortfall in confirmed versus potential species highlights the need for rigorous surveys to fully document and characterize the bat diversity of Bangladesh.

1. Introduction

Over 1455 species of bats have been described worldwide [1] of which ~37% occur in the Asian continent [2]. Within Asia, much of this diversity resides in the Indian subcontinent, the physiogeographical region comprising Bangladesh, Bhutan, India, Maldives, Nepal, Pakistan, and Sri Lanka. The first comprehensive work on the subcontinent (except the Maldives) reported 119 species of bats in 37 genera belonging to 8 families [3], and current estimates stand at 141 species from 49 genera and 10 families [4]. However, within the subcontinent, most recent research has come from India, or has been heavily focused on disease emergence from Pteropus medius, especially in Bangladesh and Pakistan. A topic-based literature search of the Web of Science (WoS) database for studies on bats over the past ~75 years (excluding bat-borne virus-related research) found 128 publications from India, 35 from Pakistan, 20 from Myanmar, 13 from Sri Lanka, 12 from Nepal, 8 from Bangladesh, 1 from Bhutan, and no research from the Maldives (Supplementary Materials Listing S1). Although, additional information is likely available in non-indexed journals and the grey literature, the differential effort across the Indian subcontinent is striking.
Bangladesh is a small country (148,460 square km) and a junction for the flora and fauna of the Indian subcontinent and Southeast Asia [5]. The country is bordered by India and Myanmar, with Nepal, Bhutan, and China within 65 miles of the northern border (Figure 1A). Bangladesh is dominated by the deltaic floodplain of the Ganges [6], but there are three distinct forest types in the country, and the country supports at least 160 mammal species [2]. With a population of nearly 168 million people, Bangladesh has one of the highest population densities in the world (>1260 people/km2) and retains only 6% of its natural habitats due to habitat conversion through agricultural activities (including timber plantations), human settlement, and infrastructure [7,8]. Rapid alteration of natural habitat [9], human persecution based on misconceptions and myths [10,11], and hunting for household consumption [12] put bats at risk in Bangladesh, but there has been very little bat research conducted in the country [13], and of the eight studies returned by our literature search, five were related to disease (Supplementary Materials Listing S1). This lack of knowledge is reflected in the IUCN Bangladesh Red List [9], that assessed 51% of the country’s bat species as Data Deficient and 17% as Not Evaluated. Moreover, the Red List observed that a quarter of the 35 species listed for the country have only been recorded once. Studies of bats in Bangladesh are therefore urgent; faced with extensive habitat loss and in a world with misconceptions about the origin of COVID-19, populations are at risk of local extirpation, taking with them the ecosystem services [14] they provide.
Tracking the history of bat research in Bangladesh is complicated by several changes in sovereignty in the Indian subcontinent over the last ~170 years. During the British colonial period (1858–1947), Bangladesh to the east and the Indian state of West Bengal were jointly called Bengal. During partition in 1947, the British provinces were divided into the Dominion of India and the Dominion of Pakistan. At that time, Bangladesh was named East Bengal and was part of the Dominion of Pakistan. The name East Bengal was changed to East Pakistan in 1955 and was used until independence from Pakistan was secured during the Bangladesh Liberation War in 1971, leading to the establishment of the People’s Republic of Bangladesh.
Bat research in Bengal started at the beginning of the 19th century and was based on specimen collection ([15,16,17] cited in [18]). Siddiqi [19] studied a collection of mammals preserved at the British Museum of Natural History, London (BMNH) (now the Natural History Museum, United Kingdom (NHMUK)) to produce a checklist of mammals of Pakistan (West Pakistan and East Pakistan). Only two bat species, i.e., Pteropus medius (reported as Pteropus giganteus following the taxonomy and nomenclature of the time), and Pipistrellus javanicus were documented as being captured from East Pakistan. Before the proclamation of Bangladeshi independence in 1971, Ahmed [20] conducted research (unavailable unpublished thesis) on bats of Bangladesh. After Bangladesh achieved sovereignty, Ahmed [21] worked (unpublished thesis) on bats of Bangladesh and mentioned a few specimen collections. However, much of the literature above could not be retrieved, so no detailed information on the studies is available (i.e., [16,17,21]). Later, Ahmed and Husain [22] published a checklist of bats of Bangladesh that comprised 52 specimens of 7 species (Pteropus giganteus (now Pteropus medius), Cynopterus sphinx, Taphozous longimanus, Taphozous saccolaimus (now Saccolaimus saccolaimus), Megaderma lyra (now Lyroderma lyra), Scotophilus temmincki (now Scotophilus kuhlii), and Tylonycteris pachypus). A review by Khan [6] listed 31 bat species in Bangladesh, of which 21 species were seen by the author, and 10 had a doubtful presence in the country. Sarker and Sarker [23] reported 17 species of bats in their systematic list through literature review and the authors’ observations. Bates and Harrison [3] reviewed the literature and museum specimens held at the BMNH for the Indian subcontinent, providing locality records, external and craniodental measurements. They reported 16 species of bats occurring in Bangladesh.
At the beginning of the 21st century, IUCN Bangladesh [24] reported 29 species of bats, although their data were principally guided by Khan [6]. Khan [10] described the extended distribution of 31 bat species that were previously mentioned in Khan [6]. Molur et al. [25] assessed South Asian bats and documented 34 species from Bangladesh. Later, 32 species were documented by Sarker and Sarker [26] and Sarker and Sarker [27], among them only 11 were verified by the authors’ visual observations. Srinivasulu and Srinivasulu [18] listed 38 species after a review of the available literature from 1982 to 2002. Subsequently, Srinivasulu et al. [28] developed a monograph on bats of South Asia (countries from the Indian subcontinent and Afghanistan) but the actual number of bat species in Bangladesh is not clearly defined. Thereupon, Srinivasulu and Srinivasulu [29] reported 37 species in the country based on their understanding. Khan [30] provided an updated checklist in which he listed 33 species of bats present in Bangladesh relying on a few field observations and previous references [6,10]. The latest assessment done by IUCN Bangladesh [9], reported a total of 35 species, primarily drawn from the species occurrence and distributions described in Khan [30]. Six (Hipposideros cineraceus, Rhinolophus pearsonii, Eptesicus pachyotis, Kerivoula papillosa, Hypsugo savii, and Scotomanes ornatus) out of 35 species were Not Evaluated by IUCN Bangladesh [9].
Since the 2015 IUCN Bangladesh assessment, six more species have been newly recorded for the country based on photographs and morphometric data, namely Megaerops niphanae [31], Rhinolophus pusillus [32], Pipistrellus javanicus [33], Hipposideros pomona [34], Macroglossus sobrinus [35], and Rhinolophus luctus [36]. Khan [7] listed 43 species in a photographic guide where he documented 15 species with photographs and included 17 species based on broad, but unsupported, distributions in the country (e.g., northwest, northeast, southeast). Eleven of the 43 species were designated as likely to occur in the country (Cynopterus brachyotis, Hipposideros armiger, Hipposideros galeritus, Rhinolophus luctus, Rhinolophus pearsonii, Rhinopoma hardwickii, Tadarida aegyptiaca, Kerivoula papillosa, Myotis formosus, Hypsugo savii, Scotomanes ornatus). Among them, 10 species had already been reported in Bangladesh from other sources, the exception being Hipposideros armiger. A recent database based on Srinivasulu and Srinivasulu [29], and Srinivasulu [37], was published by Srinivasulu et al. [4], which documented 37 species from Bangladesh. The most recent information retrieved from IUCN 2022 [2], listed a total of 40 species from 8 families.
Most of the literature cited above was written by a handful of researchers and the presence of reported species was based on their expert opinion, or propagation of prior opinions, or photographic records. Photographic evidence is problematic for bats because few species have diagnostic features that enable species identification from photographs without accompanying measurement, acoustic, or even molecular data. More generally, photographic evidence may not be available for authentication, compromising scientific credibility [38,39]. Only a handful of records are associated with voucher specimens that can validate species’ presence in Bangladesh. Consequently, the diversity and distribution of bat diversity in Bangladesh remain unclear.
The paucity of confirmed records of bats and limited research, coupled with the transitional position of Bangladesh between the Indo-Himalayan and Indo-Chinese subregions [7,40], suggest that the country may support more than the 40 species currently listed. Therefore, our goal was to summarize the available distributional information on bats of Bangladesh and its environs to provide a baseline for the plausible distribution of bats in the country. The objectives of this study are to (1) develop a confirmed checklist of bats based on the available literature and museum collections databases, and (2) collate bat species occurrence information around the political boundary of Bangladesh to identify species that are likely to occur in the country based on geographical proximity and ecology. The results of this research will clarify the locality distribution of bats confirmed in Bangladesh and can be used to identify priority areas for bat surveys in Bangladesh.

2. Materials and Methods

We followed the PRISMA guidelines [41] for data collation and removal (Supplementary Materials Scheme S1). We searched the literature, the Global Biodiversity Information Facility (GBIF), and museum databases for localities attached to confirmed records and voucher specimens in Bangladesh and surrounding countries. We generated a list of confirmed species for Bangladesh and assessed the probability of occurrence of other species from their distribution in neighboring countries and ecology. We created distribution maps for each species.

2.1. Study Countries and Regions

We focused on retrieving records from Bangladesh, and six neighboring Indian states (West Bengal, Sikkim, Meghalaya, Assam, Tripura, and Mizoram) and two neighboring Myanmar states (Rakhine and Chin) that collectively surround Bangladesh (Figure 1B). Bangladesh is a subtropical/tropical country with high humidity ranging between 65 to 96%. The summer (21–34 °C) is hot and humid, with heavy rains and storms (April–October). The winter (11–29 °C) is cool and dry (November–March) [6,42,43]. The elevation of the country varies from 0 to 1053 m above mean sea level [44]. Annual rainfall varies between 160 cm to 400 cm [43]. Inland wetlands occupy almost 9% of the total land area [45], but the country has hilly terrain despite its deltaic floodplain. The high hills are in the southeast region, whereas the low hills are in the northeast and there are moderate highlands in the country’s central, north, and northwest [46]. The original vegetation type of the high and low hilly areas is mixed evergreen forest, the moderate highlands are a combination of grassland, moist deciduous, and mixed evergreen forest [47]. The southwest region is the largest mangrove forest in the world, named the Sundarbans [9]. Grasslands, shrublands, and bamboo-dominated areas in the northeast and southeast account for ~5% of the total area of the country and serve as corridors between the mixed evergreen forest patches. The mixed evergreen forest in the northeast and southeast region of the country is continuous with comparable forest in the neighboring Indian states of Assam, and Mizoram [10] to the east, and the Chin and Rakhine states of Myanmar to the southeast. Deciduous forest is located at the center and north center of Bangladesh bordering Tripura state [10] and faces intensive anthropogenic disturbance. Non-forested vegetation cover (grasslands, agricultural lands, homestead vegetations, monoculture plantations) is about 67% of the total land area [45]. In addition, a few caves are found in the northeast and southeast Bangladesh.
The habitats and topography of states surrounding Bangladesh (Figure 1B) are as follows. In Myanmar to the southeast of Bangladesh, Chin state is hilly, and the land cover is dominated by tropical evergreen, semi-evergreen with bamboo thicket [48]. Rakhine state supports tropical mixed evergreen, deciduous, coastal mangrove swamps, and inland swamps. Bangladesh shares about an 837 km political border with the Indian state of Tripura [49,50]. Most of the evergreen forests in the northeast region of Bangladesh, hilly terrain, and small hillocks [51] and a few deciduous forest areas, extend into Tripura [10]. Mizoram to the east of Bangladesh represents hilly wet-evergreen and semi-evergreen forests, and shifting agriculture (jhum), and timber (i.e., Tectona grandis) and oil palm (Elaeis guineesis) plantations in and around the forests [52]. The state of Assam, which shares the northeastern border with Bangladesh, is mainly a valley, which features semi-evergreen forests [53]. Meghalaya consists of high hills, and about 80% of the total state area is covered by tropical forests, semi-evergreen forests, deciduous forests, pine forests and savannas [54,55]. Geologically, Sikkim is a rocky mountainous state. The northern extent is typically covered with snow and the southern part is hilly supporting temperate forests, alpine forests, and grasslands [56]. The natural areas of West Bengal, situated to the west of Bangladesh, consist of mangrove forests, broadleaf forests, semi-evergreen forests, moist deciduous forests, and montane forests [57].

2.2. Data Collection

Bat locality and distribution information was collated from the scientific literature, online open access databases of six natural history museums and the Global Biodiversity Information Facility (GBIF) (databases were last accessed February 2022). Museums were: American Museum of Natural History (AMNH), Smithsonian National Museum of Natural History (USNM), Natural History Museum, United Kingdom (NHMUK), Field Museum of Natural History (FMNH), Hungarian Natural History Museum (HNHM), and Royal Ontario Museum (ROM), and open-source species locality data (Global Biodiversity Information Facility (GBIF). Data were obtained from these museum databases by filtering taxa by the Order Chiroptera and locality information by Bangladesh and the surrounding states’ names. For the literature search, specific keywords used in a Google Scholar search: “Chiroptera”, “Bats” “Bangladesh”, “East Pakistan”, “East Bengal”, “West Bengal”, “Sikkim”, “Meghalaya”, “Assam”, “Tripura”, “Mizoram”, “Rakhine”, “Chin”, “India”, “Burma”, “Myanmar”, “Indian subcontinent”, “locality records”, “new records”, “first record”, “an addition”, “diversity”, “checklist”. A search of Google Scholar and Research Gate profiles was also performed for known research professionals in these regions. Further references were extracted from the ‘literature cited’ sections of published articles, and from book chapters, reports, newsletters, conference presentations, theses, and the IUCN Red List of Threatened Species assessments [2]. Finally, we reviewed publications on virus surveillance and discovery from Bangladesh for locality records.

2.3. Data Extraction from Records

We collated data on species occurrence from Bangladesh and surrounding states, specifically:
(1)
Locality information with latitude and longitude (fine-scale distribution) given in the record.
(2)
Locality information with latitude and longitude estimated from capture site descriptions. For many records, capture coordinates were not given, but the capture area, forest, sub-district, district, or a definite direction were listed (e.g., Netrokona, Modhupur forest, Mawsmai cave, 30 km north of Dhaka). We used Google Maps to identify the mentioned area or measured distance (e.g., 30 km north of Dhaka) and then selected a coordinate for the locality (fine-scale distribution).
(3)
State-wide distributions (coarse-scale distribution) if no specific coordinates or locality descriptions were provided but the state was named (e.g., Meghalaya, Rakhine).
(4)
Catalog number if the data were extracted from a museum database or GBIF.
(5)
Capture methods (e.g., mist nets, harp traps).
(6)
Basis of records, following Darwin Core terms. Specifically, whether a record was based on a preserved specimen (Darwin Core term “PreservedSpecimen”), tissues or organs (skulls, jaws) taken from an individual and preserved (MaterialSample), still image (“MachineObservation”) or human observation (“HumanObservation). However, any information related to body measurement, that did not fall under the Darwin Core basis of record, was referred to as measurement or fact (Darwin Core term “MeasurementOrFact”) [58].
(7)
Habitat type where the species was captured. If this was not mentioned, we collected required habitat information (e.g., caves, tropical dry forest, deciduous forest, evergreen/semi-evergreen/mixed evergreen forest, bamboo forest, mangrove forest, agricultural lands, human settlements) from the IUCN Red List species assessment [2].
We excluded species distribution records where authors stated larger areas that occupy multiple places in the country, e.g., “northeastern region”, “southeastern region”, “semi-evergreen forest”, “montane forest”, “all over the country”, “forested areas of the country”, “well-vegetated area”, “countryside”. Taxonomic classifications of the species followed Simmons and Cirranello [1]. The older names of bat species found in records were checked with Simmons [59] and aligned with current classifications.

2.4. Inferring Possible Occurrence of Species in Bangladesh

We classified the probability of occurrence of each species in Bangladesh on the basis of species locality records, distribution surrounding the country and the ecology of the species. Three rivers divide the country into east and west—Jamuna, Padma, and Meghna (Figure 1C). The distribution of animals and plants in Bangladesh is largely influenced by these rivers [6]. In addition, rivers present a strong biogeographic barrier for bat dispersal [60]. There are four states of India (Meghalaya, Assam, Tripura, and Mizoram) and two states of Myanmar (Rakhine and Chin) are to the east of these rivers. Two states of India (West Bengal and Sikkim) are to the west. We assigned species into four categories of likelihood that the species is in Bangladesh: (1) Confirmed from Bangladesh. This category was split by the strength of the basis of record. For species in category 1A the basis of record was any of the three criteria: (i) preserved specimen (PreservedSpecimen); (ii) preserved skull and jaws only (MaterialSample); (iii) morphometric measurement (MeasurementOrFact) along with key diagnostic features mentioned and comparisons with closely related species. For those in category 1B, records were based on a still image (MachineObservation), a citation of records or specimens from literature (MaterialCitation) or human observation (HumanObservation). (2) Highly Probable (yet to be confirmed)—species recorded with a preserved specimen (as for 1A) in neighboring states to both the east and west of the Jamuna, Padma and Meghna rivers, and known from habitats that are present in Bangladesh; (3) Probable (yet to be confirmed)—species recorded with a preserved specimen on either the east or west of the rivers and known from habitats present in Bangladesh; (4) Possible (yet to be confirmed)—species recorded with a preserved specimen on any side or both sides of the rivers, but for which it is not clear if suitable habitats are present in Bangladesh. In addition, the species previously reported from Bangladesh that did not fit into either category of 1A or 1B were reviewed and classified as Highly Probable, Probable, and Possible.

2.5. Occurrence Maps

Maps for the bats of Bangladesh were based on the confirmed locality records (fine-scale distribution). For the maps of bats that are yet to be confirmed in Bangladesh, we provide both fine-scale (coordinates) and coarse-scale (polygon) distribution information.

3. Results

We reviewed 43 publications that described bats of Bangladesh. Two studies collected specimens [19,22], one described species with morphometric measurements and taxonomic keys [28], and one described morphometric and craniodental measurement, species’ distributions, habitat preferences, and reproduction if known [3]. A little less than half of the remaining publications (48.7%) provided checklists of bats of Bangladesh based on literature review, experts’ opinions, visual observations, and in a few instances, photographic evidence. Publications reporting new country records and re-discoveries accounted for 23.1%, the majority of which were discovered through taxonomic and craniodental measurement, and photographs. Mating observations (observed by chance) and notes on roosting sites (i.e., Pteropus medius and Saccolaimus saccolaimus) jointly accounted for 12.8% of all studies [61,62,63,64]. Diversity studies (using mist nets), and human-bat interface (bat hunting) contributed 7.7% and 5.1%, respectively. Miscellaneous notes (e.g., death of Pteropus medius by electrocution) added to 2.6% of the study [65].
As a result of aggregating literature, museum records, and the GBIF species occurrence dataset, 46 species of bats from 8 families have been reported from Bangladesh (Table 1). However, based on our classification scheme, only 31 species were Confirmed for Bangladesh with 148 locality records (including 11 locality records of Pteropus medius from virus surveillance publications in Bangladesh [66,67,68,69,70]) (Supplementary Materials Table S1, Figure S1). Of these 31, only 22 species fell into category 1A. Fifteen of the 22 were confirmed with the basis of record a preserved specimen (PreservedSpecimen: Cynopterus brachyotis, Cynopterus sphinx, Macroglossus sobrinus, Pteropus medius, Rousettus leschenaultii, Saccolaimus saccolaimus, Taphozous longimanus, Lyroderma lyra, Rhinolophus luctus, Hesperoptenus tickelli, Pipistrellus javanicus, Pipistrellus tenuis, Scotophilus heathii, Scotophilus kuhlii, Tylonycteris pachypus), six were confirmed from processed specimens (MaterialSample: Megaerops niphanae, Coelops frithii, Hipposideros pomona, Rhinolophus pusillus, Pipistrellus coromandra, Pipistrellus pipistrellus), and one from a morphometric measurement with diagnostic characteristics described (MeasurementOrFact: Hipposideros lankadiva). The other 9 species fell into category 1B, based on still images (MachineObservation) and human observations (HumanObservation).
An additional fifteen species were listed for Bangladesh based on experts’ opinion but lacked confirmation in Bangladesh (i.e., there was no specimen, image or observation), but were considered Highly Probable (8 species), Probable (4 species), and Possible (1). No locality records were found for Hipposideros galeritus and Rhinopoma microphyllum so they were not categorized (Table 1, Supplementary Materials Table S2). Twenty of the 31 confirmed species have only been recorded to the east of the Jamuna, Padma, and Meghna Rivers, one only to the west, and 10 on both sides of the country (Table 1, Supplementary Materials Figure S1).
We considered the occurrence of an additional 38 species to be Highly Probable, 33 species Probable, and 10 species Possible (Supplementary Materials Table S2). The distribution of the total 81 species (38 Highly Probable, 33 probable, and 10 Possible) are available as maps in Supplementary Materials Figure S2. This suggests Bangladesh may be home to 31–112 species.
In terms of the geographical distribution of species potentially in Bangladesh, a total of 43 species (38 Highly Probable, 5 Possible) are known to occur in neighboring states to both the east and the west of Bangladesh. Twenty-nine species (27 Probable, 2 Possible) are known to occur only to the east, and 9 species (6 Probable, 3 Possible) are known only to occur to the west of the country.
Twenty-seven out of the 31 confirmed species in Bangladesh are categorized as Least Concern (Table 1) in the IUCN Red List global assessment [2]. Three species, namely Rousettus leschenaultii, Coelops frithii, and Kerivoula picta are classified by the IUCN as Near Threatened. The only species in the Threatened category is Hipposideros pomona (Endangered) (Table 1). This hipposiderid species was first recorded from a cave at the Chittagong Hill Tracts in the southeast region of the country [34] and was reported to occur in the northeast and north, although without confirming observations [7,29]. About a hundred individuals were observed in an undisturbed cave in dense hilly forest, and the cave is used as a shrine by the local community [34]. In addition, there are a few Threatened or Near Threatened species that we classified as Highly Probable for the country namely Myotis sicarius (Vulnerable), and Rhinolophus trifoliatus, Ia io, Myotis formosus (Near Threatened) [2].

4. Discussion

There has been very little research on bats to date in Bangladesh, as reported in the literature [33] and further evidenced by the fact that we found only 148 locality records (Supplementary Materials Table S1) and confirmed just 31 species of which only 21 were associated with specimens and one confirmed with measurement. Nonetheless, we consider it highly probable that there are at least 69 species (the 31 Confirmed and 38 Highly Probable species), and that there is potential for over 100 species.
Bangladesh is rich in mammalian diversity (both large and small mammals) because of its geographical position between the Indo-Himalayan and Indo-Chinese subregions [7,40]. The sub-regions intersect in the country’s southeastern side, which may be one explanation for why the east of the country has more bat species recorded so far (20 species out of 31, Supplementary Materials Figure S1). In addition, 29 species designated as Probable were only recorded in the states of India and Myanmar to the east of the country (Supplementary Materials Table S2). The east of Bangladesh, as well as the bordering states of India and Myanmar have similar land cover and habitat (mixed evergreen forest), suggesting that surveys in east of Bangladesh will likely add many species to the country list. Moreover, all other bat species recorded in the Indian state of Tripura are also reported from Bangladesh, except for Rousettus amplexicaudatus (Family: Pteropodidae) [71]. Similarly, we confirm many of the bats from the Myanmar states of Chin and Rakhine for Bangladesh, and the remaining species were classified as Highly Probable (Hipposideros armiger, Myotis muricola, M. hasseltii) and Probable (H. ater) (Supplementary Materials Table S2). In the west of Bangladesh, however, Coelops frithii is the only species that has been confirmed. This species occurs in primary and secondary forests of the Indian subcontinent [25], but in Bangladesh, it has recently been recorded [72] from its type locality in the mangrove forests of the southwest.
Table
Table 1. A checklist of bats in Bangladesh based on the literature, museum and GBIF records.
Table 1. A checklist of bats in Bangladesh based on the literature, museum and GBIF records.
Families and SpeciesConfirmed Records
(See Table S1)		Species Reported in the LiteratureRed List Threat Category (IUCN 2022) [2]
Museum RecordsGBIFLiterature RecordsIUCN Red List 2022 [2]Srinivasulu et al., 2021 [4]Khan 2018 [7]IUCN Bangladesh 2015 [9]Srinivasulu and Srinivasulu 2012 [29]Sarker and Sarker 2005 [27]Molur et al., 2002 [25]Khan 2001 [10]
Pteropodidae
1Pteropus medius Temminck, 18251A1A1AYYYYYYYYLC
2Rousettus leschenaultii (Desmarest, 1820)1A1B1BYYYYYYYYNT
3Cynopterus sphinx (Vahl, 1797)1A 1AYYYYYYYYLC
4Cynopterus brachyotis (Mȕller, 1838)1A Y LC
5Eonycteris spelaea (Dobson, 1871) 1B YY LC
6Megaerops niphanae Yenbutra & Felten, 1983 1A Y LC
7Macroglossus sobrinus K. Andersen, 1911 1AYYY LC
Rhinolophidae
8Rhinolophus pusillus Temminck, 1834 1A YY LC
9Rhinolophus lepidus Blyth, 1844 1BYYYYYYYYLC
10Rhinolophus luctus Temminck, 1834 1A1BYY Y YYLC
11† Rhinolophus subbadius Blyth, 1844 YYYYYYYYLC
12* Rhinolophus pearsonii Horsfield, 1851 YY YYYYLC
13* Rhinolophus macrotis Blyth, 1844 Y YY LC
14Rhinolophus affinis Horsfield, 1823 1BY Y Y LC
Hipposideridae
15Hipposideros cineraceus Blyth, 1853 1BYYY LC
16Hipposideros lankadiva Kelaart, 1850 1AYYYYY YYLC
17Hipposideros larvatus (Horsfield, 1823) 1BYYYYYYYYLC
18§ Hipposideros galeritus Cantor, 1846 Y YYYYYLC
19Hipposideros pomona K. Andersen, 1918 1A Y Y Y EN
20Coelops frithii Blyth, 1848 1AYYYYYYYYNT
Megadermatidae
21Lyroderma lyra (E. Geoffroy, 1810) 1AYYYYYYYYLC
22Megaderma spasma (Linnaeus, 1758) 1BYYYYY YYLC
Emballonuridae
23Saccolaimus saccolaimus (Temminck, 1838) 1AYYYYYYYYLC
24Taphozous longimanus Hardwicke, 1825 1A1AYYYYYYYYLC
25* Taphozous melanopogon Temminck, 1841 YYYYYYYLC
Molossidae
26Mops plicatus (Buchannan, 1800) 1BYYYY LC
27† Tadarida aegyptiaca (E. Geoffroy, 1818) YY YYYYYLC
Rhinopomatidae
28* Rhinopoma hardwickii Gray, 1831 Y YYYYYLC
29§ Rhinopoma microphyllum (Brȕnnich, 1782) Y YYYYYLC
Vespertilionidae
30Scotophilus heathii (Horsfield, 1831) 1A1AYYYYYYYYLC
31Scotophilus kuhlii Leach, 1821 1A1AYYYYYYYYLC
32* Scotozous dormeri Dobson, 1875 YYYYYYYYLC
33Pipistrellus pipistrellus (Schreber, 1774) 1A YYY LC
34Pipistrellus javanicus (Gray, 1838)1A1A1AYYY Y Y LC
35Pipistrellus coromandra (Gray, 1838) 1AYYYYYYYYLC
36Pipistrellus tenuis (Temminck, 1840)1A1A1AYYYYYYYYLC
37Pipistrellus ceylonicus (Kelaart, 1852) 1BYYYYY YYLC
38†† Hypsugo savii (Bonaparte, 1837) YY YYYYLC
39† Hypsugo affinis (Dobson, 1871) Y LC
40Kerivoula picta (Pallas, 1767) 1BYYYYYYYYNT
41* Kerivoula papillosa (Temminck, 1840) YYYLC
42† Eptesicus pachyotis (Dobson, 1871) YYY YYYYLC
43* Scotomanes ornatus (Blyth, 1851) YY YYYYLC
44* Myotis formosus (Hodgson, 1835) Y YYYYYNT
45Hesperoptenus tickelli (Blyth, 1851) 1AY YYYY LC
46Tylonycteris pachypus (Temminck, 1840) 1A Y YYY LC
Confirmed 1A = 22, 1B = 9. Total 31Species reported in literature based on 1A, 1B and expert opinion = 46
*—Highly Probable; †—Probable; ††—Possible; §—excluded from further categorization.
Most of the documented habitats for species expected to occur in Bangladesh are forests (deciduous, bamboo, semi-evergreen, evergreen, broadleaf forests), as well as caves and wetlands (Supplementary Materials Table S2). When Bangladesh was under British colonial and the Dominion of Pakistani rule, the forest policies promoted resource exploitation and agriculture expansion that continue to date [43]. Consequently, with only 6 % of natural habitat remaining, it is possible that species have already been lost from the country, before they could be documented. Bat surveys should focus on the 38 Protected Areas (PAs) in Bangladesh that collectively cover many potential habitats for bats [7] (Figure 2). Of note are: (1) the Raghunandan Hill Reserve Forest, and Rajkandi Reserve Forest in northeast Bangladesh. These reserves protect semi-evergreen forest and hillocks and border Tripura and Assam, respectively. (2) Khadimnagar National Park that protects semi-evergreen forest and is close to Meghalaya (<16 miles). (3) The Sundarbans in the southwest of Bangladesh encompassing the largest mangrove forest in the world. In addition, cave systems in southeast Bangladesh, especially the ‘Kudum cave’ in Teknaf, should also be prioritized for survey work as many bat species are cave-dependent [34].
Of the 40 species listed for Bangladesh by IUCN [2], we confirmed only twenty-three species (Table 1), although most of the remaining 17 species fell into our Highly Probable or Probable categories (Supplementary Materials Table S2). Conversely, we confirmed eight species for Bangladesh that are not included in the Red List Assessments for the country (Cynopterus brachyotis, Eonycteris spelaea, Megaerops niphanae, Macroglossus sobrinus, Rhinolophus pusillus, Hipposideros pomona, Pipistrellus pipistrellus, and Tylonycteris pachypus).
Bat research in Bangladesh is in its infancy compared to that in neighboring countries (e.g., India, Myanmar, Nepal), and surveys are urgently needed to establish baseline data that can support assessment and monitoring of bat diversity responses to land-use change, deforestation, disease, and climate change [73]. The few surveys to date have been restricted to mist-netting (e.g., [13,74,75,76,77]) and photographic evidence [36,62,78,79]. We recommend implementing harp traps in addition to mist nets to maximize capturing different bat species. Mist nets effectively capture fruit bats (Family: Pteropodidae) and some species of insectivorous bats. However, many insectivorous bat species avoid mist nets, particularly those adapted to forage in and around vegetatively complex habitats (e.g., smaller members of the Rhinolophidae, Hipposideridae, and Vespertilionidae), but are more readily captured in harp traps [80,81,82]. Harp traps have yet to be used in Bangladesh, but they rapidly increased rates of species discovery, and changed the understanding of the composition of bat assemblages, in Southeast Asia [81,83] and now Africa [82]. Therefore, it is necessary to utilize all the complementary capture methods (e.g., mist nets, harp traps, and hand nets) when conducting bat surveys to catch and identify different bat ensembles (plant-visiting, open space, edge, and forest understory [84]) in Bangladesh.
Regardless of method, many species are difficult to capture, but use high-intensity echolocation calls that can be detected acoustically, particularly insectivorous species that forage at forest edges, or in open spaces and above the canopy [84,85]. Although there is some overlap in parameters, generally echolocation signals emitted by bats when navigating and foraging are species-specific. Consequently, echolocation recordings can help confirm species identity, especially in the case of species that are morphologically cryptic but divergent in their echolocation calls [86,87]. Acoustic surveys can contribute to inventory completeness [88,89,90], and assessments of species associations with natural and modified habitats and land-uses [91,92,93,94]. However, it is essential to have a call library populated with recordings from individuals of confirmed species identity (reference calls) to cross-check with the recordings collected in field sites. We recommend researchers record echolocation calls and contribute the recordings to established call libraries (e.g., ChiroVox [95]). Recordings should ideally be made in settings that allow for the bat to use search phase calls. For example, free-flying after release for species that forage in open and edge habitats (e.g., Molossidae, many Vespertilionidae), flight cages or tents for species that use low-intensity calls in vegetatively cluttered habitats (e.g., Kerivoulinae, Murininae, Megadermatidae, Nycteridae). In the case of the Rhinolophidae and Hipposideridae, resting frequency is typically recorded from stationary bats (hand-held, or hanging in a flight tent) [85,96,97]. Bat acoustic data from Bangladesh can enrich the global bat call database, ChiroVox, as call recordings of only 19 species found in Bangladesh are currently available in the ChiroVox database and none of these recordings were from bats captured in Bangladesh. Therefore, recordings of Bangladesh’s bats can make a valuable contribution to regional coverage, and further understanding of call structures of intra-specific variation in echolocation call structure [97] across species’ ranges.
There are several limitations of our study. First, we relied on open access data, which can be spatially and temporally biased [98,99,100]. Much of our data came from India, with few records from Chin and Rakhine states in Myanmar, potentially biasing our evaluation of occurrence probability in Bangladesh. Contemporary collections held in Bangladesh, India and Myanmar were not available online and likely hold additional records, and we encourage researchers to make these data more accessible. Second, we did not verify the records by direct examination of the source material that formed the basis of record. In addition to intensive, multi-faceted surveys around Bangladesh, future efforts should also focus on examining existing museum specimens and building collections. Specimen collections are critical to examine genetics and morphology to identify species accurately as many bat species are cryptic, genetically divergent but exhibiting a comparatively low level of phenotypic diversity among species [101].

5. Conclusions

Our results confirmed 31 species with locality information in Bangladesh, with voucher material (preserved specimens, processed specimen) for 22 species. Potentially, up to 81 additional species may be present in the country. We suggest that Protected Areas, caves, and wetlands in the country should be the focus of surveys deploying complementary capture methods and acoustic data collection. Surveys should contribute voucher collections of preserved specimens to confirm the presence and distribution of bat species in Bangladesh, and to identify bat diversity hotspots in this under-studied country.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d14121042/s1 (Listing S1, and Scheme S1) and doi:10.5061/dryad.5tb2rbp7j (Figure S1, Figure S2, Table S1, Table S2). Listing S1. A topic-based literature search (n = 217) on the Web of Science database for studies on bats (except for bat-borne virus-related research) in Bangladesh and the neighboring 7 countries, i.e., Bhutan, India, Maldives, Myanmar, Nepal, Pakistan, and Sri Lanka was conducted to assess the extent of research to date. We followed both Boolean and Truncation techniques and used the following terms: Bat* OR Chiroptera, AND Name of the Country, NOT *virus, NOT virus*, NOT *virus*. The publication dates range from August 1947 to January 2022 (about 75 years) because Bangladesh, India and Pakistan were jointly named as the Indian Subcontinent before August 1947. Onward, India and Pakistan became independent. Bangladesh was named East Pakistan until the liberation war in 1971. Scheme S1. PRISMA flow diagram showing the number of records collected from the museum and open access database, and the number of publications searched to collect bat locality and distribution information. Figure S1. The confirmed locality records of 31 bat species in Bangladesh, among them 15 species are confirmed with the voucher specimen (Cynopterus brachyotis, Cynopterus sphinx, Macroglossus sobrinus, Pteropus medius, Rousettus leschenaultii, Saccolaimus saccolaimus, Taphozous longimanus, Lyroderma lyra, Rhinolophus luctus, Hesperoptenus tickelli, Pipistrellus javanicus, Pipistrellus tenuis, Scotophilus heathii, Scotophilus kuhlii, Tylonycteris pachypus), 6 species are associated with the processed specimen (Megaerops niphanae, Coelops frithii, Hipposideros pomona, Rhinolophus pusillus, Pipistrellus coromandra, Pipistrellus pipistrellus), and 1 species is confirmed with morphometric measurement (Hipposideros lankadiva). The remaining 9 species are confirmed with the basis of still images and human observation (Eonycteris spelaea, Rhinolophus lepidus, Rhinolophus affinis, Hipposideros cineraceus, Hipposideros larvatus, Megaderma spasma, Mops plicatus, Pipistrellus ceylonicus, Kerivoula picta). Figure S2. Locality records and distribution of bats in states in neighboring countries (India and Myanmar). Based on the occurrence, distribution, and the required habitats for bats, there are 81 species yet to be confirmed. Among them 38 species are Highly Probable, 33 species are Probable, and 10 species are in Possible category. Table S1. Locality records (n = 148) of 31 confirmed bats of Bangladesh. Table S2. A list of 81 bat species that are yet to be occurred in Bangladesh. Of those, 38 species are Highly Probable, 33 species are Probable, and the remaining 10 species are Possible.

Author Contributions

Conceptualization: T.K., M.A.U.H.; Methodology: T.K., M.A.U.H.; Data Collection and curation: M.A.U.H.; Map Illustration: M.A.U.H.; Original Draft Preparation: M.A.U.H., T.K.; Draft Review and Editing: T.K. and M.A.U.H.; Supervision: T.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statements

Not applicable.

Data Availability Statement

Supplementary Materials Tables S1 and S2 contain species distribution data, which can be visualized in Figures S1 and S2, respectively.

Acknowledgments

We thank Nancy McIntyre, Richard Stevens for comments that helped with the conceptualization of this study, and Paul Bates for contributions to conceptualization and review of a late-stage draft. We would also like to thank Rhett Huebner and Sajidur Rahman Akash for assisting in data collation. We appreciate the Kingston Lab members Iroro Tanshi, Benneth Obitte, Isham Azhar, Abby Rutrough, and Touseef Ahmed for the insightful remarks, which have helped to strengthen this study.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Maps of the study countries and regions. (A) Map showing the countries of the Indian subcontinent where Bangladesh is surrounded by India on the east, north and west of the country, and Myanmar on the southeast corner of Bangladesh. (B) The study regions/states that are adjacent to Bangladesh. (C) Map of Bangladesh showing the three big rivers, i.e., Jamuna, Padma, and Meghna that distinctly divide the country into east and west.
Figure 1. Maps of the study countries and regions. (A) Map showing the countries of the Indian subcontinent where Bangladesh is surrounded by India on the east, north and west of the country, and Myanmar on the southeast corner of Bangladesh. (B) The study regions/states that are adjacent to Bangladesh. (C) Map of Bangladesh showing the three big rivers, i.e., Jamuna, Padma, and Meghna that distinctly divide the country into east and west.
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Figure 2. Protected Areas in Bangladesh - priority sites for bat diversity surveys, here NP = National Parks, and WS = Wildlife Sanctuary.
Figure 2. Protected Areas in Bangladesh - priority sites for bat diversity surveys, here NP = National Parks, and WS = Wildlife Sanctuary.
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Ul Hasan, M.A.; Kingston, T. Bats of Bangladesh—A Systematic Review of the Diversity and Distribution with Recommendations for Future Research. Diversity 2022, 14, 1042. https://doi.org/10.3390/d14121042

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Ul Hasan MA, Kingston T. Bats of Bangladesh—A Systematic Review of the Diversity and Distribution with Recommendations for Future Research. Diversity. 2022; 14(12):1042. https://doi.org/10.3390/d14121042

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Ul Hasan, Md Ashraf, and Tigga Kingston. 2022. "Bats of Bangladesh—A Systematic Review of the Diversity and Distribution with Recommendations for Future Research" Diversity 14, no. 12: 1042. https://doi.org/10.3390/d14121042

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