Description of the new Indian specimens

The two captured Disk-footed bats, one adult female (FA 33.5 mm) and another juvenile female (FA 33.9 mm) were netted in a forest patch dominated by bamboo thicket. They were recognized as Eudiscopus denticulus (Osgood, 1932) owing to a combination of small size, conspicuous disk-like pads present on their feet and a Myotis-like tragus shape (Fig. 1). There were remarkable differences in pelage colour between the juvenile and adult individuals, the former (Fig. 1C) being much darker than the latter (Fig. 1A and B). The adult female had a bright reddish-brown pelage, except for the belly which was darker with paler tips. The individual hairs had darker roots both dorsally and ventrally. This colouration is thus brighter reddish brown as against cinnamon brown given in the original description of the species from Laos (Osgood, 1932) or to specimens from Vietnam (e.g. Kruskop, 2013). However, as noted by Koopman (1972) the Myanmar specimens were smaller and brighter than Laos specimens and our Meghalaya specimen thus resembles the Myanmar material in pelage colour and shorter forearm (Table 2). The wing membrane was dark brown and essentially devoid of hairs and joined at the base of the outer toe. The tail tip was completely enclosed within the interfemoral membrane which was little lighter in colour and slightly whitish on the underside. The muzzle was pinkish. The ears were relatively large and pointed, unlike those of e.g. Tylonycteris or Glischropus, whereas the tragus was straight with a concave outer border and blunt tip, much like that of a small Myotis. The thumbs were short (1.5 mm) and there were callosities at the thumb base which were dark pigmented and not very obvious. Schliemann & Rehn (1980) noted that these poorly differentiated thumb pads unlikely have adhesive function in Eudiscopus, unlike in Tylonycteris or Glischropus. Noticeable planter pads existed in the form of sub-rectangular adhesive discs (4 × 2.9 mm) which were dark pink in colour (Fig. 1B) and turning beige in ethanol-preserved specimens. This disc development was more pronounced than in Tylonycteris as noted by Schliemann & Hoeber (1978). The juvenile individual (as determined from less knobby and evenly tapered phalangeal-metacarpal joints) was externally similar to the adult one in all respects except that the pelage was dark brown (Fig. 1C).

The skull was very broad and flat (Fig. 2A and B); however, unlike Tylonycteris, rostrum was longer and narrower. The zygomatic arches were widely flared (ZW 9.7 mm). The coronoid process of mandible was high and blunt with concave posterior border (Fig. 2C). The upper incisors were bicuspid and similar in height and separated from the canine by a small gap. The canine was unicuspid and considerably exceeded the length of the third premolar. There were three pairs of lower premolars, the middle one (p₃) being minute and completely displaced internally. In our specimen, the anterior teeth of the mandible were shed during the chemical cleaning process but not before being able to examine the dental structure. Lower molars were all myotodont, as in most Myotis or Tylonycteris, but unlike in Glischropus (Kruskop, 2013).

Table 1.

Species sampling for the molecular reconstructions based on the mitochondrial cytochrome b gene with corresponding museum voucher (if any), country of origin, GenBank entries and reference of the published sequences.

Table 2.

Comparative measurements of the two E. denticulus from Meghalaya and 18 other individuals from Southeast Asia. External measurements were taken from both Meghalaya individuals, while only the adult female was measured for craniodental characters. Values in brackets are means.

Revised distribution

So far, the species was reported from several localities in Southeast Asia i.e. Yetho River, Pegu Yoma in central Myanmar (Koopman, 1970); Khlong Lan National Park, Loei, Ratchaburi, and Surat Thani in Thailand (Schliemann & Kock, 2000; Soisook et al., 2016), and Chu Mom Ray in Kon Tum Province in central, Cat Tien National Park in the south and Pu Huong, and Bu Gia Map Nature Reserve in north-central Vietnam (Borissenko & Kruskop 2003; Zsebők et al., 2014; Kruskop, 2013, 2017). Very recently, it has also been reported from three localities in Yunnan Province of China (Yu et al., 2021). According to Koopman (1970, 1972), the precise locality of two specimens from Myanmar housed in the AMNH i.e. “Yetho River, Pegu Yoma, 100ft” is indeterminate. This was confirmed by Schliemann & Kock (2000) who also noted that within a radius of 100 km, there are at least three low-elevation localities (under 50 m a.s.l.) named “Yetho” in the slopes of Pegu mountains in Myanmar and one of these places might represent the source of the Myanmar's specimens. In our view also, this locality represents a tributary of Sittuang river in south-central Myanmar and lies in the same general area (18° 00′ - 18° 05′N, 96° 00′- 96° 05′E) as postulated by Schliemann & Kock (2000) and was hitherto considered the westernmost locality for this species. The present locality in Meghalaya thus represents a range extension of about 1000 km further west into the Indian Subcontinent (Fig. 3) and was not predicted to occur in this region according to the MaxEnt modelling study of Yu et al. (2021). Furthermore, except for the type locality which is situated at an altitude of about 1300 m a.s.l. in northern Laos (Schliemann & Rehn, 1980), all records of Disk-footed bats lie below 1000 m a.s.l., including the present record from north-eastern India (210 m a.s.l.), suggesting that this is a predominantly lowland species.

Ecological notes

The two Meghalaya Disk footed bats were caught in a net set at one of the entrances of a tunnel-like closed canopy forest with predominant bamboo growths (Dendrocalamus and Bambusa spp.). The general forest habitats found in the area belongs to Tropical semi-evergreen type (Champion & Seth, 1968). These bats were caught on the inner side of the net indicating they were emerging from inside the forest patch. By virtue of remarkable morphological features like a flattened skull and adhesive pads, these bats can roost inside cramped space clinging to smooth surfaces like bamboo internodes (Koopman, 1972; Kock & Kovac, 2000; Schliemann & Kock, 2000). Considering the bamboo-dominated forest from where these specimens were collected, a similar roosting preference can be expected in Meghalaya. A knowledgeable villager indicated occasional presence of bats inside bamboo internodes. However, he indicated that they were not as bright in colouration, possibly referring to other bamboo-dwelling bats (Tylonycteris spp.) which were also recorded by the senior author from the nearby Nongkhyllem WLS during bat surveys conducted in 2016. This indicates uncommon occurrence of Eudiscopus in the area. Similar observations were also reported by Kock & Kovac (2000) who found E. denticulus only once in Thailand, after numerous probing in bamboo internodes in Southeast Asia, whereas Tylonycteris spp. were frequently recorded.

Fig. 1.

Lateral (A) and frontal (B) view of an adult female (ZSIS 621) and lateral view (C) of juvenile (ZSIS 622) E. denticulus specimen from Meghalaya (images not to scale). Notice prominent pinkish plantar disc on the hind feet (image B).

Echolocation

The echolocation call parameters (mean ± standard deviation) were as follows: SF = 104.82 ± 2.7 kHz, EF = 53.12 ± 5.79 kHz, PF = 56.81 ± 2.86 kHz, BW = 51.69 ± 2.55 kHz and D = 4.75 ± 0.63 ms. These parameters and the entire call structure (Fig. 4) are similar to those previously recorded for E. denticulus (Hughes et al., 2011; Zsebők et al., 2014). Although we could not completely rule out the possibility of these recorded calls belonging to another species, it is most probable that the calls belong to E. denticulus. During the three hours of netting session at the site, the only other species caught were Rhinolophus affinis (emitting very distinct, constant-frequency signals) and Pipistrellus coromandra. Considering the rhythm and frequency range of the recorded calls which are much higher than those reported for P. coromandra elsewhere (Srinivasulu et al., 2017), we can exclude confusion with this species as well. We did not record the long, upward-sweeping “unique call type” described by Zsebők et al. (2014) for E. denticulus. However, we recorded prominent hook-shaped starts in two pulses (as seen in some Kerivoula and Murina spp.; Schmieder et al., 2010) that were not mentioned earlier (Fig. 4).

Wing morphology

Wing morphology and echolocation calls are a reliable method to assign guild membership to bats (Norberg & Rayner, 1987; Denzinger & Schnitzler, 2013) and also allow to predict the potential vulnerability of species to anthropogenic disturbance (Núñez et al., 2019). However, these data are mostly lacking for tropical bat species, particularly those rare species like E. denticulus. Based on measurement of the adult female caught in Meghalaya, the moderate aspect ratio (6.64) and low wing loading (5.55) coupled with relatively broad tips (Tip-shape index = 1.68) indicate low flight speed and improved manoeuvrability (Norberg & Rayner, 1987). On account of these novel wing morphology data and relatively high echolocation call frequency, we corroborate Zsebők et al. (2014)'s guild assignment of E. denticulus as an ‘edge space aerial forager’ (Denzinger & Schnitzler, 2013) that can adapt to a fair degree of clutter (as bamboo forests in this case). With such wing and echolocation call characteristics it appears less well adapted to forage in complete open space. We indeed observed the flight of the juvenile individual inside a large room performing a slow, fluttering flight similar to those of some Pipistrellus spp.

Fig. 2.

Lateral (A), dorsal (B), ventral (D) view of cranium and of mandible (C) of ZSIS 621 specimen. Note that the mandibular dentition is incomplete due to inadvertent loss of few anterior teeth (incisors and canines) during the cleaning process of the skull.

Genetics

The partial cytochrome b gene was successfully amplified and sequenced from the adult female E. denticulus from Meghalaya. Remarkably, the 421 aligned base pairs of this individual were identical to homologous sequences of E. denticulus from Vietnam, despite the over 2000 km straight distance separating the two sampling localities. Both individuals from Vietnam sequenced for the complete cytochrome b (1140 bp) were also nearly identical, with a single T/C transition noted in position 996. The comparison of various individuals sequenced for another mitochondrial gene (the cytochrome c oxidase subunit I) likewise suggest minimal (<1%) molecular variation in Disk-footed bats issued from distant places in Vietnam (Kruskop et al., unpublished 2018) or in Yunnan, China (Yu et al., 2021). Such high genetic similarities for mitochondrial genes characterized by relatively high mutation rates in mammals, including bats (Bradley & Baker, 2001) suggest that Eudiscopus populations from Vietnam, China and Meghalaya certainly have a very recent common origin. As secondary bamboo regrowth has been greatly favoured by the adoption of slash-and-burn culture by expanding human population in Indochina, one hypothesis would be that these bat populations expanded from the same region, following the very recent expansion of man-made bamboo groves. Compared to other cytochrome b from various bat species (Table 1), these sequences of E. denticulus differ by at least 18% Kimura-two-parameter distance from any other Myotis or Submyotodon tested, and by 19% or more from other Vespertilionidae. All phylogenetic reconstructions based on this gene were very concordant and clearly placed the single Eudiscopus lineage within the Myotinae, with 82 (maximum likelihood) to 99% (Bayesian) support (Fig. 5). Unfortunately, these reconstructions could not resolve the relative position of Eudiscopus in this radiation, as the other two Myotinae, Myotis and Submyotodon, were also placed near the base of this radiation with low nodal support. A basal position of Eudiscopus within the Myotinae corroborate previous molecular reconstructions based on a small selection of Vespertilionidae and the 12S rDNA sequences (Borisenko et al., 2008). The recent and more extensive sampling of the mitochondrial genome of several Vespertilionidae also concluded that Eudiscopus was the most basal Myotinae (Yu et al., 2021), but clearly, genes from the nuclear genome are needed to completely resolve this radiation. At least, alternative phylogenetic hypotheses placing Eudiscopus with other bats bearing enlarged or disk-like pads (e.g. Glischropus spp., Tylonycteris spp., Hesperoptenus spp. or Myotis rosseti) or close to other Vespertilioninae can be clearly excluded by current molecular reconstructions.

Fig. 3.

Location of currently known records of E. denticulus in South and Southeast Asia.

Fig. 4.

Call spectrogram of a free flying individual of E. denticulus from Meghalaya. The values in the vertical axis indicate call frequency in kHz. Each division of the horizontal axis indicates a time interval of 10 milliseconds.

Fig. 5.

Maximum likelihood reconstruction of the Eudiscopus denticulus lineage within a selection of Vespertilionidae and outgroup Miniopteridae bats. Percent nodal support obtained from 1000 Ultrafast repeats in iQ-tree and posterior probabilities in MrBayes are indicated at each node. The actual percentages are given near each node which received less than 75% support, whereas shades of grey are used when both reconstruction methods retrieved higher support for the same node. The newly sequenced M. rosseti (ZMMU S-175291) and G. bucephalus (HMNH 21735) are not represented here, as they were identical to conspecifics.

Despite the relatively small geographic area of the state of Meghalaya, this discovery of a new genus in the country both confirm that this region is exceptionally rich in Chiropteran diversity, and certainly is still underexplored (Ruedi et al., 2012). With the present addition of E. denticulus from Meghalaya, the reported bat diversity of the state has increased to 66 species and that of India to 130 species (Saikia, 2018; Saikia et al., 2018; Chakravarty et al., 2020; Ruedi et al., 2021).