BatsinBareilly Publishedin2019 Beenaothers 1679 4544 1 SM11
BatsinBareilly Publishedin2019 Beenaothers 1679 4544 1 SM11
BatsinBareilly Publishedin2019 Beenaothers 1679 4544 1 SM11
net/publication/344157625
A Report on Bat Species Identified in Bareilly, Uttar Pradesh, India with a Brief
Description of Their Ecology. International Journal of Ecology and
Environmental Sciences 45 (2):...
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Division of Pathology, Indian Veterinary Research Institute, Izzatnagar, Bareilly 243122, Uttar Pradesh, India.
@
Current address: Indian Institute of Toxicology Research, M.G. Marg, Lucknow 226001, U.P., India
ABSTRACT
In a survey of the Indian Veterinary Research Institute campus and adjoining villages around Bareilly city of Uttar Pradesh, India,
five species of bats (order Chiroptera) were identified and their morphometric features and habitat were examined. During the
period from August, 2016 to July, 2018, a total of 24 individual bats were observed. They belonged to families Pteropodidae
(Pteropus giganteuss, Rousettus leschenaultii, Cynopterous sphinx) and Vespertilionidae (Pipistrellus coromandra, Scotophilus
heathii). Based on morphometric measurements, PCR amplification and sequencing of mt DNA, COI gene and field surveys, the
different species were recognised. In the study area, species of Fig trees, Sirius, Eucalyptus, Leechi, Mahua trees and other flora
provide a suitable habitat for different frugivorous bat species. A brief note on the ecology of these bats is provided.
16srRNA on faecal samples as in other wild species. period, humidity was maximum in August (89.15%) and
PCR based species identification studies relies mainly on minimum in March (48.96%), whereas the highest
amplification two mtDNA genes (cyt b and COI) (Pastor- temperature was recorded in May (44.17 0C ) and lowest
Beviá et al. 2014) and their sequencing. in January (4.71 0C) (Weather station, Physiology &
The Indian Veterinary Research Institute Campus Climatology division, IVRI).
and adjoining villages in Bareilly provides suitable
habitat for different bat species and prevailing species of
bats were examined during the study period. The status METHODOLOGY:
and diversity of bat species prevalent in the area was
studied by morphometry and DNA barcoding. The During the period August, 2016 to July, 2018, fresh bat
roosting sites twere observed for understanding their fecal samples were collected from their roosting and
habitat preference and foraging behavior. foraging areas in and around IVRI campus and adjoining
villages in Bareilly. Clean polythene sheets measuring
2.0 X 2.0 m were placed under known bat roosting and
STUDY AREA foraging sites after sunset, 7.00 PM. The fresh fecal
samples were collected the following morning between
The present study was undertaken in the campus of the 5:30 to 6:00 AM in vials containing RNA later. The
Indian Veterinary Research Institute (IVRI), Izatnagar samples were then transported to the laboratory, labeled
and in the adjoining villages in Bareilly which falls properly and stored at !80°C until analyzed. Detailed
between 28° 20' to 28° 54' N and 78° 58' to 79° 47' E in information of bat roosting and foraging areas (latitude,
western Uttar Pradesh (Figure 1A &1B). Bareilly has a longitude, temperature, humidity of these areas, roosting
total area of 235 km2 and a population density of about and foraging tree species, activity of different bat species
3800 km-2 (Census 2011). The climate has subtropical on climate basis and foraging vegetation and density)
features with an average temperature of 45 0C in summer were noted. The colony size was assessed through direct
and 4 0C in winter, and average rainfall of 990 mm in count using binocular and photographic methods (Tuttle
monsoon. The city is on Ganges plain, leveled and well 1979). Bats, found dead or moribund were collected
irrigated land for growing sugarcane, rice, pulses and from different sites in the study area which included
wheat. The climatic conditions of the Institute campus Bareilly city and nearby villages. They were either found
significantly varied during the year. During the study clinging to the high voltage electrical wires, fish nets
Figure 1B: Roosting and foraging areas of different bat species found in IVRI campus
over ponds or injured ones lying on the ground after a Table 1. Details of bat specimens used for morpho-metry
storm. The live Pipistrelle bats were captured using mist during study periods
nets, permission for which was obtained from concerned
agency.
Identification of bat species was carried out by PCR ID Species Sex Age Condition
amplification of COI genes and by analyzing the
BS1 Pteropus sp. Female Adult Electrocuted
morphometric measurements as well as some external
BS2 Cynopterus sp. Female Adult Electrocuted
key characters. The morphological measurements were BS3 Pteropus sp. Female Adult Electrocuted
recorded by digital vernier calipers and the data were BS4 Scotophilus sp. Female Adult Dead
compared with Bates and Harrison (1997) and recent BS5 Pteropus sp. Female Adult Moribund
available literatures. Details of the specimens collected BS6 Pteropus sp. Female Adult Dead
during the study are provided in Table 1. The order wide BS7 Pteropus sp. Male Adult Dead
species of Chiroptera were identified from the faecal BS8 Rousettus sp. Female Adult Dead
samples by amplifying the mitochondrial gene Cyto- BS9 Pteropus sp. Male Adult Moribund
BS10 Pteropus sp. Male Adult Injured
chrome-c oxidase-I (published primers) (Walker et al.
BS11 Pteropus sp. Female Adult Dead
2016). BS12 Pteropus sp. Female Adult Electrocuted
BS13 Pteropus sp. Male Adult Electrocuted
DNA Extraction, PCR Amplification BS14 Pteropus sp. Female Adult Injured
and Sequencing: BS15 Pteropus sp. Female Adult Electrocuted
BS16 Cynopterus sp. Female Adult Moribund
The faecal samples collected from same locations were BS17 Scotophilus sp. Female Adult Injured
pooled together and resuspended in 1XPBS and homo- BS18 Pteropus sp. Female Adult Electrocuted
BS19 Pipistrella sp. Female Adult Live
genized in Fast prep-24 containing ceramic beads at a
BS20 Pipistrella sp. Female Adult Live
rate of 5.5M/S for 30 second. It was repeated 3-4 times BS21 Pipistrella sp. Female Adult Live
based on the homogenization of the suspension. The BS22 Pipistrella sp. Female Adult Live
collected homogenate was then centrifuged at 5000 RPM BS23 Pipistrella sp. Female Adult Live
for 10 minutes and the supernatant was re- centrifuged at BS24 Pipistrella sp. Male Adult Live
13000 RPM for 20 minutes. A volume of 5 mL was
232 Beena et al.: Bat species in Bareilly, India Int. J. Ecol. Environ. Sci.
filtered through 0.22 ìm filter (Millipore) and 280 ìL of A total of 24 bats were collected during study
the filtrate was used for DNA extraction using period including dead, electrocuted and live bats which
commercially available QIAamp DNA stool Mini Kit had fallen on ground or were injured. The body weight
(Qiagen, Valencia, CA, USA). and body measurements of these bats were recorded and
Total genomic DNA was also isolated from tissue species was identified. The details of morphometry of
samples using the DNAeasy Tissue Kit (Qiagen, the bats that were used for species identification, are
Valencia, CA, USA) according to the manufacturer’s presented in the Table 2.
instructions. The mitochondrial gene Cytochrome c
oxidase I that target 202 bp were amplified using a Ecology
forward sequence and reverse sequence of
5’-GTHACHGCYCAYGCHTTYGTAATAAT-3’ and The roost searches were carried out to find out the
5’-CTCCWGCRTGDGCWAGRTTTCC-3’ respectively. roosting ecology of the bats and the following roost and
PCR was performed using reaction volume containing foraging location and characteristics were recorded
12.5 ìL MasterMix with loading dye (Dream Taq green (Table 3).
PCR master mix (2X), Thermoscientific), 10 ìl In this study, Pteropus giganteus was found to be
sterilized distilled water, 1.5 ìl extracted DNA largest in size compared to all other bats with a body
(approximately 20 ng ìL!1), and 0.5 ìL forward and weight of 550 to 825 g and a wing span ranging from
reverse primers (10 ìM). The PCR protocol included an 108-125 cm. They are nocturnal animals having longer
initial denaturing step at 95 °C for 3 min, followed by snouts, larger eye sockets and smaller ears, giving them
35 cycles of 95 °C for 1 min, 52 °C for 1 min and 72 °C a more dog-like appearance (flying foxes). Aina,
for 1 min with a final extension at 72 °C for 10 min. Rupapur villages and Bareilly cantonment areas are the
The amplified DNA fragments were resolved on a 1.0% common roosting places for pteropus bats seen in study
(w/v) agarose gel (1 × Tris Acetate-EDTA buffer), area (Figure 2), In Rupapur village and in Bareilly
stained with ethidium bromide and visualized with UV cantonment area (roosting places) these bats were found
light (Gel Logic 212 PRO, Care-stream Health, Inc.). to colonize in hundreds during August and on a visit in
The ampli-fied product was purified by using DNA January next year the population was found reduced. In
extraction kit (GeneJETTM Gel Extraction Kit, roosting areas especially in Rupapur village during day
Fermentas) as per manufacturer’s recommended protocol time, they fan their wings and make lot of noise where
and sent for sequencing to Eurofins Genomics, India Pvt. they collectively hang upside down on their roosting
Ltd, Bengaluru. trees like Eucalyptus and Sirius tree (Albizia lebbeck)
(Figure 3). During field surveys, in roosting places at
sunset time, some bats start circling over roosting tree
RESULTS and nearby trees and as time advanced, their movements
also increased with loud noises and almost all of them
Species Identification left for foraging within one hour after sunset. The move-
ment of these Pteropus bats was governed by food
During the study period, five species of bats belonging sources. They flew continuously for long distances with
to two families were identified among the study varying height, depending on topography. Pteropus bats
population. They are three species of fruit bats and two from Rupapur village often visited the IVRI campus for
species of insectivorous bats identified from fecal DNA foraging on different fruits, especially Ficus, mahua,
and also from the tissue of few collected bats by leechi which are found in various locations in the
amplifying and sequencing of COI gene. The barcode campus (near Kendriya Vidyalaya (KV), infront of
sequences were analysed by BLAST search in GenBank. Germplasm centre building and PM house). It was
The bats species were identified as Pteropus giganteus noticed that they start back to roosting places after
(Brünnich, 1782), Cynopterous sphinx (Vahl, 1797), foraging just before the dawn. Usually between 3.00AM
Rousettus leschenaultia (Desmarest,1820), Scotophilus to 4.00AM, these bats were found flying back to their
heathii (Horsfield, 1831) and Pipistrellus coromandra roost and at around 5.00-6.00AM all the bats were back
(Gray, 1838). All the COI sequences were deposited in to their roost. From the faecal samples and spit out
GenBank under accession no MH910622, MH910623, material collected in roosting places, it was evident that
MH910624, MH910625 and MH910626, respectively. they extract the pulp of the fruits, vegetables and also
45: 229-239 Beena et al.: Bat species in Bareilly, India 233
Table2. The list of bats identified during study period and its morphometry in cm
Morphometry Pteropus giganteus Rousettus leschenaultii Cynopterous sphinx Pipistrellus coromandra Scotophilus heathii
(n=13) (n=1) (n=2) (n=6) (n=2)
Abbrevations: BW: Body weight measured in gm; HBL: head and body length; HF: hindfoot length; TIB: length of tibia; FA: forearm length;
WSP: wing span; TL: Thumb length; 2Mc: length of second metacarpal; 3Mc: length of third metacarpal, 3Mc.1p: first phalanx of the third
metacarpal, 3Mc.2p: second phalanx of the third metacarpal; 4Mc: fourth metacarpal; 4Mc.1p: first phalanx of the fourth metacarpal; 4Mc.2p:
second phalanx of fourth metacarpal; 5Mc: fifth metacarpal; 5Mc.1p: first phalanx of the fifth metacarpal; 5Mc.2p: second phalanx of fifth
metacarpal, NA: Not Applicable, ND: Not Done
forages on leaves of those trees. These roosting places during February to April. Second most abundant species
noticed were permanent over the years for these bats but studied was Cynopterus sphinx, which occurred within
their number seems to be reduced during winters, the campus (JDR, OCBII & OCBIII).
perhaps due to shifting to hibernation roosts. Usually the These bats are of medium size with a body weight
females give birth to one young in a year after a period of 49-54g, long snout, paler silky and fine fur. This
of 6 month gestation. In one injured bat we found both species is differentiated from the Rousettues lesche-
the uterine horns were enlarged. One horn carries naultii by its white edged wing bones and ears (Figure
completely developed foetus and other one was having 4). A total of 12 colonies were noticed during the study
macerated foetus. The females were observed pregnant period in which 9 colonies were seen inside cylindrical
234 Beena et al.: Bat species in Bareilly, India Int. J. Ecol. Environ. Sci.
Figure 2A. Pteropus giganteus seen at Bareilly cantonment area Figure 2B. Pteropus giganteus seen in Aina village
S.N Roost location Tree species Species of bat No. of groups /harem Number of occupants
(roosting density) per group
1 IVRI Campus
1.1 OCB-II White fig (Ficus virens/ Cynopterous sphinx Roosting area 4-5
Ficus infectoria) (3 groups)
1.2 OCB-III White fig (Ficus virens/ Cynopterous sphinx Roosting area 3-4
Ficus infectoria) (3 groups)
1.3 Kendriya Vidhyalaya Mahua tree (Madhuca indica ) Pteropus giganteus Foraging area 20-30
(KV) (2 group)
1.4 NEAR CARI Banyan fig (Ficus bengalensis) Cynopterous sphinx Roosting area 3-4
(3 groups)
1.5 Jt Director Research White fig (Ficus virens/ Cynopterous sphinx Roosting area 5-6
JD® Ficus infectoria) (3 groups)
1.6 Germplasm Centre Mahua tree (Madhuca longifolia ) Pteropus giganteus Foraging area 20-30
(2 group)
1.7 Postmortem (PM) Banyan fig (Ficus bengalensis) Pteropus giganteus Foraging area
(2 group) 25-30
1.8 Pathology Experimental Grooves on building Scotophilus heathii Roosting area -
Animal Shed
1.9 Modular Lab Building Grooves on building Pipistrellus coromandra Roosting area 6-8
(3 groups)
2 Bareilly Cantt. Eucalyptus (Eucalyptus tereticornis) Pteropus giganteus Roosting area 250-500
and Siris tree (Albizia lebbeck) (4 groups)
3 Rupapur village Ficus insipida, Ficus religiosa, Pteropus giganteus Roosting area 350-500
Eucalyptus (Eucalyptus tereticornis) (3 groups)
and Siris tree (Albizia lebbeck)
Aina village Ficus insipida, Ficus religiosa Pteropus giganteus Roosting area 200-300
(3 groups)
45: 229-239 Beena et al.: Bat species in Bareilly, India 235
Figure 3. Pteropus giganteus seen hanging on Sirius tree at Rupapur Figure 4. Cynopterus spinx colony seen inside the grooves of Ficus
village virens tree trunk in front of JD(R)
Figure 5A&B: Cynopterus spinx colony seen in the outdoor lamp shades hanging on Ficus virens inside IVRI campus
outdoor lamp shades hanging on trees and three in the on seasonal availability) and feces appeared as dark ink
groove of tree trunks. They seemed to colonize as a like staining on the paper spread on the ground for
cluster of 5-7 bats in the outdoor lamp shades hanging on sample collection in the roosting areas. The Rousettus sp.
trees as well as in the crevices of the trees in these was found roosting on the ceilings of some abandoned
localities (Figures 5A & B). A fall in the number of bats buildings in the campus premises and shares the foraging
of this species was noticed during the study period esp. trees along with other frugivorous bats (Figure 6).
in winter time. Like the Pteropus species, its movement During flight females carries their young ones along with
was noticed after dusk and after foraging they returned them. We got one such sample in a fish net placed across
to the roosting site before dawn. The materials spitted the fish pond.
out by these bats usually contained seeds (guava, based
236 Beena et al.: Bat species in Bareilly, India Int. J. Ecol. Environ. Sci.
Figure 6. A fulvous bat fruit bat (Rouesttus Leschenaultii) foraging Figure 7. An insectivorous bat (Pipistrellus comorandra) captured
on a guava tree at night from a wall crevices having broad muzzle, pale ventral part and
oval shaped ears with folds at middle and presence of an
ectoparasite on left ear flap.
The insectivorous bats identified in the study area
were Pipistrella coromandra (Indian pipistrella) and
Scotophilus heathii. Pipistrella coromandra is a very
small bat ranging in wing span length of 1.8-2.2 cm and
a body mass of 5-7g. It has a broad muzzle, dark
brown dorsal and a paler ventral part (Figure 7). The
ears were round to oval with folds in middle edge. In our
campus we identified this species of bats in the cracks
and crevices of walls and old ceilings in hostel. In
evening its foraging was noticed very early compared to
other bat species i.e around 5.00-5:30 PM in winters and
6:30-7.00 PM in summers. It has a different pattern of
flight with a jerky movement, while feeding on insects
mainly mosquitoes in the beginning of summers and
small moths, insects in winters was observed. Following
rain/showers insects attract to light also attract these bats
for feeding. Some bats which we got in the month of
March, from grooves in wall of house were pregnant
with twins. They were seen as a maternity colony, 5-6
pregnant females with both horns pregnant. Figure 8. A moribund insectivorous bat (Scotophilus heathii) found
One female Scotophilus heathii was found on the on the ground near the experimental animal shed on the campus
ground near the Experimental animal shed in the
campus. The bat was found very week and after some
time it was dead and this specimen was used for species
identification. Its external features like robust head,
absence of yellow coloured ventral plumage, sheathed to catch its prey. Following rain/showers, insects are
tail and body measurements suggest the species was attracted to light and hence these bats come out in large
Scotophilus heathii (Figure 8). It was confirmed by number for feeding on them. Compared to Pipistrella
amplifying and sequencing mtDNA, Cytochrome Oxidase bats, during foraging time the flight height from ground
I gene. Since this species is insectivorous, they were of these bats was very less and sometimes they moved
usually noticed in the evening moving near street lights very close to humans.
45: 229-239 Beena et al.: Bat species in Bareilly, India 237
analysis revealed that these bats feed on a wide range of Bates, P.J.J. and D.L. Harrison. 1997. Bats of the Indian
insects of order Diptera, Hymenoptera, beetles and Subcontinent. Harrison Zoological Museum, Kent, England,
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Hahn, M.B.; Gurley, E.S.; Epstein, J.H.; Islam, M.S.; Patz, J.A.;
Daszak, P. and Luby, S.P. 2014. The role of landscape
CONCLUSION composition and configuration on Pteropus giganteus roosting
ecology and Nipah virus spillover risk in Bangladesh. The
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bats. Suitable roosting and foraging places were needed Roost selection and roosting ecology of fulvous fruit bat,
for the successful life and survival of bats. Good Rousettues leschnaulti (Pteropodidae). International Journal of
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dark roosting places such as grooves on trees, man-made Kumar, M.; Priya, Y.S.; Mathur, V. and Elangovan, V. 2016.
Distribution and conservation issues of Indian flying fox,
structures like buildings, artificial lights etc. are
Pteropus giganteus in Uttar Pradesh. Souvenir, International
preferred by these bats. Availability of these require- Day for Biological Diversity: 133-139. Uttar Pradesh State
ments in the campus attracted the large frugi-vorous bats Biodiversity Board, Lucknow.
from nearby places in the outskirts of Bareilly city and Kunz, T.H.; Torrez, E.B.; Bauer, D.; Lobova, T. and Fleming, T. H.
the insectivorous bats have plenty of roosting sites in the 2011. Ecosystem services provided by bats. Annals of New
campus where many farm animals are housed and the York Academy of Sciences 3: 1–38.
land is cultivated for fodder, and grains. More systematic Mildenstein, T.L.; Stier, S.C.; Nuevo-Diego, C.E. and Mills, L.S.
and intensive survey on different bat species is needed. 2005. Habitat selection of endangered and endemic large
flying-foxes in Subic Bay, Philippines. Biological Conserva-
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This study was made at the Swine diseases laboratory, Pierson, E.D. and Rainey, W.E. 1992. The biology of flying foxes of
Division of pathology, IVRI. We acknowledge the the Genus Pteropus: A review. Pages 1-17, In: Wilson, D.E.
Director of the Institute for providing facilities for it. and Graham, G.L. (Editors) Pacific Island Flying Foxes:
Author Contributions: The first author Dr Beena V, Proceedings of an International Conservation
Conference. Biological Report 90(23). Fish and Wildlife
had completed this work as part of her PhD at IVRI. She
Service, U.S Department of the Interior, Washington, DC.
made field surveys, collected samples, processed and Rainey, W.E., Pierson, E.D., Elmqvist, T. and Cox, P.A. 1995.The
compiled the results. The second author assisted in role of flying foxes (Pteropodidae) in oceanic island ecosystem
sample collections and sample processing. Dr Saikumar, of the Pacific. pages 47-62, In: Racey, P.A. and Swift, S.M.
planned the study, supervised the research and guided in (Editors) Ecology, Evolution and Behavior of Bats. Oxford
preparing the manuscript. University Press, London. 421 pages.
Rajasekar, R.; Chattopadhyay, B. and Sripathi, K. 2006. Depositing
Conflict of Interest: No conflict of interest to declare. masticated plant materials inside tent roosts in Cynopterus
sphinx (Chiroptera: Pteropodidae) in Southern India. Acta
Chiropterologica 8: 269-274.
Ruedi, M.; Mukhim, D.K.B.; Chachula, O.M.; Arbenz, T. and
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