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9316
First record of Diadem Leaf-Nosed Bat from Andaman Islands hotspot (Myers et al. 2000). These islands are very rich
in their fauna and flora, and a great number of taxa are
endemic (Rao et al. 2013; Murugan et al. 2016).
The chiropteran fauna of the Andaman & Nicobar
Islands has been summarized by Hill (1967), and more
recently by Aul et al. (2014). Prior to the work of Aul et
al. (2014), it was noted that species of the Hipposideros
genus are restricted to the Nicobar Islands, and those of
genus Rhinolophus to the Andaman Islands. Historically,
as of 1967, one endemic subspecies — Hipposideros
diadema nicobarensis (Dobson, 1871) was reported from
Trinkut Island and Great Nicobar Island in the Nicobar
group of islands (Hill 1967). This subspecies was also
reported from Katchal Island (Aul & Marimuthu 2006).
Aul et al. (2014) summarized the chiropteran diversity of
the archipelago with a note on the effects of the 2004
Indian Ocean Tsunami, and also reported the presence
of two species of genus Hipposideros — H. fulvus and H.
larvatus, from the Andaman Islands. In this paper, we
report for the first time, the presence of the Diadem
Leaf-nosed Bat Hipposideros diadema from the Andaman
Islands and provide the first specimen-based record of
Hipposideros diadema masoni from India.
Study Area and Methods
The authors have been surveying the Andaman Island
group to document its chiropteran diversity since 2012.
In 2012, a short-term survey was conducted on Baratang
Island (1206’21”N & 92045’46”E), and subsequently a
survey of most major islands was conducted from 2014–
2016. During the initial survey on Baratang Island, the
first author (BS) sighted a large hipposiderid bat with
characteristic pale hairs on the flanks living amongst a
colony of rhinolophids and myotids in a limestone cave.
After this, on two occasions the same was sighted by us
in 2014 and 2015. In October 2015, we collected this
individual using a hoop net, took external morphometric
measurements using vernier calipers (Mitutoyo LC=0.01)
and made ultrasonic recordings using an Anabat SD1
(Titley Electronics). The bat escaped during transfer to a
collection bag. Following this, about a fortnight later, we
were alerted by some locals attempting to catch bats in
the same cave. By the time we arrived on location, they
had shot (using an air-rifle) a bat (Image 1), which on closer
observation was identified to be the large hipposiderid
bat that was caught by us before. The air-rifle pellet
had, unfortunately, damaged the skull. We collected
the specimen, preserved it as a voucher and deposited
it in the Natural History Museum, Osmania University,
Hyderabad, India. We also studied and compared the
Andaman specimen collected during the present survey
Srinivasulu et al.
with the specimens of large-bodied hipposiderids such
as Hipposideros diadema (H. d. masoni: ZSI-K 291/126L,
HZM 14.38116; H. d. nicobarensis: ZSI-K 10308, HZM
7.35313) and Hipposideros larvatus (ZSI-K 18554, ZSI-K
10290; HZM 17.34708; HZM 31.37787) at the Zoological
Survey of India, Kolkata (ZSI-K), West Bengal, India and
Harrison Institute (HZM), Sevenoaks, United Kingdom.
The following external and craniodental measurements
of the specimen were taken (all in mm): External: FA forearm length, E - ear length, Tl - tail length, Tib - tibia
length, Hf - hindfoot length, 3mt - third metacarpal,
4mt - fourth metacarpal, 5mt - fifth metacarpal, 1ph3mt
- first phalanx of third metacarpal, 2ph3mt - second
phalanx of third metacarpal, 1ph4mt - first phalanx of
fourth metacarpal, 2ph4mt - second phalanx of fourth
metacarpal, Craniodental, GTL - greatest length of the
skull, CBL - condylobasal length, CCL - condylocanine
length, CM3 - maxillary toothrow, C1-C1 - anterior palatal
width, M3-M3 - posterior palatal width, ZB - zygomatic
breadth, BB - braincase breadth, CM3 - mandibular
toothrow, M - mandible length.
Genetic analysis - A 3mm wing punch was taken from the
voucher specimen (AN2) and stored in silica gel. Genomic
DNA was extracted using a QIAGen Blood and Tissue kit
(QIAGen International, Netherlands). Polymerase Chain
Reaction was carried out and we amplified a portion
(~652 bp) of the mitochondrial cytochrome C oxidase
subunit I gene using the primer pair VFi_t1 (5’-TGTAA
AACGACGGCCAGTTCTCAACCAACCACAAAGACATTG-3’)
and
VR1_t1
(5’-CAGGAAACAGCTATG
ACTAGACTTCTGGGTGGCCAAAGAATC-3’) (Ivanova et
al. 2007). The PCR reaction was performed in a 25μl
reaction volume containing 2μl of template DNA, 12.5μl
of 2X reaction buffer (0.05 U/μL Taq DNA polymerase,
reaction buffer, 4 mM MgCl2, 0.4 mM of each dNTPs),
0.5μl of each primer, and 9.5μl nuclease free water. The
thermal profile followed included: 940C for 1 min, five
cycles of 940C for 30 s, 500C for 40 s, and 720C for 1 min,
followed by 35 cycles of 940C for 30 s, 540C for 40 s, and
720C for 1 min, with a final extension at 720C for 10 min
(Ivanova et al. 2007). The amplified PCR products were
sequenced using an ABI prism 3730 sequencer (Applied
Biosystems, USA) and Big dye terminator sequencing
kit (ABI Prism, USA). The gene sequence (Genbank
accession number will be provided in revision) obtained
was analyzed by using BLAST (Altschul et al. 1990) to
determine similar sequences in the NCBI (www.ncbi.
gov) database. Additional sequences of other related
species were retrieved from the NCBI GenBank database
for phylogenetic analysis. Rhinolophus lepidus was used
as an outgroup taxon. The sequences were aligned
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 September 2016 | 8(11): 9316–9321
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:9316
–9321
First record of Diadem Leaf-Nosed Bat from Andaman Islands Srinivasulu et al.
Table 1. External and craniodental measurements of H.d. masoni from Baratang Island (Andaman Islands, India), Myanmar and Indonesia
and H.d. nicobarensis from Great Nicobar Island, Nicobar Islands, India. Measurements are in mm. Abbreviations as stated in Study Area
and Methods, † After Kitchener et al. (1992), $ After Ith et al. (2011), - Data not available; * approximate measurement as skull is broken; **
premaxilla missing
Taxon
H.d. masoni
H.d. masoni
H.d. masoni†
H. diadema$
H.d. nicobarensis
Baratang Island,
Andaman Islands, India
Mawlamyine, Myanmar
Lesser Sunda, Indonesia
Cambodia
Great Nicobar Island,
Nicobar Islands, India
AN2
ZSI-K 291/126L
-
-
ZSI-K 10308
FA
91.55
85.09
80.2–90.2
83.2–93.2
66.06
E
27.01
27.94
25.2–28.2
23.3–30.8
22.55
Tl
51.28
–
–
44.3–57.2
35.78
Tib
34.41
34.29
29.7–33.1
33.5–37.8
25.42
Hf
13.67
–
–
15.1–18.1
11.31
3mt
70.12
–
58.8–66.9
-
48.64
4mt
67.47
–
57.3–66.0
-
49.59
5mt
59.26
–
53.7–60.7
-
44.75
1ph3mt
31.36
–
25.0–30.9
-
23.26
2ph3mt
30.05
–
–
-
21.83
1ph4mt
23.26
–
–
-
17.55
2ph4mt
15.72
–
–
-
9.17
Location
Catalogue No.
External
Craniodental
GTL
30.21
28.41
28.5–30.5
31.04–33.08
26.04**
CBL
27.40
–
–
27.81–29.74
–
CCL
27.51
–
26.0–27.0
27.41–28.83
23.10
CM
12.20*
12.21
11.2–11.7
12.46–12.96
9.49
7.97
7.76
7.0–7.8
8.04–8.47
6.64
M3–M3
12.57*
12.33
11.6–11.9
12.15–12.83
9.82
ZB
17.21*
17.75
17.1–18.2
17.81–19.17
14.49
3
C1–C1
BB
13.79
11.08
11.0–12.3
-
11.12
CM3
13.76*
13.22
13.7–13.9
13.62–14.38
11.03
M
22.46
21.50
22.1–22.7
21.83–23.05
17.51
long, broad at the base and gradually tapering towards
the tip, nostrils round in shape with well-developed
narial lappets; intermediate leaf (8.25mm wide) is fleshy
and with a median ridge; posterior leaf concave with the
terminal portion folding back slightly and is erect, large
(12.63mm wide) and fleshy with a single median vertical
septum forming a small projection above the margin,
and dividing the posterior leaf into two cells. A pair of
glandular swellings is present behind the posterior leaf
located above each eye on either side of the noseleaf.
No frontal sac observed behind the posterior leaf. Three
supplementary leaflets present. A bony projection
observed on the undersurface of the chin. Hair on the
back is cream coloured with greyish-brown terminal
portion, hairs on the shoulders extending up to beneath
the ears much darker, hairs on the flanks completely pale
cream in colour and form a continuous line on either side.
Wing and interfemoral membranes uniform pale brown
in colour. Hair on the face creamish coloured at the tips
with pale brown bases. The ventral surface is pale in
general. The noseleaf is yellowish-brown in colour, and
is fleshy.
Craniodental - Skull large with a condylocanine length
of 27.97mm. Sagittal and lambdoid crests well-developed
with a shallow depression in the frontal region. Zygoma
of each side robust, with well-developed dorsal process.
Length of upper toothrow (CM3) 12.20mm; pm2 minute
in comparison to pm3 and canine, partially extruded from
the toothrow, in contact with the base of the canine and
pm3; pm3 and canine not in contact with each other. Two
pairs of lower incisors, outer pair tricuspid and the inner
pair bicuspid; incisors in contact with canine; pm2 25% of
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 September 2016 | 8(11): 9316–9321
9319
First record of Diadem Leaf-Nosed Bat from Andaman Islands Image 2. Frequency–time graph of echolocation calls of Mason’s
Diadem Leaf-nosed Bat H.d. masoni from Baratang Island, Andaman
Islands, India
the height of pm3. A small conical bony process observed
on the symphysis of the mandible.
Echolocation calls - The echolocation calls of the
species were recorded using an Anabat SD1 (Titley
Electronics, Australia) bat detector. They were analysed
in AnalookW software and frequency-time graphs
were produced using a logarithmic scale of frequency
(0-200 kHz). Each call was defined as an individual,
discrete vocal pulse and the parameters measured
were maximum frequency (Fmax), minimum frequency
(Fmin), characteristic frequency (Fc) and duration (Dur).
The calls produced by this species were of constant
frequency (CF) with a short FM tail (Fig. 1). A total of
16 calls were recorded of which only five were of good
quality and were analyzed further. The calls consisted
of mean characteristic frequency (Fc) of 59.08±0.24 kHz
(range: 58.82–59.26 kHz), maximum frequency (Fmax)
of 59.88±0.25 kHz (range: 59.7–60.15 kHz), minimum
frequency (Fmin) of 54.40±1.97 kHz (range: 51.28–55.94
kHz) and duration of 4.77±0.62 ms (range: 3.67–5.24 ms).
The frequency characteristics of the echolocation calls
of the specimen from the Andaman showed similarities
with that of the South-east Asian forms, which produced
FMAXE in the range of 57.8–61.45 kHz (Phommexay
2009; Hughes et al. 2010).
Molecular analysis - Genetic analysis based on COI
gene sequences indicated that the Andaman specimen
of Hipposideros diadema is closely related to those from
Laos and Vietnam, along with which it forms a distinct
clade (Fig. 2) both in Maximum Likelihood and Bayesian
Inference methods. The specimens from Malaysia form a
separate clade. The phylogenetic position of H. diadema
from Andaman is supported by high posterior probability
(1.0) and bootstrap value (70.0). The relationship
between other members of the species group needs to
9320
Srinivasulu et al.
be studied further to confirm the phylogenetic status of
the H. diadema species group.
The echolocation calls, morphometrics (both external
and cranio dental measurements) and the genetic
analysis shows that the Andaman specimen matches
those of the Southeast Asian specimens of H. diadema.
The subspecies H.d. masoni (Dobson, 1872) is distributed
throughout the Indomalayan region and differs from
the typical H.d. diadema in possessing a single median
septum in the posterior leaf dividing it into two cells (vs. a
strong median septum with two weak lateral septa in H.d.
diadema) (Andersen 1907; personal observations). The
Andaman specimen matches H.d. masoni in possessing a
single median septum dividing the posterior leaf into two
cells, a small conical bony process from the symphysis of
the mandible, and by having wings attached to the base
of the outer toe (as opposed to wings attached to the
base of the ankle in H.d. diadema). Interestingly, H.d.
nicobarensis also shows similar characters as in H.d.
masoni but is significantly smaller in overall external and
craniodental measurements.
This is the first specimen-based record of H.d. masoni
(Dobson, 1872) from Baratang Island and from the
Andaman group of Islands, India. Our surveys in different
localities of Little Andaman Island, Rutland Island, South
Andaman Island, Middle Andaman Islands and islands
of the Ritchie Archipelago did not yield sightings of this
taxon. Even at the Baratang cave complex (consisting of
191 limestone caves) we detected this taxon only in one
cave. The existence of the H.d. masoni (Dobson, 1872)
in a cave on Baratang Island is enigmatic and requires
further surveys to establish its continued presence north
of 10O N latitude.
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Journal of Threatened Taxa | www.threatenedtaxa.org | 26 September 2016 | 8(11): 9316–9321
First record of Diadem Leaf-Nosed Bat from Andaman Islands Srinivasulu et al.
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Threatened Taxa
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9321
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ISSN 0974-7907 (Online); ISSN 0974-7893 (Print)
September 2016 | Vol. 8 | No. 11 | Pages: 9289–9396
Date of Publication: 26 September 2016 (Online & Print)
DOI: 10.11609/jott.2016.8.11.9289-9396
www.threatenedtaxa.org
Review
Notes
Distribution records and extended range of the Sri Lanka Frogmouth
Batrachostomus moniliger (Aves: Caprimulgiformes: Podargidae) in
the Western Ghats: a review from 1862 to 2015
-- Anil Mahabal, Sanjay Thakur & Rajgopal Patil, Pp. 9289–9305
New distribution record of the Bhutan Takin Budorcas taxicolor
whitei Hodgson, 1850 (Cetartiodactyla: Bovidae) in Bhutan
-- Tashi Dhendup, Tshering Tempa, Tsethup Tshering & Nawang
Norbu, Pp. 9365–9366
Short Communications
Small carnivores of Parambikulam Tiger Reserve, southern Western
Ghats, India
-- R. Sreehari & P.O. Nameer, Pp. 9306–9315
First record of the Diadem Leaf-Nosed Bat Hipposideros diadema
(E. Geoffroy, 1813) (Chiroptera: Hipposideridae) from the Andaman
Islands, India with the possible occurrence of a hitherto unreported
subspecies
-- Bhargavi Srinivasulu, Aditya Srinivasulu, Chelmala Srinivasulu,
Tauseef Hamid Dar, Asad Gopi & Gareth Jones, Pp. 9316–9321
Recent records and distribution of the Indian Brown Mongoose
Herpestes fuscus Gray, 1837 (Mammalia: Carnivora: Herpestidae)
from the southern Western Ghats, India
-- R. Sreehari, Sandeep Das, M. Gnanakumar, K.P. Rajkumar,
K.A. Sreejith, Navaneeth Kishor, Dhaneesh Bhaskar, P.S. Easa &
P.O. Nameer, Pp. 9367–9370
First record of Dobson’s Long-tongued Fruit Bat Eonycteris spelaea
(Dobson, 1871) (Mammalia: Chiroptera: Pteropodidae) from Kerala,
India
-- P.O. Nameer, R. Ashmi, Sachin K. Aravind & R. Sreehari, Pp. 9371–
9374
New distribution records of Mesoclemmys vanderhaegei
(Testudines: Chelidae) from southeastern Brazil, including
observations on reproduction
-- Fábio Maffei, Bruno Tayar Marinho do Nascimento, Guilherme
Marson Moya & Reginaldo José Donatelli, Pp. 9322–9326
Road kills of the endemic snake Perrotet’s Shieldtail Plectrurus
perrotetii, Dumeril, 1851 (Reptilia: Squamata: Uropeltidae) in
Nilgiris, Tamil Nadu, India
-- P. Santhoshkumar, P. Kannan, B. Ramakrishnan, A. Veeramani,
A. Samson, S. Karthick, J. Leonaprincy, B. Nisha, N. Dineshkumar,
A. Abinesh, U. Vigneshkumar & P. Girikaran, Pp. 9375–9376
Spiders (Arachnida: Araneae) of Gujarat University Campus,
Ahmedabad, India with additional description of Eilica tikaderi
(Platnick, 1976)
-- Dhruv A. Prajapati, Krunal R. Patel, Sandeep B. Munjpara, Shiva S.
Chettiar & Devendrasinh D. Jhala, Pp. 9327–9333
Reappearance of the rare Shingle Urchin Colobocentrotus
(Podophora) atratus (Camarodonta: Echinometridae) after eight
decades from the rocky shore of Kodiyaghat (Port Blair), South
Andaman Islands, India
-- Vikas Pandey & T. Ganesh, Pp. 9377–9380
New records of Termite species from Kerala (Isoptera: Termitidae)
-- Poovoli Amina, K. Rajmohana, K.V. Bhavana & P.P. Rabeeha,
Pp. 9334–9338
Sallywalkerana, a replacement name for Walkerana Dahanukar et al.
2016 (Anura: Ranixalidae)
-- Neelesh Dahanukar, Nikhil Modak, Keerthi Krutha, P.O. Nameer,
Anand D. Padhye & Sanjay Molur, P. 9381
Odonata (Insecta) diversity of southern Gujarat, India
-- Darshana M. Rathod, B.M. Parasharya & S.S. Talmale, Pp. 9339–
9349
An update on the distribution pattern and endemicity of three
lesser-known tree species in the Western Ghats, India
-- K. Sankara Rao, N.V. Page, A.N. Sringeswara, R. Arun Singh &
Imran Baig, Pp. 9350–9355
Heavy metal distribution in mangrove sediment cores from selected
sites along western coast of India
-- P. Vidya & Rajashekhar K. Patil, Pp. 9356–9364
A sighting of Plastingia naga (de Nicéville, [1884]) (Lepidoptera:
Hesperiidae: Hesperiinae) from central Assam, India
-- Gaurab Nandi Das, Arajush Payra & Bitupan Boruah, Pp. 9382–9383
A note on the taxonomy, field status and threats to three endemic
species of Syzygium (Myrtaceae) from the southern Western Ghats,
India
-- R. Ramasubbu, C. Divya & S. Anjana, Pp. 9384–9390
Arnebia nandadeviensis Sekar & Rawal (Boraginaceae) a new
synonym of Onosma bracteata Wall.
-- Umeshkumar L. Tiwari, Pp. 9391–9393
Exosporium monanthotaxis Piroz. (Fungi: Ascomycota:
Pezizomycotina) from Biligirirangan Hills, southern India
-- Rashmi Dubey & Shreya Sengupta, Pp. 9394–9396
Threatened Taxa