in wildlife and ecology faculty of fisheries and...

BATS (CHIROPTERA: MAMMALIA) OF MALAKAND

DIVISION, PAKISTAN

BY

MOHAMMAD SALIM

2007-VA-543

A THESIS SUBMITTED IN THE PARTIAL FULFILLMENT

OF THE REQUIREMENTS FOR THE DEGREE

OF

DOCTOR OF PHILOSPHY

IN

WILDLIFE AND ECOLOGY

FACULTY OF FISHERIES AND WILDLIFE

UNIVERSITY OF VETERINARY AND ANIMAL SCIENCES

LAHORE, PAKISTAN

2016

To,

The Controller of Examinations,

University of Veterinary and Animal Sciences,

Lahore.

We, the supervisory committee, certify that the contents and the form of thesis, submitted by

Mohammad Salim, Registration No. 2007-VA-543 have been found satisfactory and

recommend that it be processed for the evaluation by the External Examination for award of the

Degree.

SUPERVISORY COMMITTEE

SUPERVISOR: __________________________________________

(DR. ARSHAD JAVID)

CO-SUPERVISOR: __________________________________________

(DR. MUHAMMAD SAJID NADEEM)

MEMBER: __________________________________________

(DR. ZULFIQAR ALI)

MEMBER: __________________________________________

(Prof. DR. AZHAR MAQBOOL)

i

DEDICATION

I dedicate the fruit of my humble efforts

To

My Beloved mother Kha Bibi

Who nourished me at my first cry and taught me the first word in this Universe

My affectionate father Sherin Taj

Who provided me each and every facility of life from cradle to adulthood and took

me to school for attaining higher ideals of life

My Brothers & Sisters

and

My better half Ruqia Nisar

My cute kids Zainab Salim, Mohammad Abdullah, Humaira Salim, Salma Salim

and Asma Salim

for their patience

&

My Uncle

For being my guardian during my educational career

ii

ACKNOWLEDGEMENTS

Praise is only for Allah the Almighty, the Lord of the Universe, the most Gracious, the most

Beneficent and the most Merciful and His Holy Prophet Muhammad (PBUH) who is the

ultimate source of knowledge and guidance for humanity.

I feel great pleasure to express my heartiest gratitude and deep sense of obligation to my

distinguished supervisor Dr. ARSHAD JAVID, Assistant Professor, Department of Wildlife and

Ecology, UVAS, Lahore for his generous and wise guidance, keen interest in research,

constructive criticism, constant encouragement and valuable suggestions throughout my Ph.D

study and research work. Since he has established bat science as a separate discipline in the

country, arranged funding for this study and helped me lot in confirming taxonomy of all the bats

captured from Malakand and above all worked day and night with me to refine this manuscript.

I feel great honor to express my gratitude to the members of my Supervisory Committee, Dr.

Muhammad Sajid Nadeem, Associate Professor, Department of Zoology, University of Arid

Agriculture, Rawalpindi, Dr. Zulfiqar Ali, Associate Professor, Department of Zoology,

University of the Punjab and Prof. Dr. Azhar Maqbool Chairman, Department of Parasitology,

for their guidance and encouragement. I extend my special & heartiest thanks to Dr. Momin

Khan Veterinary Officer (H) incharge C.V. H Harichand, Charsadda district for his encouraging

attitude during whole span of my study. I am very thankful to Dr. Fehmeeda Bibi Assistant

Professor, Department of Livestock & Poultry production, BZU, Multan. I also express my

sincerest sense of gratitude to my best friends Mr. Faiz-ur-Rehman Lecturer, Shaheed Benazir

Bhutto University, Sheringal (Dir Upper), Dr. Kamran Alam Lecturer, University of Haripur

and Mr. Iftikhar Ali MS student NUST, Islamabad for their keen interest in this study and

valuable practical help in my research and thesis. I acknowledge special thanks to my brothers

Amjid Ali, Sajid Ali and Wajid Ali for their valuable support, cooperation, guidance and

patience during field sampling.

I extend my special & heartiest thanks to My Lab fellows and to all those workers who worked

long hours in field to make working environment conducive for me.

Mohammad Salim

iii

TABLE OF CONTENTS

DEDICATION (i)

ACKNOWLEDGEMENTS (ii)

LIST OF TABLES (iv)

LIST OF FIGURES (vi)

CHAPTERS TITLE PAGE NO.

1. INTRODUCTION 1

2. REVIEW OF LITERATURE 4

3. RESULTS 38

Publication 3.1.

Distribution of Indian Flying Fox Pteropus giganteus Brünnich,

1782 in four Districts of Khyber Pakhtunkhwa.

40

Publication 3.2. Distribution records of fruit bats Cynopterus sphinx and

Rousettus leschenaultii from Khyber Pakhtunkhwa, Pakistan.

50

Publication 3.3. Morphological differentiation in two closely-related mouse-

tailed bat species (Chiroptera: Rhinopomatidae) captured from

Malakand division, Khyber Pakhtunkhwa, Pakistan.

67

Publication 3.4. Description of the first record of the Indian False Vampire Bat

(Megaderma lyra) E. Geoffroy, 1810 (Rhinopomatidae:

Chiroptera) captured from Northwestern Pakistan.

87

Publication 3.5. Morphological differentiation in two closely-related horseshoe

bat species (Chiroptera: Rhinolophidae) captured from Malakand

Division, Khyber Pakhtunkhwa, Pakistan.

95

Publication 3.6. New provincial record of the fulvous leaf-nosed bat

Hipposideros fulvus Gray, 1838 from Khyber Pakhtunkhwa,

Pakistan.

108

Publication 3.7. Two new bat species (Chiroptera: Mammalia)

for Pakistan: Miniopterus fuliginosus and Myotis formosus. 119

Publication 3.8. Diversity of some bat species (Family

Vespertilionidae) from Malakand Division, Pakistan. 129

Publication 3.9. Morphological features of the bats of genus

Pipistrellus from Malakand division, Khyber Pakhtunkhwa,

Pakistan.

148

Publication 3.10. First provincial record of desert yellow bat

Scotoecus pallidus (Dobson, 1876) from Khyber Pakhtunkhwa,

Pakistan.

170

4. SUMMARY 180

iv

LIST OF TABLES

TABLE

NO. TITLE

PAGE

NO

Publication 3.1.

3.1.1 Location and elevation of the five roosts of Pteropus giganteus in

Kyber-Pakhtunkhwa. 58

3.1.2

Pteropus giganteus counted on different tree species in five roosting

sites of Khyber Pakhtunkhawa from June 2008 through December

2008 (Fishing Hut, Pul Chowkai, Poji ground, Chail Kandoa Baba

Ghaffar Khan Village).

46

Publication 3.2.

3.2.1

Comparison of external body measurements (mm) of Cynopterus

sphinx (n=1) captured during present study with Aziz et al. (2007),

Senacha et al. (2006), Matveev (2005) and Bates and Harrison (1997).

60

3.2.2

Comparison of cranial measurements (mm) of Cynopterus sphinx

(n=1) captured during present study with Bates and Harrison (1997)

and Matveev (2005).

61

3.2.3

Comparison of external body measurements (mm) of Rousettus

leschenaultii (n=22) captured during present study with Bates and

Harrison (1997), Roberts (1997), Matveev, (2005) and Aeshita et al.

(2006).

62

3.2.4

Comparison of cranial measurements (mm) of Rousettus leschenaultii

captured during present study with Bates and Harrison (1997) and

Matveev (2005).

63

3.2.5 Mean bacular measurements (mm) of Rousettus leschenaultii captured

from Tura Gata in Malakand district. 63

Publication 3.3.

3.3.1

Comparison of external body measurements (mm) of Rhinopoma

microphyllum captured during present study with Rahman et al.

(2015), Benda et al. (2009), Davis, (2007), Bates and Harrison (1997),

Roberts (1997) and Schlitter and Qumsiyeh (1996).

77

3.3.2

Comparison of cranialmeasurements (mm) of Rhinopoma

microphyllum captured during present study with Rahman et al.

(2015), Benda et al. (2009), Bates and Harrison (1997) and Schlitter

and Qumsiyeh (1996).

78

3.3.3

Comparison of external body measurements (mm) of Rhinopoma

hardwickii captured during present study with Javid et al. (2012),

Benda et al. (2009), Davis, (2007), Bates and Harrison (1997),

Roberts (1997) and Qumsiyeh and Jones (1986).

79

3.3.4

Comparison of cranial measurements (mm) of Rhinopoma hardwickii

captured during present study with Javid et al. (2012), Benda et al.

(2009), Bates and Harrison (1997) and Qumsiyeh and Jones (1986).

80

3.3.5

Comparison of bacular measurements (mm) of Rhinopoma

microphyllum captured during present study with Rhinopoma

hardwickii (Javid et al. 2012).

81

v

Publication 3.4.

3.4.1

Comparison of mean external body and cranial measurements (mm)

of Megaderma lyra captured from Heroshah tehsil Dargai in

Malakand district (present study) with previous studies from South

Asia (Bates and Harrison, 1997) and Pakistan (Roberts, 1997).

88

Publication 3.5.

3.5.1

Comparison of mean external body and cranial measurements (mm)

of Rhinolophus ferrumequinum (n=2) captured from Loya Agra in

Malakand district with previous study from South Asia.

102

3.5.2

Comparison of mean external body measurements (mm) of

Rhinolophus lepidus (n=3) captured from University of Malakand in

Malakand district with a previous study from South Asia.

105

Publication 3.6.

3.6.1

Comparison of external body, cranial and bacular measurements

(mm) of Hipposideros fulvus captured during present study with

Roberts (1997), Bates and Harrison (1997) and Saikia et al. (2006).

115

Publication 3.7.

3.7.1

Wing measurements (mm) of Miniopterus fuliginosus (n = 1) and

Myotis formosus (n = 5) captured from Malakand Division,

Pakistan.

121

3.7.2

Comparison of external body and cranioental measurements (mm) of

Miniopterus fuliginosus (n=1) and Myotis formosus (n=5) captured

from Malakand Division (present study) with Sramek et al. (2013)

and Bayes and Harrison (1997), respectively.

122

Publication 3.8.

3.8.1 External body measurements (mm) of four species of family

Vespertilionidae captured from Malakand Division. 143

3.8.2 Cranial measurements (mm) of four species of family


3.8.3 Mean bacular measurements (mm) of four species of family


Publication 3.9.

3.9.1 Mean body mass (g) and external body measurements (mm) of five

species of the genus Pipistrellus captured from Malakand Division. 165

3.9.2 Cranial measurements (mm) of five species of the genus Pipistrellus

captured from Malakand Division. 166

3.9.3 Bacular measurements (mm) of five species of the genus Pipistrellus

captured from Malakand Division. 166

Publication 3.10.

3.10.1

Comparison of body mass (g) and external body measurements (mm)

of Scotoecus pallidus specimens captured from different localities in

Malakand division, KPK with available.

176

3.10.2

Comparison of cranial and bacular measurements (mm) of Scotoecus

pallidus specimens captured from different localities in Malakand

division with available literature.

177

vi

LIST OF FIGURES

FIGURE

NO. TITLE

PAGE

NO

Publication 3.1.

3.1.1

Distribution map of the Indian flying fox (Pteropus giganteus)

showing extension in its range towards the Palaearctic

region.Courtesy:ttp://www.iucnredlist.org/redlist/18725/0/rangemap).

47

3.1.2

Combined monthly variations in relative abundance (%) of the Indian

flying foxes roosting on Accacia arabica1, Brousentia papyrifera2,

Dalbergia sisso3, Eucalyptus globulus4, Ficus palmate5, Melia

Azedarch6, Morus alba7 M. nigra8, Olea ferruginea9, Platanus

orientalis10 and Populus nigra11 in four districts of Khyber

Pakhtunkhwa.

47

Publication 3.2.

3.2.1 Distribution map of P. giganteus, R. leschenaultii and C. sphinx. 57

3.2.2

Skull of the greater short-nosed fruit bat Cynopterus sphinx (a, b)

collected from the floor of “Kashmir Smasta” cave located in Mardan

and a closer view of the lateral (c), and ventral (d) sides the cranium

and mandible (e).

58

3.2.3 A fulvous fruit bat (Rouesttus leschenaultii) captured from Daim

teshil Dargai in Malakand district. 58

3.2.4

Dorsal (a), lateral (b) and ventral (c) view of cranium of Rousettus

leschenaultii along with the mandibles (d, e) captured from Tura

Gata tehsil Dargai in Malakand district.

59

3.2.5 The baculum of fulvus fruit bat Rousettus leschenaultii (Batlab No.

33) captured in different caves from Tura Gata in Malakand district. 59

Publication 3.3.

3.3.1 Distibution map of R. microphyllum and R. hardwickii. 75

3.3.2

A close up of dorsal, ventral, lateral side of the cranium of

Rhinopoma microphyllum and dorsal view of lower jaw a specimen

(BatLab No. 30) captured from Tura gata tehsil Dargai in Malakand

district, respectively.

76

3.3.3

Dorsal view of the baculum of greater mouse tailed bat Rhinopoma

microphyllum (Bat lab 314) captured in a cave from Tura Gata in

Malakand district.

76

3.3.4

A close up of dorsal and, ventral side of the cranium of Rhinopoma

hardwickii and dorsal view of lower jaw a specimen (BatLab No.

313) captured from Tura Gata tehsil Dargai in Malakand district,

respectively.

76

Publication 3.4.

3.4.1

Map showing the roosting places of Megaderma lyre recorded from

Pakistan and Afghanistan along with the first record from a cromite

mine at Heroshah in techsil Dargai of district Malakand in northern

89

vii

Pakistan.

3.4.2

Dorsal (a), Ventral (b) and Lateral (c) view of the skull of

Megaderma lyra and dorsal view (d) of the lower jaw of a specimen

(BatLab # 9) Captured form Heroshah in Tehsil Dargai of District

Malakand.

90

Publication 3.5.

3.5.1 Map of Malakand Division showing its constituent administrative

units. 99

3.5.2 Distribution map of R. ferrumequinum and R. lepidus. 100

3.5.3

Face (a), and a close up of the front (b) and side view (c) of the

horseshoe apparatus of Rhinolophus ferrumequinum. The Figure also

shows dorsal (d), ventral (e) and lateral side (f) of the cranium and

the dorsal view (g) of lower jaw a specimen of this species (BatLab

No. 237) captured from Loya Agra tehsil Batkhela in Malakand

district, respectively.

101

3.5.4

Photograph of a stained baculum of the greater horseshoe bat

Rhinolophus ferrumequinum (Bat lab 237), captured in a cave from

Loya Agra in Malakand district.

101

3.5.5

A close up of the face (a), and side view (b) of the horseshoe

apparatus of Rhinolophus lepidus and dorsal (c), ventral (d), lateral

(e) sides of the cranium, and dorsal view of lower jaw a specimen of

this species (BatLab No. 280) captured from Malakand University in

Malakand district, respectively.

104

3.5.6

Lateral view of the bacula of Blyth‟s horseshoe bat (bat lab 281)

Rhinolophus lepidus captured from University of Malakand in

Malakand district.

104

Publication 3.6.

3.6.1 Distribution map of H. fulvusin Pakistan. 114

3.6.2

A complete photograph (a) of Hipposideros fulvus (BatLab No. 87)

captured from Tura Gata in Malakand district, close up its face and

hairy inner margins of the ears (b) and ,noseleaf (c) . Dorsal (d),

ventral (e), lateral (f) views of the skull, and dorsal (g) and lateral (h)

view of mandible of this bat along with its baculum (i) are also

mentioned in this plate.

116

Publication 3.7.

3.7.1 Dorsal and lateral view of the skull (A, B) and lower jaw (C, D) of

Miniopterus fuliginosus captured from northwestern Pakistan. 126

3.7.2

A photographs of Myotis formosus showing its characteristic pelage

coloration (A) along with dorsal (B), Ventral (C), lateral (D) view of

the skull and dorsal view of the lower jaw (E). 126

Publication 3.8.

3.8.1

A close-up of the face (a) showing elongated ears and tragus of the

eastern barbastelle and dorsal (b), ventral (c), and lateral view (d) of

the skull and lower jaw (e).

135

viii

3.8.2

A Scotophilus heathii captured in the hand (a), its dorsal (b) ventral

(c), and lateral (d), view of the skull. The dorsal (e) and lateral (f)

view of lower jaw and its baculum (g) are also shown in this picture.

137

3.8.3

Dorsal (a), ventral (b) and lateral (c) view of the skull of Scotophilus

kuhlii. The dorsal (e) and lateral view of the lower jaw are also given

in the same plate.

139

3.8.4 A photograph of the stained baculum of Scotophilus kuhlii.

139

3.8.5

Dorsal (a), ventral (b) and lateral (c) view of the skull of Eptesicus

serotinus. The dorsal (e) and lateral view of the lower jaw are also

given in the same plate. 142

3.8.6 A photograph of the stained baculum of Eptesicus serotinus. 142

Publication 3.9.

3.9.1 Distribution map of five species of the genus Pipistrellus in Pakistan. 151

3.9.2

Dorsal (a), ventral (b) and lateral (c) view of the skull of Pipistrellus

pipistrellus. The dorsal (e) and lateral view of the lower jaw are also


3.9.3 The bacula of Common Pipistrelle Pipistrellus pipistrellus captured

from Lamin Bala in Upper Dir district 155

3.9.4

The dorsal (a), ventral (b) lateral (c) view of upper jaw, and the

lateral view (d) of the lower jaw of the skull of Pipistrellus javanicus

are also given in the same plate. 157

3.9.5

Dorsal (a) and lateral (b) view of the skull of Pipistrellus

coromandra. The dorsal (c) and lateral (d) view of the lower jaw are

also given in the same plate. 159

3.9.6

(1) Dorsal view (2) Lateral view of the baculum of Pipistrellus

coromandra captured from different localities in Malakand and Dir

districts. 159

3.9.7

Dorsal (a), ventral (b) and lateral (c) view of the skull of Pipistrellus

tenuis. The dorsal (d) and lateral (e) view of the lower jaw are also


3.9.8 Baculum of Pipistrellus tenuiscaptured from Head Koper in

Malakand Division. 162

Publication 3.10.

3.10.1 Distribution map of the lesser yellow house bat Scotoecus pallidus in

Pakistan showing it as new record from Malakand. 174

3.10.2 Dorsal (a), ventral (b) and lateral (c) view of the skull of Scotoecus 175

ix

pallidus captured from Malakand, KPK. The dorsal (d) and lateral (e)

view of the lower jaw.

1

CHAPTER 1

INTRODUCTION

The northwestern part of Pakistan that has recently been named by the provincial government as

“Khyber Pakhtunkhwa” possesses a unique physiographic diversity. Owing to extra-ordinary

physio-climatic features, the province is rich in wildlife resources. Its broad altitudinal (174 to

7690 m asl) and climatic range (temperature: -5oC to 50

oC; average annual precipitation: 1000 to

1200 mm; rainfall: 230 to 250 mm; annual average snowfall: 3 feet (at only Lowari Top)) make

it an excellent refuge for country‟s most prominent wild animal species. The province provides

refuge to five out of six wild pheasant species i.e. the western horned tragopan (Tragopan

melanocephalus), the Himalayan monal (Lophophorus impejanus), the white crested kalij

(Lophura leucomelanos hamiltonii), the cheer pheasant (Catreus wallichi) and the koklas

(Pucrasia macrolopha). It is also home to four sub-species of markhor i.e. the Kashmir markhor

(Capra falconeri cashmiriensis), the Astor markhor (C. f. falconeri), the Kabul markhor (C. f.

megaceros) and the Suleiman markhor (C. f. jerdoni). Two species of urial, the Punjab urial

(Ovis orientalis punjabiensis) and the Ladakh urial (O. v. vignei), two species of bear, i.e. the

Himalayan brown bear (Ursus arctos) and the Asiatic black bear (Selenarctos thibetanus) and

one sub-species of the Balochistan black bear (S. t. gedrosianus) are also present here. In

addition, five species of partridges i.e. the chukar partridge (Alectoris chukar), the snow

partridge (Lerwa lerwa), the see-see partridge (Ammoperdix griseogularis), the grey partridge

(Francolinus pondicerianus) and the black partridge (F. francolinus) are also found in this

province (Roberts, 1991; Roberts, 1997 and Shah, 2011). Owing to its ornithological importance,

the Plass Valley has been designated as one of the global hot spot of biodiversity (Birdlife

International, 2003).

2

In spite of the presence of a rich and diverse wildlife, little attention has been paid to explore bat

fauna of the north-western part of the country. Most of the available literature on bat fauna of

this region has been contributed by foreigners, before partition of India and Pakistan, during the

British reign. Since no comprehensive and updated field study is available, bat biologists still

rely on Ellerman and Morrison-Scott, 1951; Gaisler, 1970; Walton, 1974; Sinha, 1980;

Chakraborty, 1983; Blanford, 1988-91; Corbet and Hill, 1992; Bates and Harrison, 1997 and

Roberts, 1997 for authenticity of their findings.

Literature survey has revealed that bat fauna of the Khyber-Pakhtunkhwa consists of four

families, thirteen genera and 29 species representing more than a half of the bats of the country.

These bat families include Pteropodidae (the fulvous fruit bat Rousettus leshenaultii),

Rhinopomatidae (the greater mouse-tailed bat Rhinopoma microphyllum and the lesser mouse-

tailed bat R. hardwickii), Rhinolophidae (the greater horseshoe bat Rhinolophus ferrumequinum,

the lesser horseshoe bat R. hipposideros, the Blyth‟s horseshoe bat R. Lepidus and the big-eared

horseshoe bat R. macrotis) and Vespertilionidae (the lesser mouse-eared bat Myotis blythii, the

whiskered bat M. mystacinus, the dark whiskered bat M. muricola, the brown long-eared bat

Plecotus auritus, the grey long-eared bat P. austriacus, the Asian barbastelle Barbastella

leucomelas, the desert long-eared bat Otonyctris hemprichii, the Asiatic greater yellow house bat

Scotophilus heathii, the Botta‟s serotine Eptesicus bottae, the northern serotine E. gobiensis, the

common serotine E. serotinus, the particolored bat Vespertilio murinus, the common pipistrelle

Pipistrellus pipistrellus, the javan pipistrelle P. javanicus, the Thomas‟s pipistrelle P. paterculus,

the least pipistrelle P. tenius, the coromandel pipistrelle P. coromandra, the Leisler‟s noctule

Nyctalus leisleri, the mountain noctule N. montanus, the common noctule N. noctula, the

Hutton's tube-nosed bat Murina huttoni and the Scully's tube-nosed bat M. tubinaris) (Roberts,

3

1997; Bates and Harrison, 1997; Simmons, 2005; Mahmood-ul-Hassan et al. 2009). As for as the

status of these bats is concerned one species is Endangered, two are Vulnerable, six are Near

Threatened, fifteen are Least Concern and five were Data Deficient (Walker and Molur, 2003;

IUCN, 2008).

Distribution ranges of most mammals in Pakistan have changed over the past few decades.

However, no worthwhile study documenting these changes except Taber et al. (1967), Roberts

(1997), Beg and Khan (1984) and Mahmood-ul-Hassan et al. (2011, 2012) are available in the

country to show such changes. New mammal species are being explored throughout the world.

These discoveries are made especially in those areas which are either poorly surveyed or their

mammal fauna is a combination of two or more zoogeographical realams. The northwestern part

of Pakistan fulfills both these conditions.

It is not only a poorly surveyed, climatically diverse and habitat rich area but is also uniquely

located on the globe. It forms a buffer zone between Oriental and Palearctic regions and is also

connected to Russia and China through land connections. Keeping in mind all these facts, the

present study was designed to provide an authentic and up-to-date information on the bat fauna

of that part of the Khyber Pakhtunkhwa which comprises of the Malakand.

4

CHAPTER 2

REVIEW OF LITERATURE Mammals are the most successful creatures that have successfully exploited land, water and air

(Kalko, 1997; Ramirez-Pulido et al. 2005). Among the mammals, the Order Chiroptera exhibits a

remarkable diversity and broad geographic distribution (Simmons, 2005). With more than 1200

known extant taxa (Schipper et al. 2008) the Order Chiroptera is the main contributor to

mammalian diversity. Bats are equipped with a variety of features that make them living wonders.

Due to their global distribution coupled with their high functional as well as taxonomic diversity

they have achieved a remarkable status of bio-indicators of anthropogenic changes to reflect

habitate quality and magnitude of climatic changes across the globe (Jones et al. 2009). Many bat

species provide key ecosystem services as effective pollinators, seed dispersers and as bio

pesticides (Kalka et al. 2008; Kelm et al. 2008; Lobova et al. 2009; Winter and Von-Helverson,

2003; Williams-Guillen et al. 2008; Mahmood-ul-Hassan et al. 2010). Bats have an exceptional

ability to respond to a wide variety of environmental stressors such as urbanization, deforestation,

habitat degradation, loss and fragmentation, landscape changes due to logging, mining and oil

extraction and overhunting (Meyer et al. 2010). Bats are well woven in various food web structures

and their responses to various environmental stressors are often associated with other also (Jones et

al. 2009).

Bats, excluding birds, are the only vertebrates that have powered flight and cover large distances

each night (Fenton, 1992; Wilson and Reeder, 1993; Hutson et al. 2001). Their feeding habits are as

diverse as they themself are. As primary consumers, they feed on plant leaves, fruits, seeds, flower

petals, pollens and nector e.g. (Pteropus, Rousettus, Cynopterus spp.) while as tertiary consumers

they acquire the status of top order predators consumering frogs, mice, arthropods and even fish.

Review of Literature

5

One family Desmodontidae feeds nothing but the blood of other vertebrates (Beolens et al. 2009;

Fenton, 1992; Hill and Smith, 1985).

Most recent taxonomic revision of the Order Chiroptera based on their molecular phylogeography

and analysis of their echolocation call structures has led bat biologists to propose an entirely new

classification of bats (Jones and Teeling, 2006). They now group Pteropodidae with

Rhinolophoidae (Rhinolophidae, Hipposideridae, Craseonycteridae, Rhinopomatidae and

Megadermatidae) into the suborder Yinpterochiroptera while the remaining bat families such as

Emballonuridae, Nycteridae, Myzopodidae, Mystacinidae, Phyllostomidae, Mormoopidae,

Noctilionidae, Furipteridae, Thyropteridae, Natilidae, Molossidae, Miniopteridae and

Vespertilionidae constitute the suborder Yangochiroptera. Hutcheon and Kirch (2006) suggested

Pteropodiformes as an appropriate name for Yinpterochiroptera and Vespertilioniformes for

Yangochiroptera.

Since the time of Galileo, the bats have remained an important subject in scientific research. Owing

to their importance, they are extensively studied throughout world (e.g. Kalka et al. 2008; Blehert et

al. 2009; Cryan et al. 2010; Frick et al. 2010; Cryan et al. 2013; Johson et al. 2004; Whitaker, 2002;

Anthony and Kunz, 1977; Solick and Barclay, 2006; Boyles and Willis, 2010; Cleveland et al.

2006; Federico et al. 2008; Thomas and Cloutier, 1992; Bumrungsri et al. 2009; Bumrungsri et al.

2008; Rydell, 1992; Fujita and Tuttle, 1991; Downs and Racey, 2006; Baerwald et al. 2009; Arnett

et al. 2010). In addition to a number of science journals, a few (e.g. Acta Chiropterologica; Bat

Research News) are fully dedicated to bat research that regularly publish articals to showcase recent

advances in bat research. Likewise huge amount of literature is available on the morphology,

biology, ecology and other aspects of the bats of Indian subcontinent. However, keeping in mind


6

the scope of present study, the distribution, morphology and body measurements of only those bats

which were captured during the present study is reviewed ahead.

SPECIES ACCOUNT

The Indian Flying Fox Pteropus giganteus Brünnich 1782

The genus Pteropus Brisson, 1962 has 65 species and consists of medium to large fruit bats

(Simmons, 2005). It is distributed from Mafia and Pema Islands (off the Tanzania), Madagascar, the

Islands of the Indian Ocean, Indian subcontinent, Southeast Asia, Philippines and Australia (Bates

and Harrison, 1997). Of the 65, five species of the flying foxes are reported from the Indian

subcontinent which include the Indian flying fox P. g. giganteus (Brünnich, 1782), P. g. ariel (G.

Allen, 1908), P. g. leucocephalus Hodgson, 1835, the large flying fox P. vampyrus (Linnaeus,

1758), the Nicobar flying fox P. faunulus (Miller, 1902), the Island flying fox P. hypomelanus

(Temminck, 1853), P. h. satyrus K. Andersen, 1908 and the Blyth‟s flying fox P. melanotus

melanotus (Blyth, 1863) P. m. tytleri Dobson, 1874 (Bates and Harrison, 1997). The status and

geographical limits of this taxon are still uncertain (Bates and Harrison, 1997). In Pakistan, this

species has been reported from Rawal Lake, Saidpur and Margalla Hills in Islamabad, Sialkot,

Lahore, Changa Manga and Renala Khurd in Punjab, and from Jacobabad, Shahpur and Clifton

Railway Bridge in Karachi (Eates, 1968; Roberts, 1997; Bates and Harrison, 1997). It has recently

been reported from Peshawar and Charsadda districts (Mahmood-ul-Hassan et al., 2011). The

species is widely distributed across India, Maldives Nepal, Bangladesh and Sri Lanka (Bates and

Harrison, 1997). Body measurements of the P. giganteus have been recorded by Roberts (1997),

Bates and Harrison (1997), Aziz et al. (2007) and Molur et al. (2007).

The Greater Short-nosed Fruit Bat Cynopterus sphinx Vahl, 1797


7

The genus Cynopterus F. Cuvier, 1824 has 7 species (Simmons, 2005). It consists of those species

which possess having shorter and broader muzzle with a deep emergination between the nostrils. It

is distributed from India to Malaysia, Indonesia, Thailand and the Philippines (Koopman, 1993)

(Bates and Harrison, 1997). Of the 7, two species of the short-nosed fruit bats are reported from the

Indian subcontinent which include the short-nosed fruit bats C. sphinx (Vahl, 1797) and the lesser

dog-faced fruit bat C. brachyotis (Müller, 1838) (Bates and Harrison, 1997). It is the smallest of the

four species of fruit bats which occur in Pakistan with average forearm length of 70.2 mm (64 - 79

mm). When flying, it is easily recognized by its smaller size and more rapid wing beats. Its nostrils

are situated at the tip of slightly bifurcated fleshy projections. The upper lip is also deeply grooved

down the centre. Another distinctive feature is the presence of a narrow whitish border along the

margin of the ears. There is no tragus in ear. There is a short vestigial tail and the medial part of

interfemoral membrane is hairy, above and below (Roberts, 1997; Bates and Harrison, 1997).

Typically this is an Oriental faunal zone species and is confined to warmer sub-tropical areas where

there are large numbers of flowering and fruiting trees. This short-nosed fruit bat has been reported

from Karachi and Malir by Murray (1884) and Eates (1968). No specimen has been collected either

by the Zoological Survey of Pakistan or by the Bombay Natural History Society during its mammal

survey of Southern Sindh. According to farmers in the Malir area, a small fruit bat does occur

which attacks the „chiku‟ fruit (Achras sapota) as well as the custard apple (Annona squamosa)

hovering near the ground and it seems probable that this is Cynopterus. With the spread of banana

cultivation in recent decades up to Hyderabad, it is however, likely that this bat is followed as for

north as that city (Roberts, 1997). Colonies of up to 25 individuals have been recorded in India by

Vasishta and Badwaik (1994). It has been suggested that this species may be beneficial as an agent

in seed dispersal (feeding on ripe dates and dropping the pits some distance from the food tree)


8

(McCann, 1940), and also in pollinating flowers which produce nectar at night. It is probably not

mumerous enough in Pakistan to do any significant damage to the fruit crops.

The Fulvous Fruit Bat Rousettus leschenaultii Desmarest, 1820

The genus rousettus Gray, 1821 includes medium-sized fruit bats that are distributed from sub-

Saharan Africa, Arabia and Madagascar to the Indian subcontinent and Southeast Asia (Bates and

Harrison, 1997). Of the 10 species belonging to this genus, two are reported from the Indian

subcontinent which include the fulvous fruit bat R. leschenaultii (Desmarest, 1820), R. l.

leschenaultii (Desmarest, 1820) and the Egyptian fruit bat R. aegyptiacus (E. Geoffroy, 1810) R. a.

arabicus (Anderson and de Winton, 1902), (Bates and Harrison, 1997; Talmale and Pradhan, 2009).

Both of them are seasonally migratory and colonize Himalayan valleys in summer in the fruit

growing districts up to 1200 mm (4000 ft.) elevation (Roberts, 1997).

The fulvuos fruit bat is comparatively larger than its congener with a forearm length of 80.6 mm

(75 - 86 mm). The head is large and elongated with a dog-like muzzle. They have large eyes and

broad wings. The thumb is usually less than 31 mm. The second phalanx of the third digit is usually

less than 47 mm which in R. aegyptiacus exceed 51 mm. There is a small vestigial tail.

According to (Brosset, 1963) the males average slightly bigger than the females and have the sides

of their body washed with grey whereas the female are more yellowish brown all over. Female have

two pectorally located mammae (Bats and Harrison, 1997, Roberts, 1997). New born are pinkish

and naked ventrally while their back is pigmented brown. Fur develops and become dark brown

almost a salty colour (McCann, 1940 B).

It is a highly gregarious species and colonies vaulted roves, natural rock caves and open wells.

These roosts were located in the more wooded regions in the Himalayan foothill zone and adjacent

plains. Being partly migratory the Fulvous fruit Bat is mainly a summer visitor to Pakistan with the


9

exception of known Lahore and Malir colonies. It has been recorded near Muzaffarabad in the

Jhelum valley of Azad Kashmir, Malakand, the Vale of Peshawar, Sialkot, Lahore and Karachi

(Mirza, 1967; Walton, 1974; Roberts, 1974). The population of this bat does not seem large enough

to have a much effect on the fruit industry in such regions of Peshawar and Mardan. Z. B. Mirza

discovered a colony numbering several thousand in a rock cave at 1060 m elevation in the

Malakand. This was only a summer colony (Mirza, 1967) which corroborates their seasonally

migratory movements.

Greater Mouse tailed Bat Rhinopoma microphyllum Brünnich, 1782

The genus Rhinopoma E. Geoffroy, 1818 has four species worldwide and three of them occur in the

Indian subcontinent which include the lesser mouse-tailed bat R. hardwickii Gray, 1831, the greater

mouse-tailed bat R. microphyllum Brünnich, 1782 and the small mouse-tailed bat R. muscatellum

Thomas, 1903 (Simmons, 2005). The greater mouse-tailed bat is distributed from Mauritania,

Nigeria, Senegal, Arabia, Iran, Afghanistan, Pakistan, India, Sumatra and Cameroon to Egypt

(Simmons, 2005). The species is relatively abundant in the Indian subcontinent with one endemic

subspecies (R. m. kinneari).

Rhinopoma microphyllum this is the largest than that of the three Rhinopoma found in the Indian

subcontinent with a forearm length of 68.0 mm (59.5 - 74.6 mm). The tail is short and usually does

not exceed the length of the forearm (Roberts, 1997; Bates and Harrison, 1997). The eyes are

comparatively large and bright to tolerate bright light in its diurnal roost. Gaisler, 1970 reported that

the males averaging 2-3 mm greater in head and body length. The wings are short with a span of

210 - 285 mm (Sinha, 1980).

In Pakistan, the species has been reported from Ara (Hinton and Thomas, 1926), Sakesar, Rohtas

(Lindsay, 1927ii), Gujrat, Multan, Mailsi and near Jhelum in Punjab (Roberts, 1997). In Sindh,


10

colonies have been found in Sukkur, Gambat (Wroughton, 1916ci); Hyderabad, Karchat Hills,

Karachi (Roberts, 1977) and Lasbela (South Balochistan) (Gaisler, 1970a). The species has also

been reported from Sadikabad, Qutabpur. Z. B. Mirza found a large summer colony inhabiting a

natural rock cave in the Malakand Hills (Roberts, 1997). It is also found in Amb in Khyber

Paktunkhwa (Hill, 1977).

Lesser Mouse Tailed Bat Rhinopoma hardwickii Gray, 1831

Rhinopoma hardwickii is a small bat with a slender, long and free tail that usually exceeds the

forearm length. The muzzle bears a small triagonal nose-leaf structure at the terminal end. The large

prominent black eyes and tragus are well developed. There is a small nose-leaf on snout. A

pronounced dermal ridge also present on muzzle (Davis, 2007). The pinna is large and is crossed by

10 transverse ridges (Qumsiyeh and Jones, 1986). The feet are slender, smaller and more delicate

than in R. microphyllum. The interfemoral membrane is small and encloses less than one fourth of

the tail (Miller, 1907; Harrison, 1964). The face is glandular and the ears are connected across the

forehead (Madkour, 1961).The body fur also tends to be more rufescent brown dorsally in

specimens from Salt Range. As in R. microphyllum besides two pectoral teats there are two false

teats situated inguinally in the females. The second digit has two phalanges (Roberts, 1997). The

pelage is grey-brown above with paler hair roots; the belly is essentially grey. The interfemoral,

wing membranes, posterior back and lower abdomen are naked; the chin is nearly naked (Bates and

Harrison, 1997). According to Bates and Harrison (1997) R. hardwickii is widespread and believed

to be common in the Indian Subcontinent. Both the species R. hardwickii and R. microphyllum use

the same type of diurnal roosts.

R. hardwickii has an average forearm length of 59.2 mm (52.9 - 64.0 mm) and rarely exceeds 60 -

67 mm. According to Roberts (1997) this is much less common species than R. microphyllum in


11

Pakistan. The species has been reported from Amb in Khyber Paktunkhwa (Siddiqi, 1961). It has

also been reported from Ara (Hinton and Thomas, 1926), Sakesar, Rohtas in Salt Range and Chitti

Dil (Lindsay, 1927) in Punjab, around Karachi and Karchat Hills near Hyderabad (Roberts, 1997)

and Landi in southern Sindh (Wroughton, 1916).

The Greater False Vampire Megaderma lyra E. Geoffroy, 1810

The genus Megaderma E. Geoffroy, 1810 has two species which consists of the greater false

vampire M. lyra E. Geoffroy, 1810 and the lesser false vampire M. spasma Linnaeus, 1758

(Simmons, 2005). They are large bat without any tail and extensively developed interfemoral

membrane. The genus Megaderma consists of those species having large oval ears, fold of skin

across the crown and have an elongated bifurcated tragus (Roberts, 1997; Bats and Harrison, 1997).

Megadermatidae consists of four genera and five species, two of which occur in the Oriental Region

and by one genus and one species in Pakistan (Corbet and Hill, 1991; Koopman, 1993; Simmons,

2005). Megaderma lyra Geoffroy, 1810, differs from M. spasma by its longer forearm, broad and

short tragus, smaller postorbital process and deep prenasal notch. Because of these differences

Lekagul and Mcneely, 1977 have placed M. lyra in a separate subgenus, Lyroderma. According to

Andersen and Wroughton, 1907 the species (under the generic name Eucheira) can be divided into

two subspecies, E. l. lyra and E. l. caurina, both of which are found in and near the Indian

Peninsula, and the specimens derived from South China (characterized by larger skull and narrower

prenasal notch) belong to a different species, E. sinensis. Since the differences are very slight

between E. l. lyra and E. l. caurina, we agree with Brosset (1962) and Sinha (1970, 1977) who

recognised only the nominate subspecies M. l. lyra in India, Pakistan, Bangladesh and Sri Lanka. E.

sinensis is generally accepted as a subspecies of M. lyra (Ellermann and Morrison-Scott, 1951) and

distributed in South China, Burma, Thailand, Cambodia, Laos, and Malaysia. The area of M. lyra


12

was figured by Lekagul and Mcneely (1977), but with some inaccuracy, since the species is living

in Pakistan (Roberts, 1977), in Afghanistan (Gaisler, 1970) and Vietnam (Csorba and Topal, 1994).

The false vampire bat M. lyra Geoffroy 1810, is an Old World tropical gleaning bat. It detects its

prey both via echolocation (Schmidt et al. 2000) and based on prey generated rustling noises

(Neuweiler, 2000). M. lyra is a large bat with ugly appearance because of their big head, prominent

muzzle, huge naked ears and peculiar nose leaf. The skin of the noseleaf is pink and naked and

roughly lozenge-shaped with a narrow vertical ride running down its centre. Ears are bluntly

rounded at their tips, sparsely covered with hairs and pinkish grey colour when the animal alive.

The tragus is pinkish brown, long and slender, being divided into two lanceolate but unequal lobes.

The outer lobe is much longer up to 13 mm, and more slender than the inner lobe which is blunter

at its tip. The pelage is fine, soft and moderately long. The upper surface of the body is a uniform

mouse grey faintly washed with brown. The ventral surface is paler, with the hair tips on the throat

and belly white; the hair bases are grey. Dorsally the body fur is blue grey and consisting of long

silky hair. The belly fur is a paler, more yellowish grey. Whitish hairs extend around the posterior

ears bases and on to the wing membrane from the axillae to the groin. The upper lips tend to be

rather sparsely haired with a fleshy furrow dividing the middle of the lower lip. Female have two

pectoral mammae with two more false teats in the pubic region. Juvenile have a comparatively dark

pelage. The wings are broad due to the last or fifth digit being relatively long. There is no trace of a

tail in this species, but the inter femoral membrane is well developed, stretching from heel to heel

and being supported by long but weakly developed calcars. The hind feet are comparatively large is

in the development of the first digit which consists of only two joints whilst the remaining digits

have three joints (Roberts, 1997; Bates and Harrison, 1997).


13

In India the colonies of this species have been observed in man-made structures like temples, caves,

forts, dilapidated old buildings, underground tunnels, old cow sheds, grain godowns, cellars, open

walls and shallow soap stone mines (Brosset, 1962; Gopalakrishna and Badwaik, 1989; Khajuria,

1980). According to Lindsay (1927), the species has been reported from Murree foothills at

Lehtarar at 920 m while Roberts, 1997 recorded from Lahore in old ruined Mughal cellars at

Shalimar gardens and also from Sialkot. At Sukkur in Sindh, it has been found occupying hillside

caves (these are shallow man-made caves in limestone conglomerate) (Roberts, 1997). The species

has been observed entering the verandah of an occupied house in Karachi to devour its prey by

Eates (1968). The British Museum has one specimen, marked Balochistan and it seems likely that

this specimen comes from Lasbela. It has not definitely been recorded anywhere else in Pakistan. In

Pakistan it appears that this bat rather rare and decidedly local in distribution except in the northern

sub-montane zone where it may be more widespread than is presently known. Further collecting

will undoubtedly reveal its presence in the valley of Peshawar and possibly Mardan (Roberts,

1997).

The Greater Horseshoe Bat Rhinolophus ferrumequinum (Schreber, 1774)

The Family Rhinolophidae is characterized by a horseshoe shaped noseleaf on the muzzle which

consists of an erect posterior lancet, a lower horizontal horseshoe that surrounds the nostrils and a

perpendicular median sella. The genus Rhinolophus Lacepede, 1799 has 76 species worldwide of

which sixteen species exist in the Indian subcontinent and five have been recorded in Pakistan.

These five species include the greater horseshoe bat R. ferrumequinum Schreber, 1774, the lesser

horseshoe bat R. hipposideros Bechstein, 1800, the Blasius horseshoe bat R. blasii Peters, 1866, the

Blyth‟s horseshoe bat R. Lepidus Blyth, 1844 and the big-eared horseshoe bat R. macrotis Blyth,

1844 (Simmons, 2005; Bates and Harrison, 1997; Roberts, 1997). This Family is distributed from


14

southern England to Caucasus, Iran, Pakistan, India, China and Japan, Morocco, Algeria and

Taunisia. It is considered to be a monogeneric group (Corbet and Hill, 1992).

R. ferrumequinum is a medium sized with a forearm length averaging 58.9 mm. The nose-leaf has a

small sella and its anterior border is narrow above and widened below. When viewed from the side

the superior connecting process is bluntly rounded off. They have a narrow horseshoe which does

not cover the entire muzzle. In this species the nose-leaf is characterized by the lancet being quit

large and conspicuous (about 11 mm long) and having three cup like receptacles in its side and is

narrowly pointed. The pelage is soft, long, dense and not conspicuously woolly. Immature

specimens are greyer than the adults (Bates and Harrison, 1997). The dorsal colour varies from a

buffy grey-brown to grayish brown. The ventral colour is lighter than that of the dorsal (Albayrak,

1985). The wings are delicate, translucent membranes and rounded in outline. The ears are pale

brown, semi-translucent, broad and have no tragus but the outer margin curves round to form a

prominent anti-tragus. The muzzle of this bat is well covered with hairs. The eyes are extremely

minute. Adult specimens from Europe weigh up to 25 g (Roberts, 1997).

R. ferrumequinum is widely distributed in northern Himalayan region and extends southwards

through the mountains of Waziristan and northern Balochistan. This bat seems to be rare in

southern Balochistan because of the lesser supply of suitable insect prey and very dry climate which

is unfavourable to the family Rhinolophidae (Roberts, 1997). Specimens have been collected from

around Dir town (USNM), Abbotabad (HZM), Karakar pass (FMNH), Gilgit (type loc. of

proximus) (Bates and Harrison, 1997) and Kululai in Swat (Roberts, 1997). These larger greyer

specimens have been assigned to the subspecies R. f. proximus (Roberts, 1997). Small colonies

found in Balochistan near Kalat, Nushki and Quetta have been assigned to R. f. irani (Mirza, 1965;

Bates and Harrison, 1997).


15

Blyth’s Horseshoe Bat Rhinolophus Lepidus Blyth, 1844

This species is a new record for Pakistan. The first specimen was captured by Mrs. Nora Pendleton

from a phosphate mine near Abbotabad (Roberts 1997; Bates and Harrison, 1997). The species has

also been collected from Afghanistan (Corbet and Hill, 1992) and in the dryer parts of Rajasthan,

India (Sinha, 1980) so the status of this species is unknown in Pakistan (Roberts, 1997). IUCN

2003 declare this species to be Data Deficient. Rhinolophus lepidus shortridgei found in South

Asia differs from R. l. lepidus in having a longer hind foot (55 - 63 % of the tibia, against 45.8 -

47.5 %) and longer mandible (Sinha, 1973). Bates and Harrison (1997) collected specimens of R.

lepidus from Nepal, India and Pakistan.

Fulvous Leaf-nosed Bat Hipposideros fulvus GRAY, 1838

Hipposideridae is a family of bats commonly known as the "Old World Leaf-nosed Bats". This

large family is characterized by elaborate modifications of the nose and muzzle, forming leaf-like

projections that are thought to help focus echolocation signals emitted through the nose. It

comprises 80 species in eleven genera throughout the world. In Pakistan it is represented by three

genera and four species. It is a medium small species of hipposideros with characteristically very

large ears the tip of which are broadly rounded off. The feet are small. The noseleaf has a greatest

width of about 5 mm; its general morphology is similar to that of H. ater (Bates and Harrison,

1997). Adult weigh between 8 to 9 grams (Gopalakrishna, 1969). The baculum is small and

comparable to that of H. ater. It has a straight shaft with a simple base and tip (Bates and Harrison,

1997). It is closely similar in appearance to Hipposiderose cineraceus from which it can mainly be

distinguished by its slightly greater size and more rufescent dorsal pelage with very pale basal

portion to the hairs. The dorsal fur of this species can vary widely in colour in parts of western India

(Brosset, 1962) but in Pakistan all specimens from the Punjab have long soft fur with the hairs

http://en.wikipedia.org/wiki/Family_(biology)

http://en.wikipedia.org/wiki/Bat


16

pinkish white basally terminating in dark reddish brown or chestnut tips. Some individuals have

more yellowish white fur close to the body with the tips of the hairs grey brown or even golden

yellow in specimens from Sindh according to J. A. Murray, 1874. Their ventral fur is paler

yellowish white varing to almost pure white and in the field the rather streaked appearance of the

body fur is reminiscent of the down of young birds. It is a small bat with the tail wholly enclosed by

the inter-femoral membrane and the wings rather short and broad and delicately constructed. The

ears are large reaching 22 mm. the noseleaf consists of a naked brown skinned pad roughly square

in outline (Roberts, 1997).

This species seems well adapted to arid regions in the areas having a scattered growth of tropical

thorn scrub or dry sub-tropical scrub. It particularly favours the open burrows of Porcupines and

hyaenas for its diurnal roost as well as utilizing underground cellars, railway tunnels, and open

wells in Balochistan, “Kharezes”. They are very susceptible to predation from crows and kites if

flying abroad in daylight (Brosset, 1963). Specimens have been collected in the northern Punjab

from around Rawalpindi (Sinha, 1980) and Chaklala (Hinton and Thomas, 1926) in the salt range. It

apparently does not penetrate into the foothills in the north and is absent from most of the Indus

plain, occouring again in Southern Sindh around Sukkur (Wroughton, 1916) the Mausoleum of

Amir Khan Mono and in Gholam and Gharo, all in Thatta District (Lindsay, 1926) and Shujawal

(Siddiqi, 1961). In Southern Balochistan it has been collected fron Panjgur and Hoshab (Roberts,

1997). A specimen from Afghanistan weighed 9 g and Malayan specimens vary from 8 to 10 g in

body weight (Medway, 1969).

Hodgson’s Bat Myotis formosus (Hodgson, 1835)


17

This is geo-graphically widespread but little known bat Bates and Harrison (1997). It is apparently

common in South Korea (Wallin, 1969). Myotis formosus ranges from Afghanistan to China,

Taiwan, Korea, Japan, Philippines and Indonesia.

Asian Barbastelle Barbastella leucomelas (Cretzschmar, 1830/31)

This is rather a small and delicately built bat with a very striking body colour. The dorsal fur is long

and silky and of a blackish grey colour basally, with the extreme tips of hairs a pale golden brown

giving it a hoary appearance. The belly fur is paler grayish brown. The ears are large and

conspicuous being rather a squarish in outline and forward slanting. The tragus is half the height of

the ear and triangular in shape. The posterior margin of the ear lack any projections or notches as in

Barbastella barbastellus. There is an extensive inter femoral membrane with a rather small calcar

and inconspicuous lobe below the calcar. The dorsal surface of the hair is sparsely haired and shows

two dark lines or veins extending from the heel of the hind foot up to the base of the pelvis. There

are two incisors in the upper jaw, the inner jaw pair is being bi-fid and the outer incisors just

reaching the height of the lower cusp of the first pair. There is a minute first pre-molar inside the

tooth row which is invisible from without. Present limited evidences indicate that this bat is

associated with forests in the northern mountain regions, either Himalayan moist or dry coniferous

forest. Since this species is not gregarious in its diurnal roosts it is never very plentiful throughout

its range and the paucity of Pakistan specimens indicates that it is uncommon if not rare. Ellerman

and Morrison-Scott (1951) include Gilgit and the Punjab within its range on the basis of reports by

Blanford but there are no specimens in the British museum or Bombay Natural History museum

collections from Gilgit. However a specimen were collected at Dunga Gali in 1907 at 2350 m (7800

ft) and a second mummified specimen in the same location by the author on 2 May 1980. A third

specimen was collected in 1965 by the University of Maryland expedition from Naltar, Gilgit, in


18

spruce forests (Picea smithiana), at about 2450 m (8000 ft) elevation. Siddique does not include

this specimen in either of his checklists (1961, 1970). It was collected from Afghanistan in Paktia

Province (Meyer-Oehme, 1965) and from several localities in northern Iran (Etemad, 1969).

Elsewhere it occurs in Russian Turkestan and Chinese Xinjiang and Trans-Caucasia (Bobrinskii et

al. 1965) and southern China and north to Japan (Corbet and Hill, 1992). In India it occurs in

Darjeeling, Nepal Sikkim and the Bhutan Duars.

The head and body length was 55 mm of a single specimen from gilgit. The tail and hind foot

length were 49 mm and 8 mm, respectively. The ear length was 17 mm. The forearm length was 43

mm. A specimen collected from Dunga Gali, the head and body length was 60 mm. The tail and

hind foot were 45 mm and 6 mm, respectively. The ear length was 17 mm while that of the forearm

length was 40 mm (Roberts, 1997). The average forearm length of Arabian specimens is given as

37 - 38 mm by D. L. Harison (1964) but the Russian population has the forearm averaging from

40.6 to 44.5 mm (Ognev, 1928) and the northern Himalayan population which occurs in Pakistan is

also likely to average larger than Arabian specimens. The closely similar B. barbastellus averaging

from 6 to 10 gm in weight (Nowak, 1991).

Asiatic Greater Yellow House Bat Scotophilus heathii HORSFIELD, 1831

Scotophilus heathii is geographically distributed in Afghanistan to South China, including Hainan

Isl, south to Sri Lanka, Vietnam, Cambodia, Thailand and Burma. In Pakistan the species is

common and widespread throughout the Indus plains. It has been collected from Kohat (NWFP),

Islamabad city, Multan, Lahore and Sialkot districts (Punjab), Kashmoor, Sakkur, Jacobabad,

Mirpur Sakro, Dadu, Landi, Malir, Karachi (Sindh) (Wroughton, 1916; Lindsay, 1926; Taber et al.

1967; Walton, 1974; Roberts, 1997).


19

Walton (1974) captured twenty six specimens of S. heathii from Malir, Karachi and Mirpur Sakro.

The morphometric measurements include mean head and body length was 60 mm. The mean tail

length was 13 mm and that of the forearm length was 58 mm. Roberts (1997) collected six bat

specimens from south-west Punjab and Karachi and mentioned various morphometric

measurements of six bat specimens as the mean head and body length was 55 mm. The mean tail

length was 12 mm while that of the ear length was 16 mm.

Asiatic Lesser Yellow House Bat Scotophilus kuhlii Leach, 1821

It is uncommon in Pakistan with a very restricted distribution. The species is present only in

southern Sindh (Roberts, 1997). Geographiccaly this species is distributed in Bangladesh, Pakistan

to Taiwan, south to Sri Lanka, Burma, Cambodia, W Malaysia, Java, Bali, Nusa Tenggara

(Indonesia), southeast to Philippines and Aru Isles (Indonesia) (Mahmood-ul-Hassan et al. 2009).

The species is categorized as „Least Concern‟ (IUCN, 2008).

Walton (1974) captured S. kuhlii specimens from Mirpur Sakro and mentioned various

morphometric measurements of three bat samples. Their mean head and body length was 49 mm.

The mean tail length was 13 mm. The mean forearm length was 49 mm. The mean ear length was

17 mm. The mean weight was 19 gm.

Serotine Eptesicus serotinus (Schreber, 1774)

This species is rare in Pakistan. The only male specimen was collected by Roberts (1997) from

Dunga gali in Murree Hills. Walker and Moler (2003) declare this species to be Data Deficient,

Near Threatened (C.A.M.P. Report, 2002) and Least Concern according to IUCN 2008 Red List of

Threatened Animals.

E. s. pashtomus was described as a new subspecies by Gaisler (1970) in his account of bats

collected in Afghanistan from Jalalabad district. The zygomatic width of pashtomus being 14.5 mm


20

while Felten (1971) in describing a further collection of bats from Afghanistan also assigned E.

serotinus to the subspecies pashtomus which was collected from eastern Afghanistan close to the

border with Chitral (Felten, 1971).

Common Pipistrelle Pipistrellus pipistrellus (Schreber, 1774)

The taxonomic status of this bat species is unknown from Pakistan. The species is distributed in

British Isles, S Denmark, W Europe to the Volga and Caucasus, Morocco; Greece, Turkey, Israel

and Lebanon to Afghanistan, Kashmir, Kazakhstan, Pakistan, Burma, Sinkiang (China), perhaps

Korea, Japan and Taiwan. The Brisitsh Museum has one specimen that was collected from Kashmir

in the beginning of 19th

century. Two other specimens were collected from Gilgit by an expedition

carried out by University of Marryland in 1965 (Robers, 1997). The species has a restricted range in

the Indian subcontinent (Bates and Harrison, 1997) and seems to be common in Pakistan as there

has been no further field studies on bats in Kashmir or Gilgit (Roberts, 1997). Pipistrelles in Europe

have recently been shown to comprise two cryptic species P. pipistrellus which echolocates with

most energy around 45 kHz, and P. pygmaeus, with most energy at 55 kHz (Jones and Parijs, 1993;

Barratt et al. 1997).

Javan Pipistrelle Pipistrellus javanicus (Gray, 1838)

Pipistrellus javanicus distributed in East Afghanistan, North Pakistan, North and Central India,

South and East Tibet (China), Burma, Thailand, Vietnam, Through SE Asia to Lesser Sunda Isles

and Philippines; perhaps Australia.No literature is available on the distribution of this species in

Pakistan however a single specimen was collected from Gharial, Murree Hills (Mahmood-ul-

Hassan et al. 2009).

Coromandel Pipistrelle Pipistrellus coromandra (Gray, 1838)


21

Ten specimens of Pipistrellus coromandra has been collected from Chitral and seventeen

specimens from Saidu Sharif in Swat, the mean head and body length was 43 mm. The mean tail

length was 35 mm. The mean hind foot and ear length were 7 mm and 11 mm, respectively. The

mean forearm length was 32 mm. The Swat specimens averaged 6 gm in weight (Roberts, 1997).

These Pakistan specimens and also those from Afghanistan (Jalalabad) (Gaisler, 1970) appear to

average slightly larger than the population from central India (Brosset, 1962). The species also has

been collected from Dir, Yakh Tangai in Khyber Pakhtunkhwa and from Chakri in Punjab (Bates

and Harrison, 1997). This is a widely distributed and apparently common species in southern Asia.

Least Pipistrelle Pipistrellus tenuis (Temminck, 1840)

Pipistrellus tenuis is the smallest pipistrelle found within the subcontinent with an average forearm

length of 27.7 mm. The species is hard to differentiate from smaller individuals of P. coromandra

on the basis of forearm length. Its body weight averages about 2 g (Gopalakrishna and Karim,

1972). The species is distributed in Afghanistan to the Moluccas; S China, Laos, Vietnam, Cocos

eeling Isles and Christmas Isle (Indian Ocean). The species has been recorded from Malakand

(Roberts, 1997), Chitral (Sinha, 1980), Multan and Chaklala (Hinton and Thomas, 1926), Chakri,

Gambat, Sukkur (Siddiqui, 1961), Karachi, Malir (Walton, 1974).

Dormer’s Bat Pipistrellus dormeri (Dobson, 1875)

Pipistrellus dormeri is confined to India and Pakistan Bates and Harrison (1997). It is restricted to

the Indian Subcontinent where it is an abundant species in areas such as Rajasthan Advani (1983).

The species has been collected from Sialkot in Punjab and Shikarpur in Sindh (Sinha, 1980).

Desert Yellow Bat Scotoecus pallidus Dobson, 1876

Scotoecus pallidus is endemic to the Indian subcontinent and has a local and restricted distribution

in Pakistan. It was first described by Dobson in 1867 from a specimen collected from Mian Mir


22

(Lahore). Further collections were made from different regions of northern Sindh (Kashmore and

Mirpur in Jacobabbad, Larkana, Sukker and Dadu Districts) and Punjab (Muzaffargarh and

Sialkot). Its population status is uncertain and deserves further study (Mahmood-ul-Hassan et al.

2009).

Schreiber’s Long-fingered bat Miniopterus fuliginosus (kuhl, 1819)

It has not been collected from Pakistan up till now but Gaisler (1970) asserts that it is likely to

occur in the country as it is present in Afghanistan and Iran close to the western borders and in

India close to the eastern borders of Pakistan (Roberts, 1997). The status of this species is unknown

in Pakistan.

Statement of the Problem

With increase in human population and expansion of industrialization the distribution ranges of

almost all the mammalian species have been changed over the past few decades and new

distribution records have been documented from various parts of the world which were poorly

surveyed. The bat fauna of northwestern part of Pakistan has never been fully explored.

The core objectives of the present study include;

i. To provide a checklist of the bats of Malakand area.

ii. To re-define geospatial distribution and habitats of the various bats of this area.

iii. To describe morphology, external, craniodental and bacular measurements of bat of the

study area and compare it with similar information available in literature.

23

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38

CHAPTER 3

RESULTS

Title: BATS (CHIROPTERA: MAMMALIA) OF MALAKAND DIVISION, PAKISTAN

Publications

3.1. Distribution of Indian Flying Fox Pteropus giganteus Brünnich, 1782 in four

Districts of Khyber Pakhtunkhwa

(This manuscript has been published in the Journal of Animal and Plant Sciences

(Published Paper Attached as Annexure-I))

3.2. Distribution records of fruit bats Cynopterus sphinx and Rousettus leschenaultii

from khyber pakhtunkhwa, Pakistan

(This manuscript has been accepted for publication in Punjab University Journal of Zoology

(Acceptance Letter Attached as Annexure-II))

3.3. Morphological differentiation in two closely-related mouse-tailed bat species

(Chiroptera: Rhinopomatidae) captured from malakand division, Khyber

Pakhtunkhwa, Pakistan

(This manuscript has been submitted after revision in the Journal of Animal and Plant Sciences)

3.4. Description of the first record of the Indian False Vampire Bat (Megaderma lyra) E.

Geoffroy, 1810 (Rhinopomatidae: Chiroptera) captured from Northwestern

Pakistan

(This manuscript has been published in the Journal of Animal and Plant Sciences

(Published Paper Attached as Annexure-III))

3.5. Morphological differentiation in two closely-related horseshoe bat species

(Chiroptera: Rhinolophidae) captured from Malakand Division, Khyber


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39

(This manuscript has been submitted for publication in Pakistan Journal of Zoology)

3.6. New provincial record of the fulvous leaf-nosed bat Hipposideros fulvus Gray, 1838

from Khyber Pakhtunkhwa, Pakistan

(This manuscript has been submitted for publication in the Journal of Animal and Plant Sciences)

3.7. Two new bat species (Chiroptera: Mammalia) for Pakistan: Miniopterus fuliginosus

and Myotis formosus

(This manuscript has been published in Mammalia (Published Paper Attached as

Annexure-IV))

3.8. Diversity of some bat species (Family Vespertilionidae) from Malakand Division,

Pakistan

(This manuscript has been submitted for publication in Mammalia)

3.9. Morphological features of the bats of genus pipistrellus from Malakand division,

Khyber Pakhtunkhwa, Pakistan

(This manuscript has been submitted for publication in Mammalia)

3.10. First provincial record of desert yellow bat Scotoecus pallidus (Dobson, 1876) from


(This manuscript has been accepted for publication in Punjab University Journal of

Zoology (Acceptance Letter Attached as Annexure-V))

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40

DISTRIBUTION OF INDIAN FLYING FOX Pteropus giganteus BRÜNNICH, 1782 IN

FOUR DISTRICTS OF KHYBER PAKHTUNKHWA

M. Salim1 and M. Mahmood-ul-Hassan2

1Department of Forestry and Wildlife Management, University o f Haripur, Khyber


2Department of Zoology and Fisheries, University of Agriculture, Faisalabad

Corresponding Author’s Email: [email protected]

(This manuscript has been published in the Journal of Animal and Plant Sciences)

(Impact factor = 0.422)

Citation: Salim, M., and M. Mahmood-ul-Hassan. Distribution of Indian flying

fox pteropus giganteus Brünnich, 1782 in four Districts of Khyber Pakhtunkhwa.

The Journal of Animal & Plant Sciences, 25(3 Supp.2): 2015, Page: 446-449.

ABSTRACT

The Indian flying fox Pteropus giganteus (Brünnich, 1782) is Indomalayan in distribution.

Present study documents its range extension towards west of the Indus in Pakistan. Five colonies

of the Indian flying foxes were recorded in four districts of Khyber Pakhtunkhwa (KP) that form

eastern boundary of Palaearctic region. The bats preferred to roost on Populus nigra (100%),

Eucalyptus globulus (88.8%), Dalbergia sisso (76.0%) and Platanus orientalis (48.4%).

Population size varied from June (n = 5478) to December (n = 912).

Key words: Indo-Malayan, Indus, Khyber-Pakhtunkhwa, flying fox

INTRODUCTION

Mammals are the most successful creatures that have exploited land, water and air (Kalko, 1997;

Ramirez- Pulido et al. 2005). Among the mammals, the Order Chiroptera exhibits a remarkable

diversity and broad geographic distribution (Simmons, 2005). The Order Chiroptera is the main

contributor to mammalian diversity with more than 1200 known extant taxa (Schipper et al.

2008).The genus Pteropus Brisson, 1962 has 65 species and consists of medium to large fruit

bats (Simmons, 2005). It is distributed from Mafia and Pema Islands (off the Tanzania),

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41

Madagascar, the Islands of the Indian Ocean, Indian subcontinent, Southeast Asia, Philippines

and Australia (Bates and Harrison, 1997). Of the 65, five species of the flying foxes are reported

from the Indian subcontinent which include the Indian flying fox P. g. giganteus Brünnich, 1782,

P. g. ariel G. Allen,1908, P. g. leucocephalus Hodgson, 1835, the large flying fox P. vampyrus

Linnaeus, 1758, the Nicobar flying fox P. faunulus Miller, 1902, the Island flying fox P.

hypomelanus Temminck, 1853, P. h. satyrus K. Andersen, 1908, the Blyth‟s flying fox

P.melanotus melanotus Blyth, 1863 and P. m. tytleri Dobson, 1874 (Bates and Harrison, 1997).

The status and geographical limits of this taxon are still uncertain (Bates and Harrison, 1997).

Pteropus giganteus is included in Appendix II in IUCN SSC Action Plan (1992)-Not Threatened

and is Lower Risk-IUCN 2003 (Mickleburghet al. 1992; Walker and Molur, 2003).

In Pakistan, this species has been reported from Rawal Lake, Saidpur and Margalla Hills in

Islamabad, Sialkot, Lahore, Changa Manga and Renala Khurd in Punjab, and from Jacobabad,

Shahpur and Clifton Railway Bridge in Karachi (Eates, 1968; Roberts, 1997; Bates and Harrison,

1997). It has recently been reported from Peshawar and Charsadda districts (Mahmood-ul-

Hassan et al., 2011). The species is widely distributed across India, Maldives Nepal, Bangladesh

and Sri Lanka (Bates and Harrison, 1997). Body measurements of the P. giganteus have been

recorded by Roberts (1997), Bates and Harrison (1997), Aziz et al. (2007) and Molur et al.

(2007). This study documents occurrence of P. giganteus in four districts of Khyber-

Pakhtunkhwa (KP) formerly known as Northwestern Frontier Province of Pakistan. The province

constitutes eastern most limit of the Palearctic region and existence of P. giganteus in this region

indicates range extension of the species (Figure 3.1.1).

MATERIALS AND METHODS

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42

The present study was conducted in four districts of KP where five roosts were identified during

the exploratory phase of this study (June to December, 2008). These roosts were located at

Fishing hut (N34°38.900' E72°01.941'; 667.51m a.s.l.), Pul Chowkai (N34°38.586' E72°01.781':

682.44m, a.s.l.), southern edge of the Poji ground adjacent to Upper Swat Canal Bridge

(N34°30.599' E71°53.820': 466.95m a.s.l.), Chail Kandoa babanear Baizo Kharki Police Station

(N34°27.392' E72°00.511': 444.09m a.s.l.) and Shakur (N34°22.824' E71°44.091': 409.96m

a.s.l.). First two of these roosts were located in Dir (N35°12' E71°52') while the remaining three

were located in Malakand (N34°34' E71°57'), Mardan (N34°19' E71°65') and Charsadda districts

(N34°09' E71°49'), respectively. Climate and vegetation of the area varies from dry sub-tropical

mixed deciduous scrub-forests to temperate semi-ever green scrub forests (Roberts, 1997). The

average annual temperature ranges from -6°C to 23°C in winter and 10°C to 38°C in summer

while annual rainfall ranges from 800-1500 mm (Ali and Iqbal, 2012). Three important western

tributaries of the Indus viz. the Panjkora, the Swat and the Kabul traverse through study area.

The Panjkora passes through Dir district while the Swat and the Kabul cross Malakand and

Charsadda districts. A network of irrigation canals emerging from these rivers further intensified

agriculture in these districts and as such they have become a horticultural hub of the country

(Khan et al. 2010). Bat colonies were monitored from June through December, 2008 and

populations of P. giganteus were ascertained through direct roost counts following Kunz et al.

(1996). Counts were made either soon after sun rise or late afternoon when wind velocity was

low and cloud cover was minimal. Count was started when bats were not disturbed due to the

presence of observer. Three counts from different angles were taken to assure that all bats on the

tree were counted. A list of trees harboring bat roosts was prepared during the first surveys. The

additional tree roosts in successive months were added to preexisting list of tree roosts to find out

Results

43

the monthly variations in the number of bats on different tree roost. GPS location and elevation

was also recorded at each roost (Table 3.1.1).

RESULTS AND DISCUSSION

Five roosts of the Indian flying fox (Pteropus giganteus) were identified during the exploratory

phase of this study. Of these, one each was located in Malakand, Mardan and Charsadda districts

while the remaining two were located in Dir district.

1. Dir District. Two bat roosts were recorded in this district, one at fishing hut on the bank of the

river Swat while the other was located on the other side of the same river close to Pul Chowkai at

the junction of Dir-Swat highway.

(a) Fishing hut. The area of fishing hut was in the form of rectangle. The length and width of

which was 310m and 210m respectively while the total area covered by these bats was 65100

m2.The bats used 50 trees as roost that belonged to six species. These included, in alphabetical

order, the white mulberry Morus alba (n =4), the black mulberry M. nigra (n= 4), the Persian

lilac Melia azedarch (n = 1), Olea ferruginea (n = 1), the chenar Platanus orientalis (n = 10),

and the black poplar Populus nigra (n = 30).The total number of bats varied in each month from

June to December. It was 2358 in June, 1685 in July, 1720 in August, 946 in September and 374

in October. No bat was observed in November and December. The maximum number of bats

was recorded on the chenar Platanus orientalis (48.4 %) during this month (Table 3.1.2).

Combined monthly variations in relative abundance (%) of the Indian flying fox roosting on

different trees in four districts of Khyber Pakhtunkhwa were showing in figure 3.1.2.

(b) Pul Chowkai. All the 21 trees belonged to a single species i.e. the black poplar Populus

nigra at Pul Chowkai (Table 3.1.2). The total area of this roost was 6200 m2. No bat was

however recorded in this roost during November and December (Table 3.1.2). The total number

Results

44

of bats recorded in different months varied. It was 504 in June, 529 in July, 382 in August, 178

in September and 195 in October.

2. Malakand District

Dargai Bridge. The bats used 55 trees as roost that belonged to five species. These included, in

alphabetical order, Acacia arabica (n = 2), Brousonetia papyrifera (n = 25), Dalbergia sissoo (n

= 24), Ficus palmata (n = 1), and Melia azedarch (n = 3). The total number of bats varied in each

month from June to December. It was 838 in June, 743 in July, 846 in August, 355 in September,

829 in October, 1323 in November and 912 in December (Table 3.1.2). Dalbergia sisso (76.0 %)

was the most often used bat roost during August (Table 3.1.2).

3. Charsadda District

Shakur. The total area of this roost was 30975 m2. A total of 39 trees belonging to four species

were present at this roost. These included E. globulus, M. alba, P. Nigra and D. sisso (Table

3.1.2). No bat was however recorded in this village roost during November and December. The

total number of bats recorded in different months varied. It was 1057 in June, 514 in July, 417 in

August, 260 in September and 247 in October (Table 3.1.2).

4. Mardan District

Chail Kondov Baba. All the 32 trees belonged to a single species i.e. the blue gum Eucalyptus

globulus at Chail Kondov Baba village (Table 3.1.2). The total area of this roost was 9585 m2.

No bat was however recorded in this village roost during November and December (Table 3.1.2).

The total number of bats recorded 721 in June, 414 in July, 369 in August, 196 in September and

135 in October.

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45

Table 3.1.1. Location and elevation of the five roosts of Pteropus giganteus in Kyber-

Pakhtunkhwa.

Sr. #. Exact Location District GPS Elevation

1. Dargai Bridge Malakand N 34°30.599' E 71°53.820' 1532 ft

2. Chail Kandov Baba Mardan N 34°27.392' E 72°00.511' 1457 ft

3. Chakdara bridge Dir N 34°38.586' E 72°01.781' 2239 ft

4. Fishing hut Dir N 34°38.900' E 72°01.941' 2190 ft

5. Ghaffar Khan village Charsadda N 34°22.824' E 71°44.091' 1345 ft

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46

Table 3.1.2. Pteropus giganteus counted on different tree species in five roosting sites of

Khyber Pakhtunkhawa from June 2008 through December 2008 (1Fishing Hut,

2Pul Chowkai,

3Poji ground,

4Chail Kandoa Baba

5Ghaffar Khan Village).

Roost species No. roosts Jun Jul Aug Sep Oct Nov Dec % RA

(d) Dir district

1Morus alba 4 264 89 234 154 22 - - 10.8

1Morus nigra 4 224 140 73 27 74 - - 7.6

1Melia azedarch 1 2 3 6 1 3 - - 0.2

1Olea ferruginea 1 7 16 11 22 10 - - 0.9

1Platinus orientalis 10 1118 864 902 471 83 - - 48.4

1Populus nigra 24 743 573 494 271 182 - - 32.1

2Populus nigra 21 504 529 382 178 195 - - 100

Malakand district

3Acacia Arabica 2 40 37 55 3 100 220 35 8.3

3Brousonetia papyrifera 25 147 90 63 89 11 82 110 10.5

3Dalbergia sisso 24 626 603 714 250 617 939 713 76.0

3Ficus palmate 1 1 3 0 10 93 50 26 3.1

3Melia azedarch 3 24 10 14 3 8 32 28 2.1

Mardan district

4Euclayptus globulus 32 721 414 369 196 135 - - 100

Charsadda district

5Dalbergia sisso 1 10 16 28 17 4 - - 3.0

5Euclayptus globulus 36 977 418 363 183 263 - - 88.8

5Morus alba 1 42 58 0 40 7 - - 5.9

5Populus nigra 1 28 22 26 20 - - - 3.8

Total 191 5478 3885 3734 1935 1807 1323 912

Bats/m2 0.025 0.018 0.017 0.009 0.008 0.006 0.004

Bats/roost tree 28.7 20.3 19.5 10.1 9.5 6.9 4.8

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47

Fig. 3.1.1. Distribution map of the Indian flying fox (Pteropusgiganteus) showing extension

in its range towards the Palaearctic region.

Courtesy: http://www.iucnredlist.org/redlist/18725/0/rangemap).

Figure 3.1.2. Combined monthly variations in relative abundance (%) of the Indian flying foxes

roosting on Accacia arabica1, Brousentia papyrifera2, Dalbergia sisso3,

Eucalyptus globulus4, Ficus palmate5, Melia Azedarch6, Morus alba7 M. nigra8,

Olea ferruginea9, Platanus orientalis10 and Populus nigra11 in four districts of

Khyber Pakhtunkhwa.

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48

REFERENCES

Ali, M. and M. J. Iqbal (2012). A probabilistic approach for estimating return periods of extreme

annual rainfall in different cities of Khyber Pakhtunkhwa (KP), Pakistan.

Aziz, M. A., A. H. M. A. Reza, M. K. Hasan, P. K. Tonchanga, A. Sarker, K. M. Atiquzzaman,

S. Dutta, Makayching and K. M. Z. Rahaman. (2007). Some notes on three species of bats of

Jahangir Nagar University, Bangladesh. Zoos Print J., 26: 2729-2731.

Bates, P. J. J. and D. L. Harrison. (1997). Bats of the Indian Subcontinent. Harrison Zoological

Museum. UK. Pp 258.

Eates, K. R. (1968). An introduction to the vertebrate fauna of Sindh and Khairpur state, Written

in 1952 and published in West Pakistan. Gazetteer-Sindh Region, Government of Pakistan,

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Kalko, E. K. V. (1997). Diversity in tropical bats. In: Ulrich H (ed.) Tropical Biodiversity and

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Tropical Ecosystems. Zoologisches Forschungs institute und Museum Alexander Koenig, Bonn.

Pp: 13-43.

Khan, N., M. Israr, N. Shah, M. Arif, M. Naeem, S. Naz and A. Ali. (2010). A Comparative

Study of Model and Non-Model Fruit Growers in Rural Areas of Khyber Pakhthunkhwa,

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Kunz, T.H, D.W. Thomas, G. C. Richards, C. R. Tidemann, E. D. Pierson, P. A. Racey (1996).

Observational techniques for bats. In Measuring and Monitoring Biological Diversity: Standard

Methods for Mammals. Smithsonian Institution Press, Washington, DC. Pp: 105-114.

Mahmood-ul-Hassan, M., Faiz-ur-Rehman and M. Salim. (2011). Public perceptions about the

fruit bats in two horticulturally important districts of Pakistan. The J. Anim. Plant Sci., 21(2):

135-141.

Molur, S., P. Molur and B. Ravichandran. (2007). Electrocuted Flying Fox in Madicari,

Coorg. Bat Net Newsletter of the Chiroptera Conservation and Information Network of South

Asia, 8: 44 p.

Mickleburgh, S. P., A. M. Hutson and P.A. Racey. (1992). Old World fruit bats. An action plan

for their conservation. IUCN/SSC Chiroptera Specialist Group. IUCN, Gland, Switzerland. 1-16

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Ramirez-Pulido, J., J. Arroyo-Cabrales and A. Castro- Campillo. (2005). Estado actual y relación

nomenclatural de los mamíferos de México. Acta Zoologica Mexicana, 21: 21-82.

Roberts, T. J. (1997). The Mammals of Pakistan. Revised Ed. Oxford Univ. Press. Oxford.

Simmons, N. B. (2005). Chiroptera. In: The Rise of Placental Mammals, K. D. Rose and J. D.

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Schipper, J., J. S. Chanson, F. Chiozza, N. A. Cox, M. Hoffmann and V. Katariya. (2008). The

status of the World‟s land and marine mammals: diversity, threat, and knowledge. Science, 322:

225-230.

Walker, S. and S. Molur. (2003). Summary of the status of South Asian Chiroptera. Extracted

from C.A.M.P. 2002. Report. Zoo Outreach Organization. CBSG South Asia and Wild,

Coimbatore, India.

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DISTRIBUTION RECORDS OF FRUIT BATS CYNOPTERUS SPHINX AND

ROUSETTUS LESCHENAULTII FROM KHYBER PAKHTUNKHWA, PAKISTAN

Mohammad Salim1, Arshad Javid

2, Faiz-ur-Rahman

3 and FarmanUllah

4

1Department of Forestry and Wildlife Management, University of Haripur, Khyber

Pakhtunkhwa, Pakistan 2Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore,

Pakistan 3Department of Zoology, Shaheed Benazir Bhutto University (SBBU), Main Campus, Sheringal,

Khyber Pakhtunkhwa, Pakistan 4Department of Animal Breeding and Genetics, Lasbela University of Agriculture, Water and

Marine Sciences, Uthal, Balochistan, Pakistan

Corresponding Author‟s email: [email protected]


Zoology)

ABSTRACT

During present survey, extending from June 2010 through May 2012 the greater short-nosed fruit

bat Cynopterus sphinx (n = 1) and the fulvous fruit bat Rousettus leschenaultii (n = 22) were

captured from Malakand division in Khyber Pakhtunkhwa (KPK). The morphological and

cranial features of the captured specimens were compared with available literature. Baculum

morphometry is one of the key features in identification of bat species and was applied for

species confirmation of R. leschenaultii. R. leschenaultii has been already reported while C.

sphinx being reported for the first time from the study area. Pteropus giganteus is another new

record from the region.

Key words: Cranial measurements, C. sphinx, Morphometry, R. leschenaultii, Sindh

INTRODUCTION

Genus Cynopterus Cuvier, F., 1824 is represented by seven species (Simmons, 2005) while two

of them, the C. sphinx and C. brachyotis are reported from the Indian subcontinent (Bates and

mailto:[email protected]

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51

Harrison, 1997). C. sphinx ranges from Pakistan, India and Sri Lanka to southern China, Hong

Kong, Malaysia, Java, Lesser Sunda Island, Borneo and Sulawesi (Bates and Harrison, 1997).

The species is common in India and Sri Lanka. However, in Pakistan the species has been

reported from Malir, Karachi in Sindh province (Roberts, 1977).

The genus Rousettus Gray, 1821 includes medium-sized fruit bats that are distributed from sub-

Saharan Africa, Arabia and Madagascar to the Indian subcontinent and Southeast Asia (Bates

and Harrison, 1997). Of the 10 species belonging to this genus, two are reported from the Indian

subcontinent which include the fulvous fruit bat R. leschenaultii (Desmarest, 1820), R. l.

leschenaultii (Desmarest, 1820) and the Egyptian fruit bat R. aegyptiacus (E. Geoffroy, 1810) R.

a. arabicus (Anderson and de Winton, 1902), (Bates and Harrison, 1997; Talmale and Pradhan,

2009). Both of them are seasonally migratory and colonize Himalayan valleys in summer in the

fruit growing districts up to 1200 m (4000 ft.) elevation (Roberts, 1997). R. leschenaultii is a

highly gregarious species and colonies vaulted roves, natural rock caves and open wells. It has

been recorded near Muzaffarabad in the Jhelum valley of Azad Kashmir, Malakand, the Vale of

Peshawar, Sialkot, Lahore and Karachi (Mirza, 1967; Walton, 1974; Roberts, 1977). A colony

numbering several thousand in a rock cave at 1060 m elevation in the Malakand was discovered

by Mirza (1967). R. leschenaultii bat is comparatively larger than its congener with a forearm

length of 80.6 mm (75 - 86 mm). Distribution ranges of mammals of Pakistan have changed over

the past 50 years but there is no worthwhile study to document such changes except Taber et al.

(1967), Roberts (1977, 1997) and Beg and Khan (1984).

C. sphinx and R. leschenaultii are included in Appendix II in IUCN SSC Action Plan (1992)-Not

Threatened, Lower Risk-IUCN 2003 and is Least Concerned-CAMP 2003; CAMP 2002; IUCN

2008 (Walker and Molur, 2003; Mickleburgh et al. 1992; Mahmood-ul-Hassan et al. 2009).

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52

Present study was conducted in Malakand division, Khyber Pakhtunkhwa to record distribution

status of C. sphinx and R. leschenaultii in the study area.


Study Area: Landscape of Malakand is diverse including plain and hilly areas. It lies on the

northern side of the province, Khyber Pakhtunkhwa(KPK) province of Pakistan. Among the

crops, wheat is cultivated on larger scales. Average maximum temperature is 30℃ while average

minimum temperature is 17℃. The wild fauna includes the markhor (Capra falconeri), the

collared pika (Ochotona rufescens), the migratory hamster (Cricetulus migratorius), the stone

marten (Martes foina), the forest dormouse (Dryomys nitedula), Persian jird (Meriones persicus)

and the mouse-like hamster (Calomyscus bailwardi).The soil of Malakand is irrigated by the

Swat river. Malakand is surrounded by high mountains rich with mineral resources and vast

deposits of chromite iron, china clay and fuller earth have been found in Malakand.

DATA COLLECTION: Bats were collected over a duration of two years (2010- 2012) in

Malakand division and adjacent areas. All the mountainous caves were thoroughly searched. The

exact location of bat roost was searched and determined using a global positioning system device

(Garmin etrax H GPS). The bats were captured through mist and hand nets and each specimen

was weighed up to 0.1 g (Pesola balance 10050, Swiss made). The bats were euthanized and an

identification number was assigned to each specimen and brought to laboratory for further

studies. The external body measurements of the captured specimens were recorded using a

digital vernier caliper (0-150 mm) following Bates and Harrison (1997). The craniodental

measurements were taken following Bates et al. (2005) and Javid et al. (2014). Various bacular

measurements of the stained bacula were recorded following Lidicker and Yang (1986).


Results

53

A single specimen of Cynopterus sphinx was collected from “Kashmir Smasta” and its

morphological features were compared with Bates and Harrison (1997), Matveev (2005),

Senacha et al. (2006) and Aziz (2007). The head and body length, ear length, forearm length,

tibia length, hind foot length and tail length of Cynopterus sphinx was 77.12 mm, 19.50 mm,

65.48 mm, 26.60 mm, 17.94 mm and 7.34 mm, respectively while according to Aziz et al.

(2007), the range of body mass, head and body length, ear length, forearm length, tibia length,

hind foot length and tail length was 330.0-501.0 mm, 85.0-115.0 mm, 13.0-19.0 mm, 59.0-75.0

mm, 21.0-30.0 mm, 12.0-21.0 mm and 2.0-13.0 mm, respectively (Table 3.2.1). The range of

head and body length of the specimen recorded by Senacha et al. (2006) and Aziz (2007) was

larger than the present study. The head and body length of the captured specimen fall within the

ranges reported by Bates and Harrison (1997). The ear length, forearm length, third metacarpal

length, forth metacarpal length, fifth metacarpal, hind foot length and tail length fall within the

ranges described by Bates and Harrison (1997), Matveev (2005) and Senacha et al. (2006). The

ear length, forearm length, third metacarpal length, tibia length, hind foot length and tail length

fall within the ranges described by Aziz (2007). Srinivasulu et al. (2010) collected specimen

from South Asia with forearm length ranging from 64.0-79.0 mm, head and body 76.0-113.0

mm, hind foot 12.6-18.0 mm, tail 4.5-19.0 mm and ear 17.5-24.0 mm. The head and body length,

tail, ear, forearm, tibia and hind foot were 99.2 mm (89-109), 15.1 mm (13-17.5), 20.7 mm (19-

22), 71.2 mm (67-74.5), 27.2 mm (25-29) and 17.6 mm (16-20.5), respectively, from the Indian

state of Bengal (Das and Sinha, 1971). All the measurements except tail length of the present

study were within the range described by Das and Sinha (1971) (Table 3.2.1).

The rostrum was broad and short. The zygomatic arch was robust, anteriorly rounded off and

comparatively longer as compared with that of Rousettus. The braincase was ovoid with a weak

Results

54

sagittal crest. The postorbital process was well developed. The average condylo-canine length

was found to be 28.85 mm, maxillary toothrow length 10.86 mm, mandibular toothrow length

12.64 mm, greatest length of skull 32.20 mm, mandible length 24.75 mm, posterior palatal width

9.63 mm, zygomatic breadth 18.81 mm, breadth of braincase 14.50 mm, interorbital constriction

6.61 mm and anterior palatal width was 6.35 mm.

Measurements like greatest length of skull, condylo-basal length, mandibular toothrow length,

mandible length and interorbital constriction was slightly larger than the measurements reported

by Matveev (2005) while all these measurements were fall within the measurements reported by

Bates and Harrison (1997) from India , Bangladesh and Sri lanka. The greatest length of skull,

condylobasal length, zygomatic breadth, cranial width, interorbital width , length of maxillary

toothrow and length of mandibular toothrow was 33.1 mm (32-34), 31.9mm (30.6-32.5), 20.7

mm (19-22.3), 20.4 mm (18.8-21.6), 14.2 mm (13.3-14.5), 6.5 mm (5.8-7), 11.3 mm (10-12) and

12.4 mm (11.6-13), respectively, from the Indian state of Bengal reported by Das and Sinha

(1971). All the measurements of the present study fell within the ranges described by Das and

Sinha (1971) (Table 3.2.2).

R. leschenaultii (n=22) were captured during the present study from Tura gata, Cupni, Brah and

Daim in Malakand division. The mean body mass of the captured specimens was 86.05 ± 18.10 g

(Table 3.2.3). The head and body length was 120.09 ± 7.80 mm and the ear was 19.41 ± 0.85mm

long. Forearm and thumb were 80.23 ± 3.26 mm and 27.79 ± 1.22 mm long, respectively. The

length of 2nd

metacarpal was 36.14±1.91 mm while its 1st and 2

nd phalanges were 8.59±0.67 mm

and 8.50±0.60 mm, respectively. The length of 3rd

metacarpal was 52.59±2.48 mm and its 1st and

2nd

phalanges were 34.91±1.93 mm and 43.29±2.21mm, respectively. The length of 4th

metacarpal and its 1st and 2

nd phalanges was 51.27±3.06 mm, 27.18±1.82 mm and 28.18±1.79

Results

55

mm, respectively. The length of 5th

metacarpal was 49.23±2.74 mm while that of its 1st and 2

nd

phalanges were 25.45±1.50 mm and 25.50±1.71 mm, respectively. Average wingspan was

431.82±44.77 mm while tibia, calcar, hind foot and tail were 38.23±2.91 mm, 6.77±0.97 mm,

19.05±1.25 mm and 13.68±2.17 mm, respectively.

Forearm length of the specimens captured from Lahore and Malakand averaged almost similar as

reported by (Roberts, 1997), but their head and body length was larger than the specimens

captured during the present study. Specimens of R. leschenaultii collected by Bates and Harrison

(1997) from Pakistan and India had similar hind foot, forearm and thumb length. Their 2nd

phalanx on 3rd

metacarpal also had the same length but their mean head and body length was

large, tail was slightly larger and ear had almost the same length as compared with the

specimens collected during present study (Table 3.2.3). Specimens collected from SW-China had

a slightly smaller head and body length, hind foot length and wingspan and their body mass and

forearm length were smaller than our collected specimens. Their ear was, however, almost

similar in length to the present collection (Aeshita et al. 2006) (Table 3.2.3). Matveev (2005)

collected specimens of R. leschenaultii from Combodian specimens had larger body mass, tail,

hind foot length, forearm length and tail. However their tibia was slightly smaller and ear was

almost of the same length as recorded during present study (Table 3.2.3).

The dental formula of R. leschenaultii was (2132/2133=34). The greatest skull length averaged

36.97 ± 1.11 mmwhile mean breadth of the braincase and zygomatic breadth was 15.33 ± 0.0.42

mm and 21.65 ± 0.93 mm, respectively. The inter-orbital constriction was 7.60 ± 0.49 mm. The

condylo-canine and condylo-basal lengths were 33.98 ± 1.16mm and 35.41 ± 0.93 mm,

respectively. The maxillary and mandibular toothrow lengths averaged 14.08 ± 0.44 mm and

15.51 ± 0.47 mm, respectively while the mandible length averaged 28.95 ± 0.90 mm long. The

Results

56

mean anterior and posterior palatal widths of the skull were 7.37 ± 0.65mm and 11.09 ± 0.44

mm, respectively (Table 3.2.4). Cranial measurements made by Roberts (1997), Bates and

Harrison (1997) and Matveev (2005) were in line with the present study (Table 3.2.4).

Mean total baculum length of the eight specimens was 2.13 ± 0.50 mm. The width of proximal

and distal extreme of the baculum was 0.73 ± 0.35 mm and 0.64 ± 0.30 mm, respectively. The

mid width of the baculum was 0.38 ± 0.32 mm. The bacula were 0.56 ± 0.35 mm high (Table

3.2.5).

According to Shahbaz et al. (2014) total length of the baculum, length of shaft, width of

proximal branch and width of distal branch was 3.075 mm, 1.275 mm, 0.925 mm and 0.800 mm,

respectively. According to Agrawal and Sinha (1973), the baculum was dumbbell-shaped, its

proximal end was ovoid and larger than the distal. The baculum of the specimen from the Sri

Lanka was small and peg-shaped. Similarly, the baculum of Rousettus leschenaultii captured

from Tura Gata in Malakand district was exactly the same as that of the baculum described by

Agrawal and Sinha (1973).

Indian flying fox Pteropus giganteus was also recorded during present survey. The species is

unmistakable as it is the largest bat of the Indian sub-continent (Roberts, 1997).

Results

57

Fig. 3.2.1. Distribution map of P. giganteus, R. leschenaultii and C. sphinx.

Results

58

Fig. 3.2.2. Skull of the greater short-nosed fruit bat Cynopterus sphinx (a, b) collected from

the floor of “Kashmir Smasta” cave located in Mardan and a closer view of the

lateral (c), and ventral (d) sides the cranium and mandible (e).

Fig. 3.2.3. A fulvous fruit bat (Rouesttus leschenaultii) captured from Daim teshil Dargai in

Malakand district.

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59

Fig. 3.2.4. Dorsal (a), lateral (b) and ventral (c) view of cranium of Rousettus leschenaultii

along with the mandibles (d, e) captured from Tura Gata tehsil Dargai in

Malakand district.

Fig. 3.2.5. The baculum of fulvus fruit bat Rousettus leschenaultii (Batlab No. 33) captured

in different caves from Tura Gata in Malakand district.

Results

60

Table 3.2.1. Comparison of external body measurements (mm) of Cynopterus sphinx (n=1)

captured during present study with Aziz et al. (2007), Senacha et al. (2006),

Matveev (2005) and Bates and Harrison (1997).

Body

Parameters

Mean (Range) (Range) Male (n=13) Female (n=8)

Bates and

Harrison, 1997

Matveev,

2005

Senacha et

al. 2006

Aziz et

al. 2007

Das and Sinha (1971) Present

Study

BM - 35.4-49.8 - 330.0-

501.0 - - -

HB 98.8 (76.0-113.0) - 98-108 85.0-

115.0

99.2 (89-109) 99.1 (91-109) 77.12

E 20.6 (17.5-24.0) 18.1-22.2 19-23 13.0-19.0 20.7 (19-22) 20.9 (19-23) 19.50

FA 70.2 (64.0-79.0) 65.7-70.0 68-75 59.0-75.0 71.2 (67-74.5) 72.5 (67.5-76) 65.48

WS 380.4(309.0-436.0) - 340-378 - - - -

2mt - - - - - - 29.54

1ph2mt - - - - - - 7.06

2ph2mt - - - - - - 6.45

3mt 47.0 (43.2-53.4) - - 39.0-51.0 - - 43.30

1ph3mt - - - - - - 29.28

2ph3mt - - - 34.0-43.0 32.62

4mt 44.4 (40.7-51.1) - - - - - 41.21

1st Ph. 4th met - - - - - - 23.09

2nd Ph. 4th met - - - - - - 21.92

5mt 45.4 (41.1-52.1) - - - 41.19

1ph5mt - - - - - - 21.22

2ph5mt - - - - - - 20.24

TIB - 25.0-28.3 32-35 21.0-30.0 27.2 (25-29) 28 (24.5-30.5) 26.60

HF 15.6 (12.6-18.0) 12.2-15.6 14-17 12.0-21.0 17.6 (16-20.5) 17 (14.5-18.5) 17.94

T 10.9 (4.5-19.0) 6.1-12.7 15-18 2.0-13.0 15.1 (13-17.5) 15.1 (14- 19) 7.34

n - The number of specimens; BM - Body mass; HB - Head and body; E - Ear; FA - Forearm;

2mt - 2nd metacarpal; 1ph2mt - 1st Phalanx on 2nd metacarpal; 2ph2mt - 2nd Phalanx on 2nd

metacarpal; 3mt - 3rd metacarpal; 1ph3mt - 1st Phalanx on 3rd metacarpal; 2ph3mt - 2nd

Phalanx on 3rd metacarpal; 4mt - 4th metacarpal; 1ph4mt - 1st Phalanx on 4th metacarpal;

2ph4mt - 2nd Phalanx on 4th metacarpal; 5mt - 5th metacarpal; 1ph5mt - 1st phalanx on 5th

metacarpal; 2ph5mt - 2nd phalanx on 5th metacarpal; WS - Wing span; TIB - Tibia; HF - Hind

foot; T- Tail.

Results

61

Table 3.2.2. Comparison of cranial measurements (mm) of Cynopterus sphinx (n=1) captured

during present study with Bates and Harrison (1997) and Matveev (2005).

Cranial Parameters Bates and

Harrison,

1997 (Range)

Matveev,

2005

Das and Sinha (1971)

Present

Study

Male (n=13) Female (n=8)

Greatest length of skull 30.2-34.9 31.74 33.1 (32-34) 33.1 (31.7-34.5) 32.20

Condylo-canine length - 29.52 - - 28.85

Condylo-basal length 28.4-33.3 29.66-30.12 31.9 (30.6-32.5) 31.9 (30.8-33.3) 30.38

Maxillary toothrow length 10.2-12.2 11.17 11.3 (10-12) 10.8 (10.5-11) 10.86

Mandibular toothrow length 10.3-13.5 12.26 12.4 (11.6-13) 12.2 (11.8-12.6) 12.64

Mandible length 22.7-27.5 - - - 24.75

Zygomatic breadth 18.8-23.1 - 20.7 (19-22.3) 20.4 (18.8-21.6) 18.81

Breadth of braincase 11.1-14.8 - 14.2 (13.3-14.5) 14.2 (13.2-15) 14.50

Anterior palatal width - 7.10 - - 6.35

Posterior palatal width - 9.43 - - 9.63

Interorbital constriction 5.4-7.7 - 6.5 (5.8-7) 6.5 (6-7) 6.61

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Table 3.2.3. Comparison of external body measurements (mm) of Rousettus leschenaultii

(n=22) captured during present study with Bates and Harrison (1997), Roberts

(1997), Matveev, (2005) and Aeshita et al. (2006). Body

Parameters

Mean±SD

Range Bates and Harrison, 1997 Roberts, 1997 Matveev, 2005 Aeshita et al. 2006 Present Study (n=22)

BM - - - 43.00±8.00 44.30±5.50 86.05±18.10

Range - - 105.0-107.0 - - 60.00-137.00

HB 125.9±8.5 131 118.0±10.0 123.0±6.9 120.09±7.80

Range 111.0-147.0 120-145 - - - 111.00-134.00

E 20.8±1.5 21 - 18.0±1.0 18.0±1.4 19.41±0.85

Range 17.5-24.0 19-23 17.4-19.4 - - 18.00-21.00

FA 80.6±2.9 79 - 71.0±3.0 72.0±3.0 80.23±3.26

Range 75.0-86.0 - 82.2-86.5 - - 75.00-86.00

THC 27.3±1.4 30 - - - 27.79±1.22

Range 24.4-31.1 - - - - 25.00-30.00

2mt - - - - - 36.14±1.91

Range - - - - - 33.00-40.00

1ph2mt - - - - - 8.59±0.67

Range - - - - - 8.00-10.00

2ph2mt - - - - - 8.50±0.60

Range - - - - - 8.00-10.00

3mt - - - - - 52.59±2.48

Range - - - - - 48.00-57.00

1ph3mt - - - - - 34.91±1.93

Range - - - - - 31.00-39.00

2nd Ph. 3rdmt 42.6±1.6 - - - - 43.29±2.21

Range 39.6-46.2 - - - - 40.00-46.00

4mt - - - - - 51.27±3.06

Range - - - - - 45.00-56.00

1ph4mt - - - - - 27.18±1.82

Range - - - - - 23.00-30.00

2ph4mt - - - - - 28.18±1.79

Range - - - - - 25.00-31.00

5mt - - - - - 49.23±2.74

Range - - - - - 45.00-54.00

1ph5mt - - - - - 25.45±1.50

Range - - - - - 22.00-28.00

2ph5mt - - - - - 25.50±1.71

Range - - - - - 22.00-28.00

TIB - - - - - 38.23±2.91

Range - - 36.8-39.2 - - 33.00-43.00

HF 18.7±1.7 22 - 17.0±2.4 16.0±1.3 19.05±1.25

Range 15.0-22.0 - 19.5-20.9 - - 16.00-21.00

T 15.6±2.7 14 - - - 13.68±2.17

Range 8.0-21.0 10-18 17.0-17.3 - - 10.00-17.00

WS - - - 428.0±30.0 447.0±23.0 431.82±44.77

Range - - - - - 370.00-534.00

BM - Body mass; HB - Head and body; E - Ear; FA - Forearm; THC- Thumb with claw; 2mt -

2nd metacarpal; 1ph2mt - 1st Phalanx on 2nd metacarpal; 2ph2mt - 2nd Phalanx on 2nd

metacarpal; 3mt - 3rd metacarpal; 1ph3mt - 1st Phalanx on 3rd metacarpal; 2ph3mt - 2nd

Phalanx on 3rd metacarpal; 4mt - 4th metacarpal; 1ph4mt - 1st Phalanx on 4th metacarpal;

2ph4mt - 2nd Phalanx on 4th metacarpal; 5mt - 5th metacarpal; 1ph5mt - 1st phalanx on 5th

metacarpal; 2ph5mt - 2nd phalanx on 5th metacarpal; WS - Wing span; TIB - Tibia; HF - Hind

foot; T- Tail.

Results

63

Table 3.2.4. Comparison of cranial measurements (mm) of Rousettus leschenaultii captured

during present study with Bates and Harrison (1997) and Matveev (2005).

Body Parameters

Mean±SD

Bates and

Harrison,

1997

Matveev,

2005 Present Study

Condylo-basal length 35.8±1.1 38.51 35.41±0.93

Range 35.5-37.7 - 33.70-36.78

Condylo-canine length - 36.81 33.98±1.16

Range - - 32.05-36.75

Maxillary toothrow length 14.2±0.5 14.78 14.08±0.44

Range 13.5-15.2 - 13.50-14.90

Mandibular toothrow 15.7±0.5 16.17 15.51±0.47

Range 14.8-16.7 - 14.80-16.30

Greatest length of skull 37.3±1.1 40.13 36.97±1.11

Range 34.9-39.4 - 35.45-38.87

Mandible length 29.4±0.9 - 28.95±0.90

Range 27.6-31.1 - 27.70-30.50

Zygomatic breadth 22.5±0.9 - 21.65±0.93

Range 20.2-24.0 - 20.33-23.58

Breadth of braincase 15.3±0.4 - 15.33±0.42

Range 14.4-16.0 - 14.58-16.25

Anterior palatal width - 8.39 7.37±0.65

Range - - 6.45-9.50

Posterior palatal width - 11.60 11.09±0.44

Range - - 10.38-12.00

Interorbital constriction 7.6±0.5 - 7.60±0.49

Range 6.9-8.8 - 6.92-8.75

Table 3.2.5. Mean bacular measurements (mm) of Rousettus leschenaultii captured from Tura

Gata in Malakand district.

Bacular Parameters Mean± SD (n=8) Range

Total baculum length 2.13±0.50 0.95-2.63

Width of proximal extreme 0.73±0.35 0.02-1.23

Width of middle extreme 0.38±0.32 0.00-0.73

Width of distal extreme 0.64±0.30 0.02-0.98

Results

64

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MORPHOLOGICAL DIFFERENTIATION IN TWO CLOSELY-RELATED MOUSE-

TAILED BAT SPECIES (CHIROPTERA: RHINOPOMATIDAE) CAPTURED FROM

MALAKAND DIVISION, KHYBER PAKHTUNKHWA, PAKISTAN

Mohammad Salim, Arshad Javid1, Muhammad Mahmood-ul-Hassan

2, Faiz-ur-Rahman

3,

Zulfiqar Ali4

Department of Forestry and Wildlife Management, University of Haripur, Khyber Pakhtunkhwa,

Pakistan 1Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore,

Pakistan 2Department of Zoology and Fisheries, University of Agriculture, Faisalabad

3Department of Zoology, Shaheed Benazir Bhutto University (SBBU), Main Campus, Sheringal,

Khyber Pakhtunkhwa, Pakistan 4Department of Zoology, University of the Punjab, Lahore

Corresponding Author’s email: [email protected]

(This manuscript has been submitted after revision in the Journal of Animal and Plant

Sciences)

ABSTRACT

Morphological differences aid in limiting intra-species variations. Present investigation was

carried out to understand morphological differences in two closely related congeners, the greater

mouse-tailed bat Rhinopoma microphyllum (Brünnich, 1782) and the lesser mouse tailed bat

Rhinopoma hardwickii (Gray, 1831) . Variations in external body, cranial and bacular were

recorded and compared. During present survey, specimens of R. microphyllum (n = 58) and R.

hardwickii (n = 25) were roosting at two different caves (N34º 26.783′ E71º 49.070′ and N34º

26.818′ E71º 48.973′) in Malakand division, Khyber Pakhtunkhwa (KPK). Out of these, 3

specimens of R. microphyllum and 5 specimens of R. hardwickii were captured. R. hardwickii

from KPK was recorded only from Amb prior to the present investigation indicating range

extension of the species.

Key words: Cranial measurements; baculum size; R. microphyllum; R. hardwickii; Malakand.


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68

INTRODUCTION

The genus Rhinopoma E. Geoffroy, 1818 is globally represented by four species and three of

them, the lesser mouse-tailed bat R. hardwickii Gray, 1831, the greater mouse-tailed bat R.

microphyllum Brünnich, 1782 and the small mouse-tailed bat R. muscatellum Thomas, 1903 are

reported in the Indian subcontinent (Simmons, 2005). Both these species have a small dermal

ridge on their muzzle and are distinguishable on the basis of forearm length relative to their tail

length. Forearm in R. microphylum is longer than R. hardwickii but tail in R. microphyllum is

generally smaller than the forearm as compared to R. hardwickii which have a longer tail than

their forearm. The greater mouse-tailed bat is distributed from Mauritania, Nigeria, Senegal,

Arabia, Iran, Afghanistan, Pakistan, India, Sumatra and Cameroon to Egypt (Simmons, 2005).

The species is relatively abundant in the Indian subcontinent with one endemic subspecies (R. m.

kinneari). In Pakistan, the species has been reported in Punjab Province from Ara (district

Chakwal) (Hinton and Thomas, 1926), Sakesar, Rohtas (Lindsay, 1927), Gujrat, Multan, Mailsi,

Sadiqabad, Qutabpur and near Jhelum in Punjab (Roberts, 1997). In Sindh Province, colonies

have been found in Sukkur, Gambat (district Khairpur) (Wroughton, 1916); Hyderabad, Karchat

Hills (district Jamshoro) and Karachi (Roberts, 1997). The species from Balochistan Province

has been reported from Lasbela i.e. South Balochistan (Gaisler, 1970). In Khyber Paktunkhwa

Province, the known localities of species are natural rock caves in the Malakand Hills (Roberts,

1997) and Amb (district Mansehra) (Hill, 1977; Roberts, 1997).

Rhinopoma microphyllum is the largest than that of the three Rhinopoma found in the

Indian subcontinent with forearm length of 68.0 mm (59.5 - 74.6 mm). The tail is short and

usually does not exceed the length of the forearm (Roberts, 1997; Bates and Harrison, 1997).

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69

According to Bates and Harrison (1997) R. hardwickii is widespread and believed to be

common in the Indian Subcontinent. Both the species R. hardwickii and R. microphyllum use the

same type of diurnal roosts. Benda et al. (2004; 2006) reported the external body and cranial

measurements of R. hardwickii from Eastern Mediterranean region, Southwestern Arabia,

Afghanistan and India. Both the species were considered to be “Least Concerned” (South Asian

Chiroptera C.A.M.P. Report, 2002; Walker and Molur, 2003; IUCN, 2008).

Present study was planned to explore diversity of bats belonging to the genus Rhinopoma

from Malakand division and to record their morphological features that help in species

identification.


Study Area: The present study was conducted in that part of the country which is characterized

as sub-tropical dry mixed deciduous scrub forest and dry subtropical temperate semi-evergreen

scrub forest (Roberts, 1997). The area is administratively designated as Malakand Division and

is located at 34˚20ˊ and 35˚ 20ˊ North latitudes and 71˚-15ˊ and 72 ˚30′ East longitudes between

the Himalayan and Hindu Kush foothills. It covers a broad altitudinal range. The climatic

conditions are diverse and vary with altitude. Various climatic zones found in the study area, in

order of increasing altitude include; a) semi-arid humid-temperate zone (450-600m), b) warm

temperate zone (600-1100m), c) temperate zone (1100-1500m), d) cool temperate zone (1500-

1900 m), e) cold temperate zone (1900-3200m), f) alpine pastures (2300-4700m), and e) snow

and ice zone (4700-7690m). The high mountainous region occurs in north and forms southern

watershed of the valley thereby draining into the Chitral river whereas the western low

mountainous region spreads from the east of Swat in the north-south direction and covers a large

part of Khyber Pakhtunkhwa. The Swat river traverses the Malakand Division and serves as a

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70

natural boundary between Malakand and Bajaur. Further up in the north, The Swat river also

makes boundary with Dir district.

The Malakand Division comprises of five districts and two Federally Administered Tribal

Agencies which include Buner, Shangla, Swat, Dir and Malakand districts, and Bajaur and

Mohmand Agencies (Fig. 3.3.1).

Sampling Strategy: Bats were collected over a duration of two years (2010- 2012) in Malakand

Division from a variety of habitats such as croplands, plantations, mountainous caves, old

buildings, abandoned wells, ruins, houses, tree groves, crevices, old bridges, ponds and canals.

Local people were also interviewed regarding the exact location of bat roost and determined

using a global positioning system device (Garmin etrax H GPS). Mist nets of 12 m (n = 1), 9 m

(n =2) and 6 m (n = 3) size were erected either in “L” or “V” shape at strategic positions on a

pair of 3 m long bamboo poles in such a way that the last shelf of each net remained one foot

above the ground. All the nets were opened simultaneously at sunset and were checked

continuously to disentangle any captured bat. The number of euthanized bats was intentionally

kept low to avoid unnecessary killing. Field number, sex, age, exact locality and district of

capture of each bat were noted on the plastic bottle containing absolute alcohol. Each specimen

was weighed up to 0.1 g (Pesola balance 10050, Swiss made) and brought to the laboratory for

further studies. Body measurements were taken following Bates and Harrison (1997) using a

scale and digital Vernier Caliper (0-150mm).

Cranial Measurements: Eye balls, tongue, brain tissue and excessive flesh were removed from

skulls using forceps and cotton. Skulls thus cleaned were kept overnight in a dilute solution (0.2

% of Potassium Hydroxide (KOH)), absolute alcohol and acetone, respectively. Each of the dry

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71

skulls was stored in a properly labeled vial padded with cotton. The craniodental measurements

were taken following Bates et al. (2005) and Javid (2011).

Bacular Measurements: Penis of the male bats was cut down as close to the surface of the body

as possible so that the baculum is not damaged. The cut penis was placed in a test tube half filled

with cold water and boiled for two minutes. The boiled penis was then transferred to a plastic

tube containing 5% KOH and a pinch of alizarin red powder. After 24 hours, the stained bacula

were dissected out of the tissue under a dissecting microscope with fine forceps and stored in

glycerin in a labeled test tube (Bates et al. 2005). Once a stained baclum is obtained, various

bacular measurements were recorded following Lidicker and Yang (1986) under a microscope at

40X magnification using a stage and an ocular micrometer.


During the present study, R. microphyllum (n = 3) and R. hardwickii (n = 5) were captured from

Tura Gata tehsil Dargai in Malakand Division and their external body, cranial and bacular

features were compared with Rahman et al. (2015), Javid et al. (2012), Benda et al. (2009), Davis

(2007), Bates and Harrison (1997), Roberts (1997), Schlitter and Qumsiyeh (1996) and

Qumsiyeh and Jones (1986).

The face, ears and connecting membrane on the forehead and chin of R. microphyllum was naked

as described by Bates and Harrison (1997) and Roberts (1997). Ears were large and prominent

while tragus was bluntly sickle shaped (Roberts, 1997). Muzzle had a small dermal ridge and

eyes were large and bright. Pelage was short and fine. It was grey brown on the dorsal surface

and paler below. The lower back and the posterior lower abdomen were naked. All these features

were the same as described by Roberts (1997) and Bates and Harrison (1997).

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72

Average body mass, forearm length, length of 1st and 2

nd phalanges on 3

rd metacarpal, 2

nd

phalanx on 4th

metacarpal, 2nd

phalanx on 5th

metacarpal, tibia length and hind foot length

recorded by Rahman et al. (2015) were within the ranges of measurements recorded during

present study (Table 3.3.1). The specimens of R. microphyllum captured during present study

were larger than their congeners with a forearm length comparable to Benda et al. (2009), Davis,

(2007), Schlitter and Qumsiyeh (1996) and Roberts (1997). The tail was found to be shorter than

the measurements reported by Rahman et al. (2015), Benda et al. (2009), Bates and Harrison,

(1997), Roberts (1997) and Schlitter and Qumsiyeh (1996). This was exactly the same as

described by Bates and Harrison, (1997) and Roberts (1997). - The range of the wingspan was

255.00 - 275.00 mm which was exactly the same reported by Sinha (1980). The average hind

foot length was also exactly the same as reported by Rahman et al. (2015), Bates and Harrison,

(1997) and Roberts (1997) (Table 3.3.1). Similarly, average length of 2nd

metacarpal, length of

3rd

metacarpal, length of 4th

metacarpal and length of 5th

metacarpal recorded during present

study were little smaller than reported by Rahman et al. (2015) . Likewise, average length of 1st

and 2nd

phalanx on 2nd

metacarpal, 3rd

metacarpal, 4th

metacarpal and 5th

metacarpal was almost

similar to that of Rahman et al. (2015), respectively (Table 3.3.1).

The rostrum was relatively small. The sagittal crest was prominent, rises steeply over the

frontals and was then sharply reflected backwards with an almost straight superior border. The

supraorbital ridges were well developed. The general morphology of the mandible was similar to

that of R. hardwickii but the coronoid processes more robust. These features are in line with the

findings of Bates and Harrison (1997).The average condylo-canine length, maxillary toothrow

length, mandibular toothrow length, greatest length of skull, mandible length, posterior palatal

width, zygomatic breadth, breadth of braincase, postorbital constriction and anterior palatal

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73

width of two R. microphyllum captured during the present study were similar to that of Rahman

et al. (2015), Benda et al. (2009), Bates and Harrison (1997) except Schlitter and Qumsiyeh

(1996) which was smaller than the Malakand population (Table. 3.3.2). Benda et al. (2006)

reported specimens from Afghanistan and India with greatest skull length and condylocanine

length slightly larger than the Malakand population.

R. hardwickii was a small bat with a tail usually exceeding the forearm length. Face was

glandular and ears were connected across the forehead (Madkour, 1961). Large pinnae possess

10 transverse ridges (Qumsiyeh and Jones, 1986) and tragus was well developed. Eyes were

black, large and prominent. A pronounced dermal ridge on the muzzle and a small nose-leaf on

snout was also present (Davis, 2007). Inter-femoral membrane was enclosed less than one fourth

of the tail (Miller, 1907; Harrison, 1964). The second digit possesses two phalanges (Roberts,

1997). The dorsal pelage was grey-brown but the belly was essentially grey. The inter-femoral

and wing membranes, posterior back and lower abdomen was naked while the chin was nearly

naked (Bates and Harrison, 1997). All these features were the same as described by Bates and

Harrison (1997) and Roberts (1997). The average body mass, head and body length, ear length,

forearm length, wingspan, tibia length, hind foot length and tail length of the five R. hardwickii

was 10.60 ± 2.86 g, 64.67 ± 3.00 mm, 19.09 ± 1.32 mm, 59.90 ± 1.21 mm, 307.40 ± 23.08 mm,

29.22 ± 0.82 mm, 14.72 ± 0.36 mm and 66.57 ± 2.15 mm, respectively. According to Robert

(1997) the head and body length, ear length, forearm length, hind foot length and tail length was

62 mm, 18 mm, 60 mm, 11.5 mm and 67 mm, respectively. All these measurements were smaller

than the present study except forearm and tail length. Most of the metacarpal of the Malakand

Division specimens were larger than reported by Javid et al. (2012) however phalanx length

almost similar to the present study (Table 3.3.3). Bates and Harrison (1997) collected R.

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74

harrdwickii from India and Pakistan. Their average head and body, tail and ear lengths were

slightly greater than the measurements obtained during present study. Benda et al. 2009 reported

the external body of the specimens collected from Yemen. The average head and body length,

and forearm length was smaller than Malakand population. Benda et al. (2004) reported the

external body measurements of R. hardwickii collected from Libya with mean head and body

length, tail length and forearm length was 64.64 mm ± 1.277 (SD), 72.69 mm ± 3.591 (SD) and

60.52 mm ± 1.475 (SD)., respectively. The head and body length was almost similar to the

present study while forearm length and tail length was larger than the Malakand population.

Benda et al. (2009) reported the body measurements of R. hardwickii collected from Afghanistan

and India with average forearm length 59.20 mm ± 2.063 (SD) which is slightly small than the

present study (Table 3.3.3).

All the cranial measurements reported by Javid et al. (2012) were slightly smaller from

the present study except posterior palatal width, zygomatic breadth, postorbital constriction and

anterior palatal width (Table 3.3.4). The average condylo-canine length was almost similar to

that of reported by Javid et al. (2012), Benda et al. (2009), Bates and Harrison (1997) and

Qumsiyeh and Jones (1986). Similarly the maxillary toothrow length, postorbital constriction

and anterior palatal width of four R. hardwickii captured during the present study was almost

similar to that of reported by Javid et al. (2012), Benda et al. (2009), Bates and Harrison (1997)

and Qumsiyeh and Jones (1986) (Table.3.3.4). The posterior palatal width was greater than the

specimens reported by Javid et al. (2012). The zygomatic breadth was smaller reported by

Qumsiyeh and Jones (1986) than that of present study, Javid et al. (2012), Benda et al. (2009)

and Bates and Harrison (1997) (Table.3.3.4).

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75

According to Bates and Harrison (1997) the baculum was very small. It has a bifid base, a

simple tip and a deep groove on the ventral surface. All these features were exactly the same as

that of the present study. Average total length of baculum (n = 1) of R. microphyllum captured

during present study was 1.65 mm. The proximal branch length, proximal branch width, shaft

length, baculum height, distal branch length and distal branch width was 0.40 mm, 0.55 mm,

1.25 mm, 0.60 mm, 0.01 mm and 0.25 mm, respectively. The total baculum length of R.

hardwickii was 1.1 mm reported by Javid et al. (2012) which was smaller than the present study.

Similarly shaft length was also smaller than the Malakand population (Table 3.3.5).

Fig. 3.3.1. Distribution map of R. microphyllum and R. hardwickii.

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76

Figure 3.3.2 A close up of dorsal, ventral, lateral side of the cranium of Rhinopoma microphyllum

and dorsal view of lower jaw a specimen (BatLab No. 30) captured from Tura gata

tehsil Dargai in Malakand district, respectively.

Figure 3.3.3 Dorsal view of the baculum of greater mouse tailed bat Rhinopoma microphyllum

(Bat lab 314) captured in a cave from Tura Gata in Malakand district.

Figure 3.3.4 A close up of dorsal and, ventral side of the cranium of Rhinopoma hardwickii and

dorsal view of lower jaw a specimen (BatLab No. 313) captured from Tura Gata

tehsil Dargai in Malakand district, respectively.

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77

Table 3.3.1 Comparison of body mass (g) and external body measurements (mm) of Rhinopoma microphyllum captured during

present study with Rahman et al. (2015), Benda et al. (2009), Davis, (2007), Bates and Harrison (1997), Roberts (1997)

and Schlitter and Qumsiyeh (1996).

Body

Parameters

Present Study

(n=3)

Rahman et al.,

2015

Benda et al. 2009

Davis, 2007

Bates and

Harrison, 1997

Roberts,

1997

(n = 6)

Schlitter and

Qumsiyeh, 1996

BM 18.00±6.00(12.00-24.00) 19.09±1.36 29.7 10-12 - - -

HB 71.03±5.09(65.36-75.20) 65.29±2.20 88 50-63 75.3±6.2 (60.0-84.0) 74-90 -

E 20.04±1.76(18.08-21.50) 21.69±0.63 - - 19.7±1.1 (18.0-22.0) 19-22 -

TRH 6.85±1.52 (5.10-7.79) - - - - - -

FA 67.45±4.60 (64.10-72.70) 68.71±1.05 66.36± 2.48 (62.5-71.1) 50-60 68.0±3.3 (59.5-74.6) 61-71 57-75

THC 8.80±0.95 (8.24-9.90) 15.43±0.24 - - - - -

2mt 47.46±3.23 (45.36-51.18) 52.02±1.63 - - - - -

1ph2mt 4.60±0.27 (4.30-4.82) 5.03±0.21 - - - - -

2ph2mt 4.58±0.09 (4.52-4.68) 4.36±0.31

3rd met 48.57±2.95 (46.85-51.98) 52.41±1.86 - - - - -

1st Ph. 3rd met 9.53±0.83 (8.93-10.48) 9.97±0.42 - - - - -

2nd Ph. 3rd met 17.40±1.73 (15.77-19.22) 16.80±2.63 - - - - -

4th met 38.28±2.76 (36.35-41.44) 41.93±1.27 - - - - -

1st Ph. 4th met 14.49±0.31 (14.13-14.70) 15.23±0.62 - - - - -

2nd Ph. 4th met 11.52±0.84 (10.84-12.45) 11.11±0.56 - - - - -

5th met 43.19±2.60 (41.46-46.18) 47.10±0.66 - - - - -

1ph5mt 10.64±0.28 (10.34-10.89) 11.16±0.30 - - - - -

2ph5mt 9.80±0.75 (9.12-10.60) 9.78±0.47 - - - - -

WS 266.67±10.41 (255.00-275.00) 197.49±9.76 - - - - -

TIB 26.59±1.84 (25.18-28.67) 26.91±1.14 - - - - -

HF 15.51±0.70 (15.09-16.31) 15.93±0.43 - - 15.0±1.0 (14.0-18.0) 15-16 -

T 51.45±1.18 (50.37-52.71) 57.20±2.80 68 48-68 58.1±5.6 (50.0-77.0) 46-55 41-63

n - The number of specimens; BM - Body mass; HB - Head and body; E - Ear; TRH- Tragus height; FA - Forearm; THC– Thumb with claw; 2mt - 2nd metacarpal; 1ph2mt - 1st Phalanx on 2nd

metacarpal; 2ph2mt - 2nd Phalanx on 2nd metacarpal; 3mt - 3rd metacarpal; 1ph3mt - 1st Phalanx on 3rd metacarpal; 2ph3mt - 2nd Phalanx on 3rd metacarpal; 4mt - 4th metacarpal; 1ph4mt - 1st

Phalanx on 4th metacarpal; 2ph4mt - 2nd Phalanx on 4th metacarpal; 5mt - 5th metacarpal; 1ph5mt - 1st phalanx on 5th metacarpal; 2ph5mt - 2nd phalanx on 5th metacarpal; WS - Wing span; TIB -

Tibia; HF - Hind foot; T- Tail.

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78

Table 3.3.2. Comparison of cranial measurements (mm) of Rhinopoma microphyllum captured during present study with Rahman et

al. (2015), Benda et al. (2009), Bates and Harrison (1997) and Schlitter and Qumsiyeh (1996).

Cranial

Parameters

Present Study

(n = 2)

Rahman et al. 2015

Benda et al. 2009

Bates and

Harrison, 1997

Schlitter and

Qumsiyeh, 1996

Condylo-canine length 18.29±0.95 (17.62-18.96) 18.61±0.21 18.64±0.563 (17.74-19.92) 18.9±1.1 (17.2-22.7) -

Maxillary toothrow 7.30±0.18(7.17-7.43) 7.38±0.26 7.52±0.214(7.07-7.95) 7.5±0.3 (7.0-8.0) 6.4-7.9

Mandibular toothrow 8.11±0.11(8.03-8.19) 7.88±0.21 8.18±0.257(7.51-8.73) 8.2±0.3 (7.6-8.6) -

Greatest length of skull 20.15±0.64(19.69-20.60) 19.64±0.21 20.77±0.568 (19.72-22.29) 20.9±0.9 (19.2-22.3) 18.4-22.1

Mandible length 14.38±0.63 (13.93-14.82) 14.41±0.26 - 14.8±0.7 (13.7-15.8) -

Posterior palatal width 8.92±0.30(8.71-9.13) 4.96±0.19 9.20±0.347(8.47-9.82) - -

Zygomatic breadth 12.22±0.88 (11.59-12.84) 12.13±0.15 12.19±0.460 (11.40-13.08) 12.4±0.6 (11.4-13.4) 10.8-13.5

Breadth of braincase 8.74±0.53(8.36-9.11) 8.62±0.22 - 8.9±0.4 (8.2-9.4) 7.8-9.2

Postorbital constriction 2.65±0.11 (2.57-2.73) 2.66±0.23 2.64±0.178 (2.28-3.02) 2.8±0.2 (2.1-3.1) -

Anterior palatal width 4.91±0.49(4.56-5.25) 9.31±0.27 5.32±0.302(4.75-6.12) - -

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Table 3.3.3. Comparison of body mass (g) and external body measurements (mm) of Rhinopoma hardwickii captured during present

study with Javid et al. (2012), Benda et al. (2009), Davis, (2007), Bates and Harrison (1997), Roberts (1997) and

Qumsiyeh and Jones (1986).

Body

Parameters

Present Study

(n=5)

Javid et al. 2012

(n=2)

Benda et al. 2009

(n=3)

Davi,

2007

Bates and Harrison,

1997

Robert,

1997

(n=9)

Qumsiyeh

and Jones, 1986

BM 10.60±2.86 (7.00-13.00) 15.30±0.424(14.9-15.7) 9.90±0.529 (9.5-10.5) 10-12 - - -

HB 64.67±3.00 (61.30-68.01) 66.00±5.657(62.0-70.0) 61.3±5.033(56-66) 50-63 66.6±4.1 (55.0-73.0) 62 (55-69) -

E 19.09±1.32 (17.20-20.02) 15.50±2.121 (14.0-17.0) - - 19.3±0.9 (17.0-21.0) 18 (16-20) 18-21

TRH 7.35±0.80 (6.11-8.01) 6.50±0.707 - - - - -

FA 59.90±1.21 (58.00-61.00) 54.00±0.000 (54.00-54.00) 59.02±2.411 (53.7-62.3) 50-60 59.2±2.6 (52.9-64.0) 60 (60-67) 52.4-60.0

THC 8.23±0.38 (8.01-8.90) - - - - - -

2mt 42.11±1.84 (39.11-44.00) - - - - - -

1ph2mt 5.23±0.54 (4.61-6.00) - - - - - -

2ph2mt 3.74±0.26 (3.50-4.01) - - - - - -

3rd met 43.57±1.60 (41.12-45.01) 39.00±0.000 - - - - -

1st Ph. 3rd met 9.19±0.34 (9.01-9.80) 9.00±0.000 - - - - -

2nd Ph. 3rd met 16.46±1.42 (14.20-18.00) 14.25±4.596 - - - - -

4th met 36.83±1.37 (34.50-38.01) 32.75±0.354 - - - - -

1st Ph. 4th met 12.17±0.52 (11.60-13.01) 11.50±1.414 - - - - -

2nd Ph. 4th met 10.64±0.51 (10.10-11.10) 10.50±0.707 - - - - -

5th met 41.63±1.43 (39.20-43.01) 37.50±0.707 - - - - -

1ph5mt 10.51±0.71 (9.50-11.11) 10.75±1.061 - - - - -

2ph5mt 9.85±0.79 (9.10-11.01) - - - - - -

WS 307.40±23.08 (280.00-338.00) 260.50±0.707 - - - - -

TIB 29.22±0.82 (28.10-30.01) 27.50±1.414 - - - - -

HF 14.72±0.36 (14.20-15.01) 14.00±0.000 (14.00-14.00) - - 13.4±1.2 (11.0-15.0) 11.5 (9-15) 12-15

T 66.57±2.15 (64.80-70.10) 59.00±2.828(57.0-61.0) 71.0±4.000 (67-75) 48-68 66.8±5.4 (56.0-78.0) 67 (57-77) 57-70

n - The number of specimens; BM - Body mass; HB - Head and body; E - Ear; TRH- Tragus height; FA - Forearm; THC– Thumb with claw; 2mt - 2nd metacarpal; 1ph2mt - 1st Phalanx on 2nd

metacarpal; 2ph2mt - 2nd Phalanx on 2nd metacarpal; 3mt - 3rd metacarpal; 1ph3mt - 1st Phalanx on 3rd metacarpal; 2ph3mt - 2nd Phalanx on 3rd metacarpal; 4mt - 4th metacarpal; 1ph4mt - 1st

Phalanx on 4th metacarpal; 2ph4mt - 2nd Phalanx on 4th metacarpal; 5mt - 5th metacarpal; 1ph5mt - 1st phalanx on 5th metacarpal; 2ph5mt - 2nd phalanx on 5th metacarpal; WS - Wing span; TIB -

Tibia; HF - Hind foot; T- Tail.

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Table 3.3.4. Comparison of cranial measurements (mm) of Rhinopoma hardwickii captured during present study with Javid et al.

(2012), Benda et al. (2009), Bates and Harrison (1997) and Qumsiyeh and Jones (1986).

Cranial

Parameters

Present Study

(n=4)

Javid et al. 2012

(n=2)

Benda et al. 2009

Bates and Harrison, 1997 Qumsiyeh and Jones,1986

Condylo-canine length 16.17±0.18 (16.01-16.42) 16.12±1.075 (15.36-16.88) 16.27±0.480 (15.23-17.62) 16.5±0.6 (15.5-17.5) -

Condylo-basal length - 17.78±0.898 (16.88-18.68) - - 15.6-16.9

Maxillary toothrow 6.08±0.07 (6.02-6.18) 5.84±0.359 6.29±0.179 (5.95-6.81) 6.4±0.2 (6.0-6.8) 5.7-6.3

Mandibular toothrow 6.72±0.13 (6.56-6.86) 6.10±0.718(5.59-6.60) 6.80±0.187 (6.38-7.21) 7.0±0.3 (6.5-7.5) -

Greatest length of skull 18.20±0.48 (17.78-18.80) 19.68±0.108 (19.60-19.75) 18.33±0.639 (16.31-19.74) 18.7±0.5 (17.5-19.7) -

Mandible length 12.38±0.23 (12.18-12.61) 11.28±1.652 (10.11-12.45) - 12.8±0.4 (11.8-13.6) 11.3-12.4

Posterior palatal width 7.89±0.30 (7.58-8.29) 9.53±0.180 7.88±0.280 (7.33-8.47) - -

Zygomatic breadth 10.48±0.46 (10.12-11.15) 12.08±0.162 (11.96-12.19) 10.77±0.390 (9.81-11.58) 10.9±0.4 (10.1-11.7) 9.9-10.9

Breadth of braincase 8.25±0.20 (7.95-8.39) 7.61±0.018 (7.59-7.62) - 8.2±0.2 (7.8-8.5) -

Postorbital constriction 2.93±0.14 (2.72-3.01) 2.88±0.054(2.84-2.92) 2.85±0.466(2.50-5.27) 2.8±0.2 (2.5-3.2) 2.4-2.9

Anterior palatal width 4.26±0.40 (3.77-4.64) 4.98±0.934 4.68±0.275 (4.16-5.16) - -

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Table 3.3.5. Comparison of bacular measurements (mm) of Rhinopoma microphyllum

captured during present study with Rhinopoma hardwickii Javid et al. (2012).

Bacular Parameters Present study (n=1) Javid et al. 2012 (n=1)

R. microphyllum R. hardwickii

Total baculum length 1.65 1.1

Proximal branch length 0.40 0.1

Proximal branch width 0.55 0.3

Distal branch length 0.01 0.00

Distal branch width 0.25 0.2

Width of distal extreme 0.43 -

Shaft length 1.25 1.0

Baculum height 0.60 0.4

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Bates, P., D. Thong and S. Bumrungsri. (2005). Voucher specimen preparation: bats. Harrison

Institute, England. Part of the Darwin Initiative Project: Taxonomic initiative for Southeast Asian

bat studies (Vietnam, Thailand, Cambodia and Lao PDR), 12 p

Bates, P. J. J. and D. L. Harrison. (1997). Bats of the Indian Subcontinent. Harrison Zoological

Museum (HZM). UK. 258 p

Benda, P., A. Reiter, M. Al-jumaily, A. Karim and P. Hulva (2009). A new species of mouse-

tailed bat (Chiroptera : Rhinopomatidae : Rhinopoma) from Yemen, J. Nat. Mus. (Prague), Nat.

Hist Ser. 177: 53-68.

Benda P., M. Andreas, D. Kock, R. K. lucan, P. Munclinger, P. Nová, J. Obuch, K. Ochman, A.

Reiter, M. Uhrin and D. Weinfurtova (2006). Bats (Mammalia: Chiroptera) of the Eastern

Mediterranean. Part 4. Bat Fauna of Syria: Distribution, systematics, ecology. Acta. Soc. Zool.

Bohem, 70: 1-329.

Benda, P., V. Hanák, M. Andreas, A. Reiter and M. Uhrin (2004). Two new species of bats

(Chiroptera) for the fauna of Libya: Rhinopoma hardwickii and Pipistrellus rueppellii. Myotis,

41-42: 109-124.

Brünnich, M.T. (1782). Dyrenes Historieog Dyre-Samlingenudi Universetets Natur-Theater.

Band 1. Kobenhaven.

Davis, L. (2007). An Introduction to bats of United Arab Emirates. Echoes Ecology Ltd. UK.

www.echosecology.co.uk. 24 p

Geoffroy, E. (1818). Description de lʹEgypte… Description des mammiferes. Paris 2

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Gaisler, J. (1970). The bats (Chiroptera) collected in Afghanistan by the Czechoslovak

expeditions of 1965-1967. Acta. Sci. Nat. Acad. Sci. Bohemoslov. Brno, 4: 1-56.

Gray, J. E. (1831). Description of some new genera and species of bats. Zoological Miscellany,

London.37-38.

Harrison, D. L. (1964). The mammals of Arabia. Ernest Benn Limited, London, 1: 1-192.

Hill, J. E. (1977). A review of the Rhinopomatidae (Mammalia: Chiroptera). Bulletin Brit. Mus.

Nat. Hist. (Zool. Ser.) London. 32: 29-43.

Hinton, M.A.C. and O. Thomas. (1926). Report No. 42. Kashmir and Punjab. Bombay Natural

History Society‟s Mammal Survey of India, Burma and Ceylon. Journal Bombay Nat. Hist. Soc.

31: 606-614.

IUCN. (2008). IUCN Red List of Threatened Species.Version 2.8.1.www.iucnredlist.org.

Javid, A., M. Mahmood-ul-Hassan, M. S. Nadeem and N. Rana and N. Khan. (2012). First

record of the Lesser Mouse-tailed bat Rhinopoma hardwickii (Rhinopomatidae: Chiroptera) from

Southern Punjab, Pakistan. The J. Anim. Plant Sci. 22(2): 278-282.

Javid, A., M. M. Hassan, S. M. Hussain and K. J. Iqbal. (2011). Recent record of the Asiatic

lesser yellow house bat (Scotophilus kuhlii) from Punjab, Pakistan. Mammalia, 78: 133–137.

Lidicker, W.Z., Jr. and A. Yang (1986). Morphology of the penis in the taiga vole (Microtus

xanthognathus). Journal of Mammalogy, 67: 497-502.

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of India. Journal Bombay Nat. Hist. Soc. 31: 597–607.

Madkour, G. (1961). The structure of the facial area in the mouse tail bat Rhinopoma hardwickii

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Qumsiyeh, M. B. and J. K. Jones (1986). Rhinopoma hardwickii and Rhinopoma muscatellum

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(2015). Occurrence of Rhinopoma microphyllum (Brunnich , 1782 ) in Khyber Pakhtoonkhawa,

Pakistan. The J. Anim. Plant Sci. 25(3 Supp. 2), 450–453.

Roberts, T.J. (1997). Mammals of Pakistan. Revised Ed. Oxford Univ. Press. Oxford, Pp 361.

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Schlitter, D. A. and M. B. Qumsiyeh.(1996). Rhinopoma microphyllum. Mammalian Species,

542: 1-5.

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Geographic Reference, D.E. Wilson and D.M. Reeder, eds., Smithsonian Institution Press,

Washington, DC.

Sinha, Y.P. (1980). The bats of Rajasthan: taxonomy and zoogeography. Record Zool. Sur.

India. 76: 7-63.

Thomas, O. (1903). On the of the genus Rhinopoma Annals Mag. Nat. Hist. (7)11:496-499.

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from C.A.M.P. 2002.Report.Zoo Outreach Organization. BSG South Asia and Wild,

Coimbatore, India.

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Mammal Survey of India, Burma and Ceylon. Journal Bombay Nat. Hist. Soc. 24:291–316.

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DESCRIPTION OF THE FIRST RECORD OF THE INDIAN FALSE VAMPIRE BAT

(Megaderma lyra) E. Geoffroy, 1810 (RHINOPOMATIDAE: CHIROPTERA) CAPTURED

FROM NORTHWESTERN PAKISTAN

Mohammad Salim and Muhammad Mahmood-ul-Hassan*

Department of Forestry and Wildlife Management, University of Haripur, Haripur, Pakistan.

*Department of Zoology and Fisheries, University of Agriculture, Faisalabad

Corresponding author’s Email: [email protected]; [email protected]

(This manuscript has been published in the Journal of Animal and Plant Sciences)

(Impact Factor = 0.422)

Citation: M. Salim and M. Mahmood-ul-Hassan. Description of the first record of the

Indian False Vampire Bat (Megaderma lyra) E. Geoffroy, 1810 (Rhinopomatidae:

Chiroptera) captured from Northwestern Pakistan. The Journal of Animal & Plant

Sciences, 24(4): 2014, Page: 1-6.

ABSTRACT

The greater false vampire bat Megaderma lyra is an Indomalayan bat species. Although this

species has been reported from Punjab, Sind and Baluchistan, no specimen has been captured

from Khyber-Pakhtunkhwa (KP). We report its occurrence further northwest of Pakistan in

Malakand district where 40 greater false vampire bats were recorded roosting in a chromite mine

at Heroshah of tehsil Dargai. We used a hand net to capture the bats. Upon examination it was

found that all were females. The captured bats were identified on the basis of their unique facial

appearance, an erect and elongated nose-leaf and large oval ears that joined on the forehead. This

paper documents craniomorphometeric characteristics of the greater false vampire bats

inhabiting northwestern part of the country and compares with previous available records.

Key words: First record; Malakand; Heroshah; Chiroptera.


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INTRODUCTION

Family Megadermatidae (Chiroptera: Mammalia) is one of the eight bat families that are

confined to the Old World tropics (Bates and Harrison, 1997) and consists of four genera and six

species worldwide. Three genera (Cardioderma Peters, 1873, Lavia Gray 1838 and Macroderma

Miller, 1906) are monospecific (C. cor, L. frons and M. gigas) while the fourth one i.e.

Megaderma E. Geoffroy, 1810 is represented by two species. Of these two, M. lyra E. Geoffroy,

1810 is a larger Oriental species that differs from its congener (M. spasma) by a longer forearm,

short and broad tragus, deep prenasal notch and smaller postorbital process (Csorba and Topal,

1994). It is due to these morphological differences that M. lyra is placed in a separate subgenus

Lyroderma (Lekagul and McNeely, 1977). Family Megadermatidae, represented in Pakistan only

by a single species i.e. Megaderma lyra, is widely distributed in the south and southeast Asia

from Afghanistan to southern China, Burma, Thailand, Cambodia, Laos, Vietnam, south to Sri

Lanka, West Malaysia and Bangladesh (Simmons, 2005). The mammal collection of the British

Museum (London) houses seven specimens of M. lyra from Pakistan of which six were collected

from Lehtrar (Murree), Punjab and one from Baluchistan (Siddiqi, 1961). The Baluchistan

specimen was collected from Lasbela (Roberts, 1997). Some specimens have also been collected

from Lahore and Sialkot (Punjab), and from Sukker in Sindh (Roberts, 1997). However, this

species has never been recorded from northern Pakistan. Although these bats have been collected

from Nangahar Province in Afghanistan (Gaislar, 1970), the species has not been reported from

Iran (Roberts, 1997; Bates and Harrison, 1997; Simmons, 2005; Mahmood-ul-Hassan et al.,

2009). This paper documents cranio-morphometeric characteristics of five specimens of M. lyra

collected for the first time from District Malakand, Khyber PakhtunKhwa.

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Malakand district (N34°33′56″ E71°55′51″) is located in northwest Pakistan at an elevation of

844 m above sea level. It is bounded on the north by the district Lower Dir, on the northeast by

Swat and southeast by Buner. Mardan and Charsadda districts lie in south while Bajaur and

Mohmand Agencies lie in west of Malakand district. The district is surrounded by mountains on

the northeast and west that separate it from Swat, Bajaur and Mohmand, respectively. The

district is famous for chromite and granite mining and is typified by steppic forest in

intermediate latitudes vegetated with Juniperus macropoda, Franxinus xanthoxyloides, Pinus

gerardiana, Artmisia maritime, Rheum emodi, Ephedra nebrodensis, Rosa webbiana, Tennisetum

orientalis, Pistacia mutica, Thymus serpyllum and Eremurus aurantiacus. The mammal fauna of

the area includes the collared pika Ochotona rufescens, the migratory hamster Cricetulus

migratorius, the stone martin Martes foina, the forest dormouse Dryomys nitedula, the Persian

jird Meriones persicus and the mouse-like hamster Callomyscus bailwardi (Roberts, 1997; Ali et

al., 2012). A survey of the Malakand Division (Pakistan) was carried out to record its bat fauna.

All the potential bat roosts such as mines, old and undisturbed buildings, abandoned wells and

farm houses were thoroughly searched (Mahmood-ul-Hassan et al., 2012). Local people were

interviewed for gaining information about the exact location of various bat roosts. A handheld

GPS (Garmin Etrax H) was used to record geographical coordinates. A total of 40 M. lyra were

found roosting in a mine at Heroshah, (N34° 26.762ʹ E71° 49.064), Tehsil Dargai. The mine was

83 m long, 1.5 m high and 2 m wide, and had been mined for the last ten years. The floor was

littered with bat guano. We used a locally made hand net to capture the bats all of which were

adult females. The captured specimens were placed in separate cotton bags, weighed up to 0.1 g

(Pesola Spring Balance 300g) and measured before being euthanized and preserved in absolute

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alcohol. Specimens were then brought to the laboratory for recording cranial measurements. The

skulls (n =3) were prepared and measured following Bates et al. (1997, 2005) and Javid et al.

(2012a,b). The remaining two specimens remained preserved in absolute alcohol in the BatLab,

Department of Zoology and Fisheries, University of Agriculture, Faisalabad.

RESULTS

Distribution: Of the seventeen mines roosts visited, only a single colony of M. lyra was recorded

from Heroshah where it was co-roosting with Rousettus leschenaultii and Hipposideros fulvus.

Dental Formula. 0123/2123=28. Morphology. This is a large bat with a big head and prominent

muzzle. Its huge semi-naked ears, which are bluntly rounded, join in the middle of the forehead

and possess bifurcated tragus. The noseleaf is simple, straight and long enough to reach almost

near the forehead. The skin of the nose leaf is pink and naked with a ridge and two furrows in

the middle. The eyes are quite large and prominent. The lower jaw is comparatively longer the

upper one. Dorsal body fur is mouse grey and consists of long, fine and silky hair. The belly fur

is a paler and more yellowish grey. Wings are broad as the fifth digit is relatively long. The

second phalanx on the second metacarpal is absent. Tail does not extend beyond the inter-

femoral membrane which is supported by calcars. Female have two pectoral mammae with two

more false teats in the pubic region.

Body Mass and External Body Measurements. The mean body mass of the five M. lyra was

52.40g ± 3.58 (SD). Their head and body length was 85.56 mm ± 2.40 (SD) while their ear was

38.19 mm ± 3.65 (SD) long. Mean thumb and forearm length was 11.80 mm ± 0.44 (SD) and

70.06 mm ± 0.69 (SD), respectively. The tragus height was 13.00 mm ± 0.01 (SD). The nose leaf

height was 10.00 mm ± 0.00 (SD). The length of 2nd

metacarpal was 57.43 mm ± 1.50 (SD). The

mean length of 1st phalanx on 2

nd metacarpal was 8.09 mm ± 1.51 (SD). The mean length of 3

rd

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metacarpal was 51.43 mm ± 0.88 (SD) while that of 1st and 2nd

phalanges on 3rd

metacarpal were

29.63 mm ± 1.11 (SD) and 51.43 mm ± 0.52 (SD), respectively. The mean length of 4th

metacarpal was 56.25 mm ± 0.42 (SD). The mean length of 1st and 2nd phalanges on 4th

metacarpal was 18.43 mm ± 0.88 (SD) and 24.27 mm ± 0.75 (SD), respectively. The mean

length of 5th

metacarpal was 60.85 mm ± 0.82 (SD) while that of 1st phalanx on 5th

metacarpal

was 21.22 mm ± 0.44 (SD). The length of 2nd

phalanx on 5th

metacarpal was 20.62 mm ± 0.52

(SD). The mean wing span was 452.00 mm ± 1.58 (SD). Their tibia and calcar were 36.33 mm ±

1.07 (SD) and 9.86 mm ± 1.01 (SD), respectively while the length of hind foot was 18.08 mm ±

1.17 (SD).

Table 3.4.1. Comparison of mean external body and cranial measurements (mm) of

Megaderma lyra captured from Heroshah tehsil Dargai in Malakand district

(present study) with a previous studies from South Asia (Bates and Harrison,

1997) and Pakistan (Roberts, 1997).

Body Parameters Bates and

Harrison,

1997

Present

study

Bates

and

Harrison,

1997

Present study

(Range)

Roberts,

1997

Head and body length 82.8± 5.9 85.40±2.41 70.0-95.0 82.00-88.00 76-94

Ear length 37.9± 1.8 38.14±3.63 31.5-45.0 31.70-40.00 33-40

Forearm length 66.4±2.2 70.00±0.71 56.0-71.5 69.00-71.00 65-72

Wingspan 416.7±32.4 452.00±1.58 396-454 450.00-454.00

Hind foot length 16.7±1.4 18.00±1.22 14.0-20.0 17.00-20.00 45-47

Nose-leaf height - 10.00±0.00 - 10.00-10.00 -

Greatest skull length 28.7± 0.6 29.60±0.46 27.1-30.2 29.10-30.01 -

Condylocanine length 25.4±0.5 26.37±0.21 24.5-27.8 26.20-26.60 -

Zygomatic Breadth 16.4±0.4 17.01±0.01 15.4-17.1 17.00-17.01 -

Breadth of the braincase 12.2±0.2 12.57±0.25 11.8-12.9 12.30-12.80 -

Post-orbital constriction 4.7±0.1 4.97±0.12 4.3-5.2 4.90-5.10 -

Maxillary tooth row length 11.2±0.3 11.40±0.10 10.6-12.1 11.30-11.50 -

Mandibular tooth row length 12.2±0.3 11.94±0.04 11.6-12.2 11.90-11.98 -

Mandible length 19.8±0.5 20.04±0.03 18.8-21.2 20.01-20.07 -

Cranial Measurements. Mean greatest length of skull of the three specimens was 29.60 mm ±

0.46 (SD) (Plate 3.4.2). The breadth of braincase was 12.57 mm ± 0.25 (SD) while that of

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Figure. 3.4.1. Map showing the roosting places of Megaderma lyre recorded from Pakistan and

Afghanistan along with the first record from a cromite mine at Heroshah in techsil

Dargai of district Malakand in northern Pakistan.

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Figure 3.4.2. Dorsal (a), Ventral (b) and Lateral (c) view of the skull of Megaderma lyra and

dorsal view (d) of the lower jaw of a specimen (BatLab # 9) Captured form Heroshah in Tehsil

Dargai of District Malakand.

zygomatic bone was 17.01 mm ± 0.01 (SD). The post-orbital constriction was 4.97 mm ± 0.12

(SD) long. The mean condylo-canine length was 26.37 mm ± 0.21 (SD). Anterior and posterior

palatal widths measured 5.79 mm ± 0.14 (SD) and 9.93 mm ± 0.13 (SD), respectively. The

maxillary toothrow length was 11.40 mm ± 0.10 (SD). The mandibular tooth row length was

11.94 mm ± 0.04 (SD). The mandible length was measured as 20.04 mm ± 0.03 (SD).

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DISCUSSION

The bat fauna of Pakistan is the least explored both in terms of the number of bat species and

their distribution (Mahmood-ul-Hassan and Nameer, 2006). Most of the studies on bats of the

country were done during the British reign, and as such no major reference bat collection is

available in any museum of the country even today. Descriptions of some bats (e.g. Hippsideros

cinaraceus and Triaenops persicus) are based only on a single specimen and have not been

collected afterwards from the country. Siddiqi (1961), Roberts (1977, 1997), Bates and

Harrison(1997), Mahmood-ul-Hassan et al. (2009) and Srinivasulu et al. (2010) are the main

sources of information on the bat fauna of the country but mainly relied on reviews. Mahmood-

ul-Hassan et al. (2011) and Javid et al. (2012a, b) have made some recent efforts to redefine

distribution and status of some bat species in Punjab, Pakistan. The bat fauna of northern

Pakistan has however remained unexplored so far. Detailed knowledge about almost all the bat

species is currently lacking thereby making a perplexing situation regarding their taxonomy and

distribution. The new bat species are generally recorded from the area that either has remained

least surveyed or the species have changed their distribution ranges over the past few decades.

Both these situations are true in case of Pakistan. The cavernicolous roost from which these M.

lyra were recorded lies in the northwest of Lehtrar (Murree) Punjab at 167.8 km and 115.6

degrees and southwest of Nangarhar Province Afghanistan at 112.2 km and 259.2 degree and

represents the first record of M. lyra from northern Pakistan. The false vampires are neither

blood sucking nor the members of family Desmodontidae which are confined to South America

(Roberts, 1997). They belong to an ancient family of carnivorous bats and are placed in super

family Rhinolophoidae along with rhinopomatid and rhinolophid bats in the Suborder

Yinpterochiroptera (Springer et al., 2001; Teeling et al., 2005; Jones and Teeling, 2006). Like

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most of the Oriental bat species, M. lyra colonized Pakistan from the south through the savannah

type vegetation of the Rann of Katch as well as from the north through the Himalayan foothills

(Mahmood-ul-Hassan et al., 2009). Its colonies have been recorded in man-made structures such

as temples, cellars, natural caves and open wells (Brosset, 1962; Eates, 1968; Roberts, 1997) and

diet includes small mammals, birds, frogs and fishes as well as large insects (Hill and Smith,

1984). Owing to its feeding habits, the false vampire bat is acknowledged as a good friend of

farmers and is rewarded with protection by farmers, who call it the “goddess Laxmi” and provide

it food during harsh weather (Mahmood-ul-Hassan and Nameer, 2006). Colonies ranging from

25 to 240 individuals, consume rats and mice, which destroy different grains stored in bags

(Sinha, 1986). The cranio-morphometeric comparison of the bat specimens captured from

Heroshah revealed that the bats captured from northern Pakistan averaged a bit larger than those

reported by Bates and Harrison (1997). All their body parameters however were in the ranges

recorded by Bates and Harrison (1997) and Roberts (1997) (Table 3.4.1).

Acknowledgements: This study was partly funded by the Rufford Small Grants Foundation (UK)

and Bat Conservation International (USA). The financial assistance provided by these funding

agencies is gratefully acknowledged.

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MORPHOMETRIC VARIABILITY IN HORSESHOE BAT SPECIES, RHINOLOPHUS

FERRUMEQUINUM AND RHINOLOPHUS LEPIDUS CAPTURED FROM DISTRICT

MALAKAND, KHYBER PAKHTUNKHWA, PAKISTAN

Mohammad Salim, Arshad Javid1, Faiz-ur-Rahman

2, Khalid Javed Iqbal

3 andFarmanUllah

4

Department of Forestry and Wildlife Management, University of Haripur, Khyber Pakhtunkhwa,

Pakistan 1Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore,


Khyber Pakhtunkhwa, Pakistan 3Department of Life Sciences, TheIslamia University of Bahawalpur

4Department of Animal Breeding and Genetics, Lasbela University of Agriculture, Water and



(This manuscript has been submitted for publication in Pakistan Journal of Zoology)

(Impact Factor = 0.478 Impact factor)

ABSTRACT

Specimens of Rhinilophus ferrumequinum (n = 2) and R. Lepidus (n =3) were captured from

Malakand district, Khyber Pakhtunkhwa during a three years survey extending from June 2010

through May 2013. Mean body mass of the captured R. ferrumequinum specimens was 18.45 ±

0.35 g, head and body length was 60.11 ± 1.42 mm and forearm length was 60.01 ± 1.41 mm.

Similarly, average greatest length of skull was 23.35 ± 0.20 mm while the total length of

baculum of a single specimen was recorded 4.13 mm. The mean body mass, head and body

length and forearm length of the R. lepidus specimens captured from the study area was 3.93 ±

0.21 g, 38.49 ± 0.54 mm and 38.02 ± 0.63 mm, respectively. Average greatest length of skull of

two specimens was 15.94 ± 0.15 mm while their baculum was 2.33 ± 0.14 mm long.

Key words: Horseshoe bat, Baculum, R. lepidus, Malakand, Abbottabad

INTRODUCTION


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96

The genus Rhinolophus Lacepede, 1799 has 76 species worldwide of which sixteen species exist

in the Indian subcontinent while five have been recorded from Pakistan which include greater

horseshoe bat R. ferrumequinum Schreber, 1774, the lesser horseshoe bat R. hipposideros

Bechstein, 1800, the Blasius horseshoe bat R. blasii Peters, 1866, the Blyth‟s horseshoe bat R.

Lepidus Blyth, 1844 and the big-eared horseshoe bat R. macrotis Blyth, 1844 (Roberts, 1997;

Bates and Harrison, 1997; Simmons, 2005).

R. ferrumequinum is widely distributed in northern Himalayan region and extends southwards

through the mountains of Waziristan and northern Balochistan. This bat seems to be rare in

southern Balochistan because of the lesser supply of suitable insect prey and very dry climate

which is unfavorable to the family Rhinolophidae (Roberts, 1997). Specimens have been

collected from around Dir town (USNM), Abbotabad (HZM), Karakar pass (FMNH), Gilgit

(Bates and Harrison, 1997) and Kululai in Swat (Roberts, 1997). These larger greyer specimens

have been assigned to the subspecies R. f. proximus (Roberts, 1997). Small colonies found in

Balochistan near Kalat, Nushki and Quetta have been assigned to R. f. irani (Mirza, 1965; Bates

and Harrison, 1997). The greater horseshoe bat is considered to be Least Concerned worldwide

(IUCN, 2008; Mahmood-ul-Hassan et al., 2009) and Near Threatened in South Asia (South

Asian Chiroptera C. A. M. P. Report, 2002; Walker and Molur, 2003; IUCN, 2008).

R. Lepidus in Pakistan was captured together with R. macrotis during October 1985 near

Abbotabad from an elevation of 1280m in Khyber Pakhtunkhwa, Pakistan (Roberts 1997; Bates

and Harrison, 1997). The species has also been collected from Afghanistan (Corbet and Hill,

1992) and in the dryer parts of Rajasthan, India (Sinha, 1980). Population status of R. lepidus in

Pakistan is unknown (Roberts, 1997).

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In Pakistan, the bats are amongst the least studied group of animals. Present survey was therefore

planned to ascertain the presence or absence of Rhinolophus species from Malakand district,

Khyber Pakhtunkhwa, Pakistan.


Study area: District Malakand owns variety of habitat types ranging from plain to mountainous

areas. River Swat is the natural water body that irrigates cultivable areas in the district. Other

sources include water tanks, tube wells and lift pumps. The climate is moderately cool in winter

and pleasant in summer, hottest months are June, July and August. The maximum temperature

during summer reaches 41℃ and minimum during winter reaches -2 ℃. Rose and tulips are

wildly grown. Main plant species in Malakand include Bakain (Melia azerdarach), Shesham

(Dalbergia sissoo), Persian walnut (Juglans regia), figs (Ficus carica), phulai or Paloosa

(Acacia modesta), white mulberry (Morus alba) black mulberry (Morus nigra) chilgoza pine

(Pinus gerardiana) blue gum (Eucalptus globulus) Persian poplar (Populus caspica) and chinar

(Platanus orientalis) are grown in hilly as well as in plain areas. The common wild animals

found in the area are jackal, deer, leopard, monkey and wolf. The wild fauna includes the

markhor (Capra falconeri), the collared pika (Ochotona rufescens), the migratory hamster

(Cricetulus migratorius), the stone marten (Martes foina), the forest dormouse (Dryomys

nitedula), Persian jird (Meriones persicus) and the mouse-like hamster (Calomyscus bailwardi).

The livestock animals in the district are buffalo, cow, sheep, goat, camel, horse, ass and poultry.

Sampling strategy: Bats were trapped over duration of three years (2010-2013) on their roosting

and foraging grounds using hand net and mist nets at randomly preselected points within

Malakand district. Sampling stations were decided based on a pilot study designed to assess the

species composition in a variety of habitats. Mist nets of 12 m, 9 m and 6m size were erected at

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10 to 50 meter intervals along trails and water bodies, and were monitored for three hours

depending on weather and bats‟ activities. The nets used throughout the survey were thesame

and were opened simultaneously at sunset each evening. On either side of the mist net torches

were positioned to illuminate bats approaching from either side of the net. Bats were removed

and placed in cloth bags (made with a breathable material), and each bat was weighted (g) with a

digital scale. The external body, cranial and bacular measurements were taken with a digital

vernier caliper (Bates and Harrison, 1997; Javid, 2011).


During present survey, a colony of 46 Rhinolophus ferrumequinum was observed in a cave at

Loya Agra tehsil Batkhela in Malakand district (Figure 3.5.1) and two of them were captured

through hand net. The length of cave was 40 ft, width of cave opening 4ft, width of cave middle

8ft while height of the cave was 7ft. The captured specimens had awoolly fur, doom shaped head

and curved ears that had no tragus. The outer margins of the ears however were curved round to

form a prominent antitragus. The muzzle of the bat was well covered with hairs. The wings were

delicate, short and rounded in outline. A well-developed interfemoral membrane is supported by

calcars which have no lobe of skin beneath them. The front and side view of the noseleaf show

that horseshoe apparatus is broad, sella is small and the superior connecting process is broadly

triangular in these bats (Figure 3.5.1). The inferior extremity is bluntly rounded and lancet is

equilateral triangular in shape. The mean body mass of two R. ferrumequinum was 18.45 ± 0.35

g, their head and body length was 60.11 ± 1.42 mm while their ear was 20.62 ± 0.70 mm long.

Mean thumb with claw and forearm length was 4.01 ± 0.01 mm and 60.01 ± 1.41 mm,

respectively. Average length of 2nd

metacarpal was 39.56 ± 3.47 mm, length of 3rd

metacarpal

was 40.07 ± 1.34 mm, length of 4th

metacarpal was 43.62 ± 0.57 mm while average length of

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5th

metacarpal was 45.66 ± 0.64 mm. Average wingspan and calcarlength was 359.00 ± 1.41 mm

and 6.51 ± 0.69mm, respectively. Their tibia, tail and hind foot lengths were 26.06 ± 1.34 mm,

34.60 ± 0.71 mm and 12.11 ± 8.56 mm, respectively (Table 3.5.1).

Average greatest length of skull (n = 2) of R. ferrumequinum specimens (Figure 3.5.1) was 23.35

± 0.20 mm, breadth of braincase 9.69 ± 0.23 mm and zygomatic bone of the two specimens was

12.15 ± 0.12 mm long. The postorbital constriction was 2.98 ± 0.02 mm, condylo-canine length

was 20.78 ± 0.05 mm while anterior and posterior palatal widths were 6.31 ± 0.01 mm and 8.73

± 0.14 mm, respectively. The maxillary toothrow length,mandibular toothrow length and

mandible length was 9.18 ± 0.02 mm, 9.86 ± 0.01 mm and 16.33 ± 0.13 mm, respectively.

Total baculum length of a single R. ferrumequinum specimen was 4.13 mm, width of proximal

tip 0.33 mm, width of middle extreme 0.80 mm, width of distal extreme 1.13 mm while baculam

height was recorded 0.83 mm (Table 3.5.1, Figure 3.5.2).

Figure. 3.5.1. Map of Malakand Division showing its constituent administrative units.

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Figure. 3.5.2. Distribution map of R. ferrumequinum and R. lepidus.

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101

Figure 3.5.3 Face (a), and a close up of the front (b) and side view (c) of the horseshoe

apparatus of Rhinolophus ferrumequinum. The Figure also shows dorsal (d), ventral (e) and

lateral side (f) of the cranium and the dorsal view (g) of lower jaw a specimen of this species

(BatLab No. 237) captured from Loya Agra tehsil Batkhela in Malakand district, respectively.

Figure 3.5.4. Photograph of a stained baculum of the greater horseshoe bat Rhinolophus

ferrumequinum (Bat lab 237), captured in a cave from Loya Agra in Malakand

district.

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Table 3.5.1. Coparison of mean external body and cranial measurements (mm) of Rhinolophus

ferrumequinum (n=2) captured from Loya Agra in Malakand district with a

previous study from South Asia.

Body Parameters

Mean±SD

Albayrak

1985

Bates and

Harrison, 1997

Roberts,

1997

Benda et al.

2010

Albayrak et

al. 2013

Present

Study (n=2)

Body mass 21.9±4.19 - 25 - 19.3±3.76 18.45±0.35

Head and body 73.2±1.98 65.9±6.6 71 73.5±2.268 72.2±3.39 60.11±1.42

Ear 24.6±2.10 24.3±2.1 24 - 25.2±1.87 20.62±0.70

Forearm 54.2±1.29 58.9±2.2 - 57.55±1.477 53.3±1.72 60.01±1.41

Thumb with claw - - - - - 4.01±0.01

2nd metacarpal - - - - - 39.56±3.47

1st phalanx on 2nd metacarpal - - - - - 4.01±0.01

2nd phalanx on 2nd metacarpal - - - - - 18.56±0.64

3rd metacarpal - 39.3±1.3 - - - 40.07±1.34

1st Phalanx on 3rd metacarpal - 20.5±1.0 - - - 21.56±0.64

2nd Phalanx on 3rd metacarpal - 32.6±2.1 - - - 31.57±0.62

3rd phalanx on 3rd metacarpal - - - - - 4.01±0.01

4th metacarpal - 43.9±1.3 - - - 4.01±0.01

1st Phalanx on 4th metacarpal - 12.5±0.9 - - - 13.62±0.57

2nd Phalanx on 4th metacarpal - 20.1±1.3 - - - 13.58±0.61

5th metacarpal - 45.3±0.5 - - - 45.66±0.64

1st Phalanx on 5th metacarpal - - - - - 16.07±1.33

2nd Phalanx on 5th metacarpal - - - - - 18.59±0.63

Wing span - 356.0 - - - 359.00±1.41

Hind foot 13.2±1.19 11.6±1.3 12 - 13.8±0.87 12.11±8.56

Tail 35.0±3.34 34.9±3.0 34 40.0±4.071 37.9±3.46 34.60±0.71

Calcar - - - - - 6.51±0.69

Condylo-basal length 20.3±0.32 - - - 20.4±0.46 -

Condylo-canine length - 21.5±0.6 - 21.31±0.443 - 20.78±0.05

Cranial Parameters Albayrak

1985

Bates and

Harrison, 1997

Roberts,

1997

Benda et al.

2010

Albayrak et

al. 2013

Present

Study (n=2)

Greatest length of skull - 24.2±1.1 - - 23.8±0.45 23.35±0.20

Condylo-canine length - 21.5±0.6 - - - 20.78±0.05

Zygomatic breadth - 12.4±0.5 - - 12.0±0.31 12.15±0.12

Interorbital constriction - 2.6±0.2 - - 2.5±0.17 2.98±0.02

Breadth of braincase - 9.5±0.4 - - 10.2±0.26 9.69±0.23

Anterior palatal width - - - - - 6.31±0.01

Posterior palatal width - - - - - 8.73±0.14

Maxillary toothrow - 9.1±0.3 - - 8.6±0.18 9.18±0.02

Mandible length - 9.9±0.3 - - 15.9±0.35 16.33±0.13

Mandibular toothrow - 17.0±0.6 - - 9.2±0.25 9.86±0.01

Bacular Parameters Albayrak

1985

Bates and

Harrison, 1997

Roberts,

1997

Benda et al.

2010

Albayrak et

al. 2013

Present

Study (n=1)

Total baculum length - - - - - 4.13

Width of proximal tip - - - - - 0.33

Width of proximal extreme - - - - - 0.8

Width of distal extreme - - - - - 1.13

Baculum height - - - - - 0.83

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Specimens (n = 3) of Rhinolophus lepidus were captured from Malakand University in Malakand

district through mist nets during present survey. The horseshoe in this species is 6.0-8.0 mm

broad and does not cover the whole muzzle (Figure 3.5.3). The sella is generally narrow. The

lancet is well developed. The pelage color is typically grey brown dorsally and slightly pale

ventrally. Average body mass, head and body length and ear of three Blyth‟s horseshoe bat was

3.93 ± 0.21 g, 38.49 ± 0.54mm and 14.80 ± 0.27 mm, respectively. The mean thumb with claw

length and forearm length was 3.87 ± 0.13 mm and 38.02 ± 0.63 mm, respectively (Table 3.5.2).

The length of 2nd

metacarpal, 3rd

metacarpal, 4th

metacarpal and 5th

metacarpal was 27.98 ± 0.76

mm, 28.21 ± 0.01 mm, 29.61 ± 0.01 mm and 29.43 ± 0.01 mm, respectively. Average wingspan,

tibia, calcar, hind foot and tail length was 232.67 ± 1.15 mm, 15.83 ± 0.67mm, 8.67 ± 0.58 mm,

7.86 ± 0.28 mm and 18.96 ± 3.24 mm, respectively (Table 3.5.2).

The mean greatest length of skull (Figure 3.5.3) of R. lepidus specimens (n = 2) captured from

university of Malakand was 15.94 ± 0.15 mm, breadth of braincase 6.76 ± 0.06 mm, zygomatic

bone 7.61 ± 0.01 mm, post-orbital constriction 2.34 ± 0.01 mm and condylo-canine length was

13.90 ± 0.08 mm. Anterior and posterior palatal width was 3.73 ± 0.01 mm and 5.72 ± 0.01 mm,

respectively. The maxillary toothrow length, mandibular toothrow length and mandible length

was 5.86 ± 0.02 mm, 6.57 ± 0.64 mm and 10.34 ± 0.04 mm, respectively (Table 3.5.3). The

mean total baculum length, width of proximal extreme, shaft length, width of middle extreme,

width of distal extreme and baculum height of R. lepidus (n = 2) was 2.33 ± 0.14mm, 0.01 ±

0.00 mm, 2.16 ± 0.12 mm, 0.01 ± 0.00 mm, 0.49 ± 0.05 mm and 0.55 ± 0.00mm, respectively

(Table 3.5.2, Figure 3.5.4).

Prior to the present study, R. ferrumequinum was reported from Gilgit, Kululai in Swat,

Kohistan, Dir, Abbotabad and Karakar Pass (Roberts 1977; Bates and Harrison, 1997) in Khyber

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Pakhtunkhwa (KPK). In Baluchistan, the species has so far only been collected from Kalat and

Nushki (Mirza, 1965). The first specimen of R. lepidus was captured in mid-Octuber 1985 from

Abbotabad (Corbet and Hill, 1992; Roberts 1977; Bates and Harrison, 1997) in KPK. The

species was reported from Gujranwala in Punjab province (Shahbaz et al., 2014).

Figure 3.5.5. A close up of the face (a), and side view (b) of the horseshoe apparatus of

Rhinolophus lepidus and dorsal (c), ventral (d), lateral (e) sides of the cranium,

and dorsal view of lower jaw a specimen of this species (BatLab No. 280)

captured from Malakand University in Malakand district, respectively.

Figure 3.5.6. Lateral view of the baculum of Blyth‟s horseshoe bat (bat lab 281) Rhinolophus

lepidus captured from University of Malakand in Malakand district.

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Table 3.5.2. Coparison of mean external body measurements (mm) of Rhinolophus Lepidus

(n=3) captured from University of Malakand in Malakand district with a previous

study from South Asia.

BodyParameters

Mean (Range)

Bates and Harrison,

1997

Shahbaz et al. 2014

(n=10)

Present Study

(n=3)

Body mass - 6.42 (5.0-8.20) 3.93±0.21(3.70-4.10)

Head and body 42.9±4.8 (35.0-54.0) 42.36 (41-44.6) 38.49±0.54(38.17-39.11)

Ear 16.9±1.3(14.5-20.6) 13.49 (11-16) 14.80±0.27 (14.61-15.11)

Horseshoe -(6.0-8.0*) - 6.00±0.00(6.00-6.00)

Forearm 39.8±1.0 (37.0-41.8) 40.34 (39-42) 38.02±0.63(37.39-38.64)

Thumb with claw - - 3.87±0.13 (3.76-4.02)

2nd

metacarpal - - 27.98±0.76 (27.11-28.52)

1st phalanx on 2

nd metacarpal - - 9.00±1.00 (8.00-10.00)

3rd

metacarpal 30.4±1.3(28.2-33.3) 31.28 (30-32.4) 28.21±0.01(28.20-28.22)

1st Phalanx on 3

rd metacarpal 11.8±0.6(10.0-13.3) 12.35 (11.7-13) 10.66±0.32(10.45-11.03)

2nd

Phalanx on 3rd

metacarpal 17.3±0.6(16.0-18.9) 19 (17-23) 16.02±0.01(16.01-16.02)

4th

metacarpal 31.4±1.0(29.6-33.8) 32.0 (30.8-33) 29.61±0.01(29.61-29.62)

1st Phalanx on 4

th metacarpal 8.7±0.5(7.6-10.5) 9.68 (9-11) 8.82±0.23(8.67-9.08)

2nd

Phalanx on 4th

metacarpal 10.8±0.7(9.6-12.3) 11.55 (9-13) 9.78±0.29(9.61-10.11)

5th

metacarpal 31.1±0.9(29.4-33.4) 31.48 (30.4-32.7) 29.43±0.01(29.43-29.44)

1st phalanx on 5

th metacarpal - 10.61 (9.8-11.5) 9.66±0.20 (9.43-9.81)

2nd

phalanx on 5th

metacarpal - - 9.70±0.53 (9.09-10.02)

Wing span 244.0±12.0(232.0-256.0) 240.10 (220.9-250.2) 232.67±1.15(232.00-234.00)

Tibia 16.7±0.7(14.9-18.4) 17.19 (16.5-18.1) 15.83±0.67(15.20-16.53)

Hind foot 7.6±1.0(5.5-10.0) 8.78 (8-10.5) 7.86±0.28(7.62-8.17)

Tail 20.4±4.0(14.0-28.0) 22.79 (21-26) 18.96±3.24 (16.19-22.52)

Cranial Parameters Bates and Harrison,

1997

Shahbaz et al. 2014

(n=2)

Present Study

(n=2)

Condylo-canine length 14.6±0.5 (13.8-15.5) 14.2 (14-14.4) 13.90±0.08(13.84-13.96)

Maxillary toothrow 6.1±0.3(5.6-6.8) 6.75 (6.5-7) 5.86±0.02(5.84-5.87)

Mandibular toothrow 6.6±0.3(6.0-7.4) 5.6 (5.5-5.8) 6.57±0.64(6.12-7.02)

Greatest length of skull 17.2±0.7(16.2-18.4) 17.5 (16.8-17.5) 15.94±0.15(15.83-16.04)

Mandible length 11.0±0.5(10.0-12.1) 11.2 (11-11.4) 10.34±0.04(10.31-10.37)

Posterior palatal width 5.9±0.3(5.7-6.3) 6.3 (6.2-6.4) 5.72±0.01(5.71-5.72)

Zygomatic breadth 8.2±0.3(7.6-8.8) 8.5 (8.3-8.7) 7.61±0.01(7.60-7.61)

Breadth of braincase 7.1±0.3(6.5-7.8) 7.5 (7.3-7.7) 6.76±0.06(6.72-6.80)

Postorbital constriction 2.2±0.1(1.8-2.6) 2.3 (2.2-2.4) 2.34±0.01(2.33-2.34)

Anterior palatal width 4.0±0.1(3.7-4.2) 4.3 (4.2-4.4) 3.73±0.01(3.72-3.74)

Bacular Parameters Bates and Harrison,

1997

Shahbaz et al. 2014

(n=2)

Present Study

(n=2)

Total baculum length - 4.35 (4.06-4.61) 2.33±0.14 (2.23-2.43)

Width of proximal extreme - - 0.01±0.00 (0.01-0.01)

Width of middle extreme - - 0.01±0.00 (0.01-0.01)

Width of distal extreme - - 0.49±0.05 (0.45-0.53)

Shaft length - 3.85 (3.69-4.02) 2.16±0.12 (2.08-2.25)

Baculum height - 1.30 (1.23-1.38) 0.55±0.00 (0.55-0.55)

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NEW PROVINCIAL RECORD OF THE FULVOUS LEAF-NOSED BAT

HIPPOSIDEROS FULVUS GRAY, 1838 FROM KHYBER PAKHTUNKHWA,

PAKISTAN


2, Muhammad Mahmood-ul-Hassan

3, Faiz-ur-Rahman

4 and

Zulfiqar Ali5



Pakistan 3Department of Zoology and Fisheries, University of Agriculture, Pakistan

4Department of Zoology, Shaheed Benazir Bhutto University (SBBU), Main Campus, Sheringal,

Khyber Pakhtunkhwa, Pakistan 5Department of Zoology, University of the Punjab, Lahore


(This manuscript has been submitted for publication in the Journal of Animal and Plant

Sciences)

(0.422 Impact factor)

ABSTRACT

Fulvous leaf-nosed bat Hipposideros fulvus Gray, 1838 was reported from Punjab, Sindh and

Baluchistan provinces prior to the present investigation. During present survey, more than 66

bats were recorded roosting in a cave of Tura Gata (N34º 26.770′ E71º 49.090′) tehsil Dargai in

Malakand district. Identification of the species was based on shape of noseleaf apparatus, dental

formula and cranio-morphological characters. The morphological features, external body, cranial

and bacular measurements of captured specimens were compared with available literature.

Average head and body length of all the captured specimens (n = 17) of H. fulvus was 49.09 ±

1.16 mm, average forearm length was 41.41 ± 0.97 mm, greatest skull length (n = 13) was 18.45

± 0.16 mm while average baculum length (n = 9) was 1.45 ± 0.07 mm.

Key words: Cranial measurements; baculum size; the fulvous leaf-nosed bat; Malakand


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INTRODUCTION

The biology and ecology of almost all bat species in Pakistan is poorly known. Most of the

literature on bat species of Pakistan was generated during the 19th

century, and no worthwhile

efforts had been made to explore its bat fauna so far (Mahmood-ul-Hassan et al. 2009).The bat

fauna of Pakistan is as rich and diverse as compared to the whole Palaearctic which is the largest

biogeographic region of the world, comprising 26 genera and 8 families (Horacek et al., 2000). It

comprises 80 species in eleven genera throughout the world. In Pakistan it is represented by three

genera and four species which include Hipposideros Gray, 1831(H. fulvus, H. cineraceus),

Asellia Gray, 1838 (A. tridens) and Triaenops Dobson, 1871 (T. persicus) (Walker and Molur,

2003; Roberts, 1997; Bates and Harrison, 1997). All of the four species are uncommon.

Hipposideros fulvus is a small sized species of hipposideros with characteristically very large

ears, the tip of which are broadly rounded off (Figure 3.6.1). The feet are small. The noseleaf has

a greatest width of about 5 mm; its general morphology is similar to that of H. ater(Bates and

Harrison, 1997). Body weight of the adult animal ranges between 8 to 9 g (Gopalakrishna, 1969).

The baculum is small and comparable to that of H. ater. It has a straight shaft with a simple base

and tip (Bates and Harrison, 1997). It is closely similar in appearance to H. cineraceus from

which it can mainly be distinguished by its slightly greater size and more rufescent dorsal pelage

with very pale basal portion to the hairs. The dorsal fur of this species can vary widely in color in

parts of western India (Brosset, 1962) but in Pakistan all specimens from the Punjab have long

soft fur with the hairs pinkish white basally terminating in dark reddish brown or chestnut tips.

The tail is wholly enclosed by the inter-femoral membrane and the wings rather short and broad

and delicately constructed. The ears are large reaching 22 mm. the noseleaf consists of a naked

brown skinned pad roughly square in outline (Roberts, 1997).

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This species seems well adapted to arid regions in the areas having a scattered growth of tropical

thorn scrub or dry sub-tropical scrub. It particularly favors the open burrows of Porcupines and

hyenas for its diurnal roost as well as utilizing underground cellars, railway tunnels, and open

wells in Baluchistan, “Kharezes”. They are very susceptible to predation from crows and kites if

flying in daylight (Brosset, 1963).

This bat species is rare and locally distributed in Pakistan. The sub-species from northern India

and Pakistan is identified as to H. f. pallidus on account of its paler dorsal pelage coloration

(Corbit and Hill, 1992; Roberts, 1997; Bates and Harrison 1997). This species inhabits arid

regions typified by tropical thorn scrub or dry sub-tropical scrub. The Zoological Society of

Pakistan has collected fifteen specimens in the northern Punjab from around Rawalpindi (Sinha,

1980) and Chaklala (Hinton and Thomas, 1926) in the salt range. It apparently does not penetrate

into the foothills in the north and is absent from most of the Indus plain, occurring again in

Southern Sindh around Sukkur (Wroughton, 1916) the Mausoleum of Amir Khan Mono and in

Gholam and Gharo, all in Thatta District (Lindsay, 1926) and Shujawal (Siddiqi, 1961). In

Southern Baluchistan it has been collected fromPanjgur and Hoshab (Roberts, 1997).It is

recently recorded from Indian Occupied Kashmir (Saikia et al. 2006). The species is considered

to be least concern in South Asia (Walker and Molur, 2003; IUCN, 2008; Mahmood-ul-Hassan

et al. 2009; South Asia Bat CAMP, 2002).

Hipposideros fulvus has never been reported from Khyber Pakhtunkhwa province of Pakistan

prior to the present investigation. Present survey was therefore conducted to certain the presence

or absence of this species from Malakand division, Khyber Pakhtunkhwa.

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This two years study extending from 2010 to 2012 was carried out in Malakand district of the

Khyber Pakhtunkhwa, Pakistan. Malakand district is bounded on the north by Lower Dir district,

on the East by Swat district, and on the south east and south west by Mardan and Charsadda

districts, respectively and on the west by Mohmand and Bajur Agencies. The total area of

Malakand district is 952 Km2 and has a population density of 596 people per square kilometer.

Malakand is located from 34° 30′ 0″ north latitude and from 71° 45′ 0″ east longitudes. The

average maximum temperature is 30℃ and the average minimum temperature is 17℃. The

rainfall is extremely low and humidity is 54%. The soil of Malakandis irrigated by Swat river.

Malakand is surrounded by high mountains rich with mineral resources, vast deposits of

chromite iron, china clay and fuller earth have been found in Malakand.

Exploratory visits were made to locate as many bat roosts in the district as possible. All the

mountainous caves, Old buildings, abandoned wells, ruins, houses, tree groves and plantations

were thoroughly searched for bat roosts. Local people were also interviewed for gaining

information about the location of bat roosts. Once the information was received through

interviews of the locals, the exact location of each bat roost was searched and determined using a

global positioning system device (Garmin etrax H GPS).

Mist nets and hand nets were used to capture bat specimens. Each net was erected either in “L”

or “V” shape at strategic position on a pair of 3 m long bamboo poles in such a way that the last

shelf of each net remained one foot above the ground. The nets were ready to operate half an

hour before the sunset. All the nets were opened simultaneously at sunset and continued to

operate, depending on the weather conditions, for two hours after sunset. Nets were checked

continuously to disentangle any captured bat. The bats were disentangled from the nets as soon

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as they were trapped. Most of the trapped bats were released after their body measurements were

recorded using a digital vernier caliper (0-150 mm) following Bates and Harrison (1997). Only a

small sample was euthanized, placed in cotton bat bags, each specimen was weighed up to 0.1 g

(Pesola balance 10050, Swiss made) and brought to the laboratory for the preparation of their

skull and baculafollowing Bates et al. (2005) and Javid (2011). No juvenile was euthanized and

only mature specimens were used for further studies.


During present study, seventeen fulvous leaf - nosed bat were captured and external body, cranial

and bacular features of these specimens were compared with Roberts (1997) and Bates and

Harrison (1997), the only authentic sources on bats of the region. These specimens were captured

from Tura Gata (N34º 26.770′ E71º 49.090′) tehsil Dargai in Malakand district (Fig. 3.6.1). This

is a medium small size bat with very large ears reaching 22 mm, the tips of which were broadly

rounded off. The feet were small. The noseleaf has a greatest width of about 5mm. The noseleaf

was consisted of a naked brown skinned pad roughly square in outline. The pelage was variable

in color including dull yellow, pale grey, dull brown and golden-orange. Their ventral fur was

paler yellowish white. The tail was wholly enclosed by the inter-femoral membrane. The dental

formula of fulvous leaf - nosed bat was 1123/2123=30. Our findings are in line with Bates and

Harrison (1997) and Roberts (1997).

Average head and body length of all the 17 specimens captured during present study was 49.09 ±

1.16 mm, forearm length was 41.41 ± 0.97 mm, hind foot length was 8.57 ± 0.41 mm, ear length

was 22.37 ± 0.82 mm and the tail was 26.73 ± 1.48 mm long while according to Roberts (1997),

the average head and body length, forearm length, hind foot length, ear length and tail length was

44 mm, 8.0 mm, 8.0 mm, 21.0 mm and 27.0 m, respectively Table.3.6.1. All these measurements

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fall within the ranges given by Roberts (1997) and Bates and Harrison (1997). The mean body

mass of seventeen fulvous leaf - nosed bat was 8.53 ± 1.12 g while according to Medway (1969),

the mean body mass of the specimens from Afghanistan and Malayan was weighed 9 g and 8 to

10 g, respectively.Similarly, average length of 3rd

metacarpal, length of 4th

metacarpal and length

of 5th

metacarpal recorded during present study were 29.74 ± 0.68 mm, 31.52 ± 0.72 mm and

31.11 ± 0.62mm, respectively. Bates and Harrison (1997) recorded average length of 3rd

metacarpal 29.2 mm, 31.2 mm. and 30.8 mm. All these measurements, except length of 5th

metacarpal, which is slightly larger fall within the ranges given by Bates and Harrison (1997).

The upper incisors were more widely spaced from each other. The first upper premolar was

minute. The canine has a well definedcingulum internally and a broad base. These features are in

line with the findings of Bates and Harrison (1997). Average breadth of braincase of thirteen H.

fulvus captured during present study was 8.46 ± 0.18 mm, zygomatic breadth was 9.30 ± 0.19

mm, postorbital constriction 2.66 ± 0.11 mm, condylo-canine length 16.02 ± 0.22mm, greatest

length of skull 18.45 ± 0.16 mm, maxillary toothrow length 6.50 ± 0.14 mm, anterior palatal

width 3.89 ± 0.08 mm, posterior palatal width 6.52 ± 0.10 mm, mandibular toothrow length 6.96

± 0.18 mm and mandible length was 11.73 ± 0.14 mm (Table 3.6.1).According to Bates and

Harrison (1997), average breadth of braincase of H. fulvus which were captured from Indiawas

8.3 mm, zygomatic breadth 9.2 mm, postorbital constriction 2.5 mm, condyle-canine length 15.6

mm, greatest length of skull 18.0 mm, maxillary toothrow length 6.3 mm, Anterior palatal width

4.0 mm, posterior palatal width 6.3 mm, mandibular toothrow length 6.8 mm and mandible

length was 11.5 mm. All these measurements are comparable while average breadth of braincase,

mandibular toothrow length and mandible length of thirteen H. fulvus were within the ranges

mentioned by Bates and Harrison (1997).

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Average total length of baculum (n = 9) of H. fulvus captured during present study was 1.45 ±

0.07 mm, the shaft was 1.41 ± 0.07mm long while the height of baculum was 0.02 ± 0.01 mm

high. The width of proximal extreme, middle extreme and distal extreme was 0.01 ± 0.00 mm,

0.01 ± 0.01 mm and 0.02 ± 0.00mm, respectively (Table.3.6.1). The bacular features of the

species are reported for the first time in country.

Fig. 3.6.1. Distribution map of H. fulvus in Pakistan.

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Table 3.6.1. Comparison of external body, cranial and bacular measurements (mm) of Hipposideros fulvus captured during present study with Roberts

(1997), Bates and Harrison (1997) and Saikiaet al., (2006).

Body

Parameters

Present Study

(n=17)

Bates and

Harrison, 1997

Roberts, 1997 Saikiaet

al, 2006

Cranial

Parameters

Present Study

(n=13)

Bates and

Harrison, 1997

Saikiaet

al, 2006

BM 8.53±1.12 (5.00-10.00) - 8-10g - CCL 16.02±0.22 (15.52-16.21) 15.6±0.3 (15.0-16.4) 15.6

HB 49.09±1.16 (47.11-50.00) 47.0±3.0 (40.0-50.0) 44 (41-49) 43 CBL - - 16.3

E 22.37±0.82 (21.11-24.01) 22.0±1.3 (19.0-26.0) 21 (20-23) 20 CMn 6.50±0.14 (6.29-6.79) 6.3±0.2 (6.0-6.9) 6.5

FA 41.41±0.97 (40.02-43.02) 40.4±1.5 (38.4-44.0) 42.2 (38.8-43) 40.3 CMn 6.96±0.18 (6.73-7.38) 6.8±0.2 (6.4-7.5) 7.1

2mt 31.98±0.75 (31.01-33.02) - - - GTL 18.45±0.16 (18.16-18.60) 18.0±0.3 (17.2-18.6) 18.2

1ph2mt 15.28±0.73 (14.00-16.01) - - - M 11.73±0.14 (11.50-12.00) 11.5±0.3 (11.1-12.0) 11.5

3rd met 29.74±0.68 (28.01-31.11) 29.2±0.9 (27.3-31.2) - 31.2 Mn-Mn 6.52±0.10 (6.36-6.71) 6.3±0.2 (5.8-6.8) 7

1st Ph. 3rd met 17.89±0.31 (17.01-18.01) 17.5±0.8 (16.1-18.9) - - ZB 9.30±0.19 (8.80-9.49) 9.2±0.2 (8.6-9.6) 9.4

2nd Ph. 3rd met 17.87±0.71 (17.01-19.01) 18.0±0.8 (16.2-19.5) - - BB 8.46±0.18 (8.09-8.67) 8.3±0.5 (7.5-9.4) 8.1

4th met 31.52±0.72 (30.03-33.01) 31.2±1.1 (28.3-33.9) - - IC 2.66±0.11 (2.45-2.79) 2.5±0.1 (2.2-2.8) 2.7

1st Ph. 4th met 11.62±0.59 (10.01-12.00) 11.0±0.5 (10.0-12.0) - - Ci-Ci 3.89±0.08 (3.70-3.99) 4.0±0.2 (3.6-4.4) 4

2nd Ph. 4th met 9.86±0.32 (8.81-10.34) 9.6±0.7 (8.2-11.2) - - Bacular

Parameters

(n=9)

5th met 31.11±0.62 (30.04-32.14) 30.8±1.5 (28.7-33.1) - 30.7 TLB 1.45±0.07 (1.38-1.58) - -

1ph5mt 12.84±0.39 (12.01-13.03) - - - WPE 0.01±0.00 (0.01-0.01) - -

2ph5mt 12.00±0.44 (11.01-13.01) - - - WME 0.01±0.00 (0.01-0.01) - -

WS 271.18±6.14 (260.00-280.00) - - - WDE 0.02±0.00 (0.01-0.02) - -

TIB 19.61±0.49 (19.01-20.01) 18.5±1.0 (16.5-20.7) - 20 SL 1.41±0.07 (1.33-1.55) - -

HF 8.57±0.41 (7.88-9.04) 7.6±1.3 (6.0-9.8) 8 (5-9) 7.6 BH 0.02±0.01 (0.00-0.02) - -

T 26.73±1.48 (25.04-30.06) 29.5±3.0 (24.0-35.0) 27 (22-29) 25

n - The number of specimens; BM - Body mass; HB - Head and body; E - Ear; NLW- Nose leaf width; FA - Forearm; TH - Thumb; 2mt - 2nd metacarpal; 1ph2mt - 1st Phalanx on

2nd metacarpal; 2ph2mt - 2nd Phalanx on 2nd metacarpal; 3mt - 3rd metacarpal; 1ph3mt - 1st Phalanx on 3rd metacarpal; 2ph3mt - 2nd Phalanx on 3rd metacarpal; 4mt - 4th

metacarpal; 1ph4mt - 1st Phalanx on 4th metacarpal; 2ph4mt - 2nd Phalanx on 4th metacarpal; 5mt - 5th metacarpal; 1ph5mt - 1st phalanx on 5th metacarpal; 2ph5mt - 2nd

phalanx on 5th metacarpal; WS - Wing span; TIB - Tibia; CA - Calcar; HF - Hind foot.

CBL - Condylo-basal length; CCL - Condylo-canine length; CMn - Maxillary toothrow; CMn - Mandibular toothrow; GTL - Greatest length of skull; M - Mandible length; Mn-

Mn - Posterior palatal width; ZB - Zygomatic breadth; BB - Breadth of braincase; IC -Interorbital constriction; Ci-Ci - Anterior palatal width.

TLB - Total baculum length; WPE - Width of proximal extreme; WME - Width of middle extreme; WDE - Width of distal extreme; SL - Shaft length; PBL - Proximal branch

length; DBL - Distal branch length; PBW - Proximal branch Width; DBW - Distal branch width; BH - Baculum height

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Figure 3.6.2. A complete photograph (a) of Hipposideros fulvus (BatLab No. 87) captured from

Tura Gata in Malakand district, close up its face and hairy inner margins of the

ears (b) and, noseleaf (c) . Dorsal (d), ventral (e), lateral (f) views of the skull, and

dorsal (g) and lateral (h) view of mandible of this bat along with its baculum (i)

are also mentioned in this plate.

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117

REFERENCES

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Brosset, A. (1962). The Bats of Central and WesternIndia., III. J. Bombay Nat. Hist. Soc. 59: 1-

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Brosset, A. (1963). The bats of Central and Western India. Part IV. Journal Bombay Natural


Corbet, G. B. and J. E. Hill (1992). Mammals of the Indomalayan Region. A systematic review.

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Dobson, G. E. (1871). Description of four new species of Malayan bats…Proceedings Asiat.

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Gray, J. E. (1838). A revision of the genera of bats…Magazine Zool. Bot. 2:483-505.

Gray, J. E. (1831). Description of some new genera and species of bats. Zoological Miscellany

37-38. London.

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History Society‟s Mammal Survey of India, Burma and Ceylon.Journal of Bombay Natural

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biogeographic review. Proceedings of the VIIIth European Bat Research Society, 1: 157.

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Javid, A., Hassan M. M., Hussain, S. M., Iqbal, K. J. (2011). Recent record of the Asiatic lesser

yellow house bat (Scotophilus kuhlii) from Punjab, Pakistan. Mammalia, 78 (1): 133–137.

Lindsay, H. M. (1926). Report No. 40: Gwalior; Bombay Natural History Society‟s Mammal

Survey of India. Journal Bombay nat. Hist. Soc. 31: 379-382.

Mahmood-ul-Hassan, M., G. Jones and C. Dietz (2009).Bats of Pakistan. The least known

mammals.Verlag Dr. Muller. Saarbucken, Germany. Pp.168.

Medway, L., (1969). The wild Mammals of Malaya and offshore Islands including

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S. Molur, G. Marimuthu, C. Srinivasulu, S. Mistry, A. M. Hutson, P. J. J. Bates, S. Walker, K.

Padma Priya and A. R. Binu Priya (Editors) (2002). Status of South Asian Chiroptera:

Conservation Assessment and Management Plan (C.A.M.P.) Workshop Report, 2002. Zoo

Outreach Organisation, CBSG South Asia and WILD, Coimbatore, India, CD-Rom.

Roberts, T. J. (1997). Mammals of Pakistan. Revised Ed.Oxford Univ. Press. Oxford.

Saikia, U., Sharma, R. M., Sharma, D. K., (2006). Record of fulvus leaf-nosed bat from

HipposiderosfulvusGray 1838 from Jammu and Kashmir, India. Zoos‟ Print Journal, 21: 2197.

Siddiqi, M. S. (1961). Checklist of mammals of Pakistan with particular reference to the

mammalian collection in the British Museum (Natural History), London. Biologia, 7: 93-225.

Sinha, Y. P. (1980). The bats of Rajasthan: taxonomy and zoogeography. Records of the

Zoological Survey of India. 76: 7-63 pp.

Walker, S. and S. Molur (2003). Summary of the status of South Asian Chiroptera. Extracted

from C.A.M.P. 2002.Report.Zoo Outreach Organization.CBSG South Asia and Wild,

Coimbatore, India. 24pp.

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MammalSurvey of India, Burma and Ceylon. J. BombayNat. Hist. Soc. 24: 291–316.

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Two new bat species (Chiroptera: Mammalia) for Pakistan: Miniopterus fuliginosus and

Myotis formosus

*Corresponding author: Muhammad Mahmood-ul-Hassan, Department of Zoology and

Fisheries, University of Agriculture, Faisalabad 38040, Pakistan, e-mail:

[email protected]; [email protected]

Mohammad Salim: Department of Forestry and Wildlife Management, University of Haripur,

Haripur, Pakistan

(This manuscript has been published in Mammalia)

(Impact factor = 0.538)

Citation: Muhammad Mahmood-ul-Hassan and Mohammad Salim. Two new bat species

Chiroptera: Mammalia) for Pakistan: Miniopterus fuliginosus and Myotis

formosus. Mammalia, 79(1): 125-129.

Abstract

Although over 50 bat species have been recorded in Pakistan, more are expected to inhabit the

country. We recorded two new hitherto unrecorded bat species, i.e., Miniopterus fuliginosus and

Myotis formosus in northwestern Pakistan. M. fuliginosus was captured from Barcharai Daim

in Malakand district, while M. formosus was captured from Chinai Ghaz in Dir, Wach Khwar in

Swat and Barcharai Diam in Malakand districts, respectively. This paper describes external,

cranial, and bacular measurements of captured specimens of these two species.

Keywords: Hodgson‟s bat; long-fingered bat; morphology; new record; northwestern

Pakistan.

Intensive field efforts across the globe have raised the total number of bat species from 900 to

1200 in the last few years (S immons 2005). Although exploratory efforts are mostly focused in

the tropics and Southeast Asia, Pakistan still remains a poorly surveyed country (Mahmood-ul-

Hassan et al. 2009) . Most of the literature on bat species of Pakistan was generated during the

19th century, and no worthwhile effort has been made to explore its bat fauna so far. R oberts

(1997) has described 50 bat species belonging to 23 genera and eight families from Pakistan.

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120

Walker and Molur (2003) expected the presence of some additional bat species from the country.

Recent bat surveys in Punjab have revealed significant changes in their distribution ranges

(Mahmood-ul-Hassan et al. 2011, 2012, Javid et al. 2012a,b, 2014), but similar information is

missing from the northwestern and southwestern parts of the country. T hen, a yearlong bat

survey was conducted in three districts of Malakand Division, which is located between the

Himalayan and the Hindu Kush foothills and covers a broad altitudinal range. Various climatic

zones are identified according to increasing altitude: a) semi-arid-humidtemperate zone (450– 6

00 m), b) warm temperate zone (600 – 1100 m), c) temperate zone (1100 – 1500), d) cool

temperate zone (1500– 1 900 m), e) cold temperate zone (1900– 3 200 m), f) alpine pastures

(3200– 4 700 m), and g) snow and ice zone (4700 – 6300 m). B ats were captured using a 16 × 1

6-mm mesh sized and 2.5 m high mist net (Ecotone 716/12) erected 1 foot above the ground. The

net was operated from 19:00 to 20:30 h (Pakistan standard time) each night. Only one

Miniopterus and five Myotis were captured during three nights spent at Chinai Ghaz (35 °

00.850 ′ N, 72 ° 03.439 ′ E, 1154 m a.s.l.), Wach Khwar (34 ° 58.104 ′ N, 72 °2 8.270′ E,

1159 m), and Barchari Daim (34 °3 3.737′ N, 71 °4 4.872′ E, 851 m), respectively. External,

cranial, and bacular measurements of these specimens were recorded following Bates and

Harrison (1997) , Mahmood-ul-Hassan et al. (2011) , and Javid et al. (2012a,b). These revealed

to be hitherto unrecorded bat species in Pakistan. Miniopterus fuliginosus (Hodgson, 1835):

With the recent development of genetic analyses, many cryptic species have been identified

within the genus Miniopterus Bonaparte, 1837 across the World (e.g., Appleton et al. 2004 ,

Miller-Butterworth et al. 2005 , Bilgin et al. 2006 , Furman et al. 2010 , Š r á mek et al. 2013 ).

So, Tian et al. (2004) have shown that Asian populations of previous Miniopterus schreibersii

belong to a distinct species, M. fuliginosus as it was previously suggested by M aeda (1982). T

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he Eastern Schreiber‟s long-fingered bat Miniopterus fuliginosus captured at Barchari Daim (one

female) was recognized in the field on the basis of its small size (body mass: 11.5 g), its bulging

forehead, and its exceptionally long second phalanx of the third metacarpal, which was

approximately three times the length of the first phalanx ( Table 3.7.1 ). Wing membrane was

uniformly dark with a soft and silky dark pelage deep blackish brown dorsally and slightly paler

with a grayer tinge ventrally. Pelage on the forehead was short and dense and extended up to the

nostril pads. The cheeks were naked below the eyes. The tragus (5.66 mm) was almost half the

height of the pinna and slightly curved forward, while the antitragus (2.01 mm) was low.

Table 3.7.1. Wing measurements (mm) of Miniopterus fuliginosus (n = 1) and Myotis

formosus (n = 5) captured from Malakand Division, Pakistan.

Measurements M. fuliginosus M. formosus

Mean ±SD (Range)

Second metacarpal (2 mt) 42.72 43.93 ± 2.36

(41.69 – 47.57)

1st Phalange of 2

nd finger 3.21

3.25 ± 0.45

(2.71 – 3.95)

2nd

Phalange of 2nd

finger 6.63 16.30 ± 1.77

(14.45 – 18.32)

1st Phalange of 3

rd finger 12.25

18.77 ± 1.61

(17.40 – 21.49)

2nd

Phalange of 3rd

finger 32.96 15.47 ± 1.78

(14.28 – 18.62)

3rd

Phalange of 3rd

finger 8.04 6.00 ± 0.44

(5.35 – 6.51)

1st Phalange of 4

th finger 9.74

14.26 ± 0.99

(13.49 – 15.90)

2nd

Phalange of 4th

finger 17.52 12.19 ± 1.17

(10.56 – 13.42)

1st Phalanx on 5

th finger 10.73

13.88 ± 1.27

(12.31 – 15.83)

2nd

Phalange of 5th

finger 8.54 11.63 ± 0.86

(10.23 – 12.44)

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Table 3.7.2. Comparison of external body and cranioental measurements (mm) of Miniopterus

fuliginosus (n=1) and Myotis formosus (n=5) captured from Malakand Division (present

study) with Sramek et al. (2013) and Bates and Harrison (1997), respectively.

Species

Body parameters

M. fuliginosus (n=1) M. formosus (n=5)

Present Study

Mean±SD

(Range)

Šrámek et al.

2013 mean±SD(R

ange)

Present Study

Mean±SD (Range)

Bates and

Harrison 1997

Mean±SD

(Range)

Head and body 57.0 -

Tail 52.22 - 45.85±2.99 41.3±6.1

(40.83–47.92) (36.0–48.0)

Forearm 48.54 - 48.74±2.02 47.4±1.9

(46.66–52.03) (44.5–49.1)

Ear 13.49 - 18.27±1.09 13.6±0.9

(17.22–19.91) (12.8–14.5)

Hind foot 10.19 - 12.05±0.80 10.6±0.6

(10.99–12.75) (10.2–11.6)

Tibia 19.94 - 24.18±1.22 22.5±0.9

(22.96–26.19) (21.0–23.2)

3rd finger 43.11 - 44.26±1.15 44.3±1.1

(43.37–46.20) (43.2–45.7)

4th finger 41.42 - 43.94±1.81 43.1±0.8

(42.38–46.83) (42.3–44.0)

5th finger 38.04 - 43.97±1.70 43.5±1.3

(42.52–46.78) (42.3–47.2)

Greatest length of skull 15.61 15.636±0.254 17.81±0.12 18.4±0.4

(15.03–16.13) (17.71–17.94) (18.1–18.9)

Condylo-canine length 14.26 - 15.95±0.17 16.4±0.2

(15.75–16.05) (16.3–16.6)

Condylo-basal length 15.30 15.296±0.213 - -

(14.86–15.45)

Zygomatic breadth 8.49 8.919±0.184 - -

(8.57–9.30)

Braincase breadth 7.86 8.178±0.159 8.37±0.09 8.4±0.3

(7.75–8.51) (8.27–8.45) (8.1–8.7)

Postorbital constriction 3.94 3.928±0.083 4.51±0.09 4.5±0.1

(3.76-4.15) (4.41–4.57) (4.4–4.5)

Rostral breadth 4.82 4.720±0.118 5.09±0.12 5.1±0.2

(4.45–4.91) (4.95–5.17) (4.9–5.3)

Rostral breadth 6.66 6.713±0.135 7.75±0.30 7.6±0.2

(6.34–6.96) (7.55–8.10) (7.4–7.8)

Maxillary toothrow length 6.09 6.117±0.107 7.15±0.05 7.1±0.2

(5.89–6.34) (7.10–7.20) (6.8–7.2)

Mandible length 11.75 11.304±0.166 13.85±0.07 13.9±0.2

(11.00–11.60) (13.77–13.89) (13.7–14.1)

Mandibular toothrow length 6.68 6.507±0.113 7.80±0.05 7.4±0.2

(6.31–6.74) (7.75–7.84) (7.4–7.8)

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This bat had 36 teeth (dental formula: 2123/3133) (Figure 3.7.1). A comparison of the

craniodental parameters of this specimen (Table 3.7.2) with a population from eastern

Afghanistan (Šrámek et al. 2013) confirmed the identification of this specimen.

Historic records of Miniopterus from South Asia were considered a subspecies of Miniopterus

schreibersii (e.g., Bates and Harrison 1997 , Simmons 2005 ); they are now recognized as

Miniopterus schreibersii fuliginosus (Tian et al. 2004 , Srinivasulu and Srinivasulu 2012 ,

Šrámek et al. 2013). West of Pakistan M. fuliginosus has been recorded from eastern Afghanistan

(Gaisler 1970, Šrámek et al. 2013) and from northern Iran (Etemad 1969). This species has also

been recorded from Northern Myanmar to Nepal and India close to the northeastern part of

Pakistan (Bates and Harrison 1997). Although Roberts (1997) and other authorities (e.g., Walker

and Molur 2003, Mahmoodul-Hassan and Nameer 2006) expected its occurrence in Pakistan,

Brosset (1962) emitted a negative opinion on the basis of its habitat requirements. This record

ascertains that there are suitable microclimatic conditions for this species in some parts of

Pakistan.

Myotis formosus (Hodgson, 1835): The genus Myotis Kaup, 1892 is represented by 15 species

in the Indian Subcontinent and hitherto by three species in Pakistan, i.e., Myotis blythii , Myotis

nipalensis, Myotis muricola (Bates and Harrison 1997, Srinivasulu and Srinivasulu 2012) . The

five specimens captured at Chinai Ghaz (1, 2), Wach Khwar (1), and Barchari Diam (1) revealed

to belong to a fourth one, Myotis formosus.

These Hodgson‟s bats were readily identified by matching their photographs with the reference

(Bates and Harrison 1997). These medium-sized Myotis bats (body mass: 13.86 ± 1 .64 g) were

ginger brown dorsally with orange-brown flanks. The throat was lighter cinnamon brown, and

the ventral surface was orange in color. The whole body, except some areas around the eyes,

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124

nostrils, and lips, was hairy. Ears were relatively short, naked, and orange in appearance with

relatively darker margins. The tragus was long (8.77 ± 0 .88 mm), narrow, and obtusely pointed;

the antitragus (4.02 ± 0.48 mm) was almost half the length of tragus. Their broad wings (Table

3.7.1) had narrow orange colored lines alongside each of the metacarpals, while black triangular

areas were present between the metacarpals.

These black triangular areas were dotted and streaked with orange. The interfemoral membrane

was also orange (Figure 3.7.2A). The baculum of two specimens was extracted and measured (in

mm); total length: 0.78 ± 0 .04 (SD), shaft length: 0.65 ± 0 .11, proximal branch length: 0.01 ±

0.01, proximal branch width: 0.38 ± 0.04, width of proximal extreme: 0.51 ± 0.02, width of

distal extreme: 0.43 ± 0.07. These bats had 34 teeth (dental formula: 2132/3132) (Figure 3.7.2B–

D).

A comparison with other specimens from the Indian Subcontinent indicated that the Pakistanese

specimens had extraordinarily longer ears but slightly longer forearm, hind foot, and tail than

those recorded from India and Tibet (Table 3.7.2). On the contrary, the greatest length of the

skull and condyle-canine length was a bit smaller than those reported by Bates and Harrison

(1997) .

Widely distributed in northern India (Bates and Harrison 1997, Srinivasulu and Srinivasulu

2012), Myotis formosus formosus has also been reported from Kalat-us-Seraj, in the Nangarhar

province of Afghanistan (G aisler 1970). So this presence in Pakistan that should have been

foreseen confirms the western extension of a species, which possibly extends from northeastern

Pakistan along the Indian border to Kashmir and in the northwestern part of Pakistan including

Malakand Division.

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125

With these two newly recorded species, the bat fauna in Pakistan reaches to 55 species. Further

bat surveys are requested to record all species that were already reported close to Pakistan

borders, such as Myotis emarginatus and Myotis longipes (R oberts 1997, Walker and Molur

2003, Mahmood-ul-Hassan and Nameer 2006 ).

Acknowledgments: Financial assistance provided by the “Bat Conservation International” for

this study is gratefully acknowledged. We also thank Dr. Srinivasulu, Dr. Aulagnier, and an

anonymous referee for their improvement of the manuscript.

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126

Figure 3.7.1. Dorsal and lateral view of the skull (A, B) and lower jaw (C, D) of Miniopterus

fuliginosus captured from northwestern Pakistan.

Figure 3.7.2.A photographs of Myotis formosus showing its characteristic pelage coloration (A)

along with the dorsal (B), ventral (C), lateral (D)view of the skull and dorsal view

of the lower jaw (E).

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127

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of the bentwing bat complex Miniopterus schreibersii (Kuhl, 1817) (Chiroptera:

Vespertilionidae). Mol. Phylogenet. Evol. 31: 431 – 439. B ates, P.J.J. and D.L. Harrison. 1997.

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Bilgin, R., A. Karataş , E. Ç oraman, I. Pandurski, E. Papad-atou and J.C. Morales. 2006.

Molecular taxonomy and phylogeography of Miniopterus schreibersii (Kuhl, 1817) (Chiroptera:

Vespertilionidae), in the Eurasian Transition. Biol. J. Linn. Soc. 87: 577– 5 82.

Brosset, A. 1962. The bats of central and western India – part III. J. Bombay Nat. Hist. Soc. 59:

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Etemad, E. 1969. Psiandaran airan – khafa š ha. Khafa š hai [The bats of Iran, and the keys to

identify them]. University of Tehran, Tehran, Iran. pp. 201 [in Farsi, with a summary in English,

paginated separately, pp.25].

Furman, A., T. Ö ztunc and E. Ç o raman. 2010. On the phylogeny of Miniopterus schreibersii

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Miniopterus taxa (Chiroptera: Vespertilionidae). Acta Chiropterol. 12: 61 – 72.

Gaisler, J. 1970. The bats (Chiroptera) collected in Afghanistan by the Czechoslovak expeditions

of 1965 – 1967. Acta Sci. Nat. Brno 4: 1 – 56.

Javid, A., M. Mahmood-ul-Hassan, M. Afzal, M.S. Nadeem and S.M. Hussain. 2012a. Recent

record of the least pipistrelle Pipistrellus tenuis (Vespertilionidae: Chiroptera) from the Margalla

Hills National Park Pakistan. J. Anim. Plant Sci. 22: 1042– 1 047.

Javid, A., M. Mahmood-ul-Hassan, M.S. Nadeem, N. Rana and N. Khan. 2012b. First record of

the lesser mouse-tailed bat Rhinopoma hardwickii (Rhinopomatidae: Chiroptera) from southern

Punjab, Pakistan. J. Anim. Plant Sci. 22: 278 – 282.

Javid, A., M. Mahmood-ul-Hassan, S.M. Hussain and K.J. Iqbal. 2014. Recent record of the

lesser yellow house bat (Scotophilus kuhlii) from Punjab, Pakistan. Mammalia 78: 133 – 137.

Maeda, K. 1982. Studies on the classification of Miniopterus in Eurasia, Australia and

Melanesia. Honyurui Kagaku (Mammalian Science) Suppl. 1. Mammal Research Association,

Japan, pp. 1 – 176.

Mahmood-ul-Hassan, M. and P.O. Nameer. 2006. Diversity, role and threats to the survival of

bats in Pakistan. J. Anim. Plant Sci. 16: 38 – 42.

Mahmood-ul-Hassan, M., G. Jones and C. Dietz. 2009. Bats of Pakistan. The least known

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Mahmood-ul-Hassan, M., A. Javid, M. S. Nadeem and S. Ashraf. 2011. An extra-limital record

of Egyptian tomb bat Taphozous perforatus from Pakistan. Mammalia 76: 227 – 229.

Miller-Butterworth, C.M., G. Eick, D.S. Jacobs, M.C. Schoeman and E.H. Harley. 2005. Genetic

and phenotypic differences between South African long-fingered bats, with a global miniopterine

phylogeny. J. Mammal. 86: 1121 – 1135.

Roberts, T.J. 1997. Mammals of Pakistan. Revised edition. Oxford Univ. Press. Karachi,

Pakistan. pp. 525.

Simmons, N.B. 2005. Order Chiroptera. In: (D.E. Wilson and D.M. Reeder, eds.) Mammal

species of the World: a taxonomic and geographic reference. 3rd edition. The Johns Hopkins

University Press, Baltimore, MD. pp. 312 – 529.

Šrámek, J., V. Govž d í k and P. Benda. 2013. Hidden diversity in bent-winged bat (Chiroptera:

Miniopteridae) of the Western Palaearctic and adjacent regions: implications for taxonomy.

Zool. J. Linn. Soc. 167: 165 – 190.

Srinivasulu, C. and B. Srinivasulu. 2012. South Asian mammals, their diversity, distribution and

status. Springer, New York. NJ. pp. xii + 467.

Tian, L., B. Liang, K. Maeda, W. Metzner and S. Zhang. 2004. Molecular studies on the

classification of Miniopterus schreibersii (Chiroptera: Vespertilionidae) inferred from

mitochondrial cytochrome b gene sequences. Folia Zool. 53: 303 – 311.

Walker, S. and S. Molur. 2003. Summary of the status of South Asian Chiroptera. Extracted

from C.A.M.P. 2002. Report. Zoo Outreach Organization. CBSG South Asia and Wild,

Coimbatore, India. pp. 24.

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DIVERSITY OF SOME BAT SPECIES (FAMILY VESPERTILIONIDAE) FROM

MALAKAND DIVISION, PAKISTAN


2, Faiz-ur-Rahman

3 and FarmanUllah

4







(This paper has been submitted for publication in Mammalia journal)

ABSTRACT

A 3-year survey extending from 2010 through 2013 was conducted in three districts namely

Malakand, Dir and Swat was conducted to record the bat species belonging to the family

Vespertilionidae. During the survey, four species of bats the Asian barbastelle (Barbastella

leucomelas), the Asiatic greater yellow house bat (Scotophilus heathii), the Asiatic lesser yellow

house bat (Scotophilus kuhlii) and the serotine (Eptesicus serotinus) were recorded from the

study area. E. serotinus was captured from Dir and Malakand districts while B. leucomelas was

captured only from Dir district. S. heathii and S. kuhlii were captured only from Malakand

district. The forearm length of B. leucomelas, S. heathii, S. kuhlii and E. serotinus was 42.88

mm, 62.25±1.76 mm, 50.06±7.13 mm and 53.37±1.39 mm, respectively.

Key words: Barbastella; Scotophilus; Eptesicus, Malakand, Pakistan

INTRODUCTION

Bats play vital ecological roles in every ecosystem as insect predators, pollinators and seed

dispersers. Many tropical plant species depend entirely on bats for the distribution of their seeds.

Bats are the second largest order of mammals after rodents, with about 1240 bat species which

are present throughout the world with the exception of extremely cold regions. About 70 % of

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130

bats species are insectivores. Microbats are highly specialized by emitting sound of high

frequency and they use echolocation for navigation and foraging (or hunting) in many

environments.

Asian Barbastelle Barbastella leucomelas (CRETZSCHMAR, 1830/31):

Present limited evidences indicate that this bat is associated with forests in the northern mountain

regions, either Himalayan moist or dry coniferous forest. Since this species is not gregarious in

its diurnal roosts it is never very plentiful throughout its range and the paucity of Pakistan

specimens indicates that it is uncommon if not rare. Ellerman and Morrison-Scott (1951) include

Gilgit and the Punjab within its range on the basis of reports by Blanford but there are no

specimens in the British museum or Bombay Natural History museum collections from Gilgit.

However a specimen were collected at Dunga Gali in 1907 at 2350 m (7800 ft) and a second

mummified specimen in the same location by the author on 2 May 1980. A third specimen was

collected in 1965 by the University of Maryland expedition from Naltar, Gilgit, in spruce forests

(Picea smithiana), at about 2450 m (8000 ft) elevation. Siddique does not include this specimen

in either of his checklists (1961, 1970). It was collected from Afghanistan in Paktia Province

(Meyer-Oehme, 1965) and from several localities in northern Iran (Etemad, 1969). Elsewhere it

occurs in Russian Turkestan and Chinese Xinjiang and Trans-Caucasia (Bobrinskii et al. 1965)

and southern China and north to Japan (Corbet and Hill, 1992). In India it occurs in Darjeeling,

Nepal Sikkim and the Bhutan Duars.


Scotophilus heathii is geographically distributed in Afghanistan to South China, including

Hainan Isl, south to Sri Lanka, Vietnam, Cambodia, Thailand and Burma. In Pakistan the species

is common and widespread throughout the Indus plains. It has been collected from Kohat

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(NWFP), Islamabad city, Multan, Lahore and Sialkot districts (Punjab), Kashmoor, Sakkur,

Jacobabad, Mirpur Sakro, Dadu, Landi, Malir, Karachi (Sindh) (Wroughton, 1916; Lindsay,

1926; Taber et al. 1967; Walton, 1974; Roberts, 1997).

Asiatic Lesser Yellow House Bat Scotophilus kuhlii Leach, 1821

The average forearm length was 49.0 mm (44.0 - 56.4 mm). It can only be distinguished from S.

heathii by its small size. The pelage is chesnut brown above, paler below but usually without the

characteristic yellowish tinge of S. heathii. It is uncommon in Pakistan with a very restricted

distribution.The species is present only in southern Sindh (Roberts, 1997). Geographiccaly this

species is distributed in Bangladesh, Pakistan to Taiwan, south to Sri Lanka, Burma, Cambodia,

W Malaysia, Java, Bali, Nusa Tenggara (Indonesia), southeast to Philippines and Aru Isles

(Indonesia) (Mahmood-ul-Hassan et al. 2009).

Serotine Eptesicus serotinus (SCHREBER, 1774)

This species is rare in Pakistan. Literature survey revealed that only two specimens have been

collected from the country. One of these was collected from Astor district near Karakar Pass in

1908 (Bates and Harrison, 1997) while the other (Male specimen) was collected by Roberts

(1997) in 1971 from Dunga Gali in Murree Hills. The species is expected to be present in Gilgit,

Swat and Chitral (Roberts, 1997). Walker and Molur, 2003 declare this species to be Data

Deficient, Near Threatened (C.A.M.P. Report, 2002) and Least Concern according to IUCN

2008 Red List of Threatened Animals. E. s. pashtomus was described as a new subspecies by

Gaisler (1970) in his account of bats collected in Afghanistan from Jalalabad district. The

zygomatic width of pashtomus being 14.5 mm while Felten (1971) in describing a further

collection of bats from Afghanistan also assigned E. serotinus to the subspecies pashtomus

which was collected from eastern Afghanistan close to the border with Chitral (Felten, 1971).

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Sampling strategy

A 3-year survey extending from 2010 through 2013 was conducted in three districts Malakand,

Dir and Swat of Malakand division, Khyber Pakhtunkhwa province, Pakistan. Field visits were

made to locate as many bat roosts as possible and almost all the mountainous caves were

searched. Local people were also interviewed for gaining information about the location of

various bat roosts. Once the information was received through interviews of the locals, the exact

location of each bat roost was searched and determined using a global positioning system device

(Garmin etrax H GPS). Cave bats were captured using a hand made net (diameter 0.46 m and

pole length 1.83 m). Mist nets were also used to capture bat in open from various localities. A

total of six viz., 12 m (n = 1), 9 m (n =2) and 6 m (n = 3) long high quality, deep black, UV

stable and strong mist nets (Ecotone 716/6, 716/9 and 716/12) were used to capture bats. Each of

these five shelved, 16×16 mm mesh sized and 2.5 m high net was erected either in “L” or “V”

shape at strategic positions on a pair of 3 m long bamboo poles in such a way that the last shelf

of each net remained one foot above the ground. Mist nets were not used regularly however

when used the total mistnetting area (120 m2) was kept the same. The nets were ready to operate

half an hour before the sunset. All the nets were opened simultaneously at sunset and continued

to operate, depending on the weather conditions, for two hours after sunset. Nets were checked

continuously to disentangle any captured bat. The bats were disentangled from the nets as soon

as they were trapped. Most of the trapped bats were released after their body and weight external

body measurements were recorded. Only a small sample was euthanized for the preparation of

their skull. No juvenile was euthanized and only mature specimens were used for further studies.

Most of the females were also released alive.

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Morphometry

Each captured bat was placed in a separate cotton bag, weighed up to 0.1 g (Pesola balance

10050, Swiss made) in the field and numbered after recording their body measurements. A small

proportion of the bats was euthanized and preserved in absolute alcohol. Only the adults and

specifically the males were euthanized while majority of the adult females were released. The

number of euthanized bats was intentionally kept low to avoid unnecessary killing. Field

number, sex, age, exact locality and district of capture of each bat were noted on the plastic

bottle containing absolute alcohol. After three consecutive nights of mist netting at each station,

the catch was brought to the laboratory at the end of each month. Measurements were taken

using a digital vernier caliper (0-150 mm) following Bates and Harrison (1997). For cranial and

bacular measurements, the skulls and bacula were prepared and measured following Bates et al.

(2005).


Asian Barbastelle Barbastella leucomelas (CRETZSCHMAR, 1830/31):

Only a single specimen was captured from Lamin Bala (N35º 27.802′ E72º 14.310′) in Upper Dir

district during this study (Fig.3.8.1a). This is rather a small and delicately built bat with a very

striking body colour. The dorsal fur is long and silky and of a blackish grey colour basally, with

the extreme tips of hairs a pale golden brown giving it a hoary appearance. The belly fur is paler

grayish brown. The ears are large and conspicuous being rather a squarish in outline and forward

slanting. The tragus is half the height of the ear and triangular in shape. The posterior margin of

the ear lack any projections or notches as in Barbastella barbastellus. There is an extensive inter

femoral membrane with a rather small calcar and inconspicuous lobe below the calcar. The

dorsal surface of the hair is sparsely haired and shows two dark lines or veins extending from the

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heel of the hind foot up to the base of the pelvis. The dental formula of Asian Barbastelle was

2123/3123=34. The body mass, head and body length and ear length of a single Aisian

Barbastelle was 9.20 g, 51.00 mm and 15.87 mm, respectively (Table 3.8.1). Thumb and forearm

length was 5.65 mm and 42.88 mm, respectively. The tragus height was 10.32 mm. The length of

2nd

metacarpal was 40.14 mm. The length of 1st and 2

nd phalanx on 2

nd metacarpal was 2.01 mm,

2.96 mm. The length of 3rd

metacarpal was 41.45 mm while that of 1st, 2

nd and 3

rd phalanx on 3

rd

metacarpal was 15.16 mm, 17.84 mm and was 6.86 mm, respectively. The length of 4th


nd phalanges on 4

th metacarpal was 12.71 mm

and 12.36 mm, respectively. The length of 5th

metacarpal was 37.33 mm while that of 1st and 2

nd

phalanx on 5th

metacarpal was 12.84 mm and 8.39 mm, respectively. The wing span was 300.00

mm. Their tibia, calcar, hind foot and tail were 20.43 mm, 13.42 mm, 7.35 mm and 46.34 mm,

respectively (Table 3.8.1). The skull of an Aisian Barbastelle captured from Lamin Bala (BatLab

No. 261) is shown in Fig. 3.8.1b. The greatest length of skull, breadth of braincase, zygomatic

bone and condylo-canine length of a single specimen was 15.87 mm, 7.53 mm, 7.59 mm

and14.19 mm, respectively. The post-orbital constriction was 3.98 mm long. Anterior and

posterior palatal width measured was 2.39 mm and 5.61 mm, respectively. The maxillary

toothrow length, mandibular toothrow length and mandible length was 4.91 mm, 5.43 mm

and10.02 mm, respectively (Table 3.8.2).

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Fig. 3.5.1. A close-up of the face (a) showing elongated ears and tragus of the eastern

barbastelle and dorsal (b), ventral (c), and lateral view (d) of the skull and lower

jaw (e).


Twenty two bats were captured through mist net in Head Koper (N34º24.454′ E71º50.061′),

Bazdara Bala (N34º 30.355′ E72º04.692′), Malakand Top (N34º34.007′ E71º55.736′), Batkhela

(N34º36.903′ E71º57.768′) and Daim (N34º36.647′ E71º47.704′) in Malakand district during this

study. The tail is long, with only the terminal 2-3 mm projecting free from the interfemoral

membrane. The muzzle is broad and blunt; it is swollen on the sides, dark in colour and most

naked. The nostrils are simple in form, round and slightly outward facing. The ears are small in

relation to the size of the head; they are naked and have a number of transverse ridges. The

antitragus of each ear is well formed and separated from the posterior margin of the pinna by a

distinct notch. The tragus is half the height of the pinna and crecent shaped. The pelage is fine

and short; it is longer on the nape of the neck and throat. The head and back have pale buffy

brown hair roots and darker olive-grey-brown tips; the nape of the neck is paler. The throat, chest

and belly are pale yellow-buff throughout. The interfemoral membrane and wings are uniformly

dark brown and essentially naked, except for some hairs adjacent to the body and forearm on the

ventral surface of each wing. In the wing, the third metacarpal slightly exceeds the fourth and

fifth in length. The feet are about half the length of the tibiae. The dental formula was

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136

1113/3123=30. The mean body mass of Asiatic Greater Yellow House Bat (n=22) was 43.30±

7.91 g (Table 3.8.1). Their head and body length and ear length was 84.61 ± 2.71 mm and 17.26

± 1.14 mm, respectively. Mean thumb and forearm length was 9.06 ± 0.41 mm and 62.25 ± 1.76

mm, respectively. The tragus and anti-tragus height was 8.69 ± 0.81 mm and 3.71 ± 0.47 mm,

respectively. The length of 2nd

metacarpal, 1st and 2

nd phalanx on 2

nd metacarpal was 59.40 ±

1.37 mm, 5.80 ± 0.73 mm and 14.04 ± 0.85 mm, respectively. The mean length of 3rd

metacarpal, 1st, 2

nd and 3

rd phalanges on 3

rd metacarpal were 60.80 ± 1.46 mm, 20.00 ± 0.90 mm,

16.27 ± 0.70 mm and10.63 ± 0.77 mm, respectively. The mean length of 4th

metacarpal, 1st and

2nd

phalanges on 4th

metacarpal was 59.53 ± 1.49 mm, 15.81 ± 1.48 mm and 12.91 ± 0.92 mm,

respectively. The mean length of 5th


nd phalanx on 5

th metacarpal was 56.02

± 1.59 mm, 11.08 ± 0.58 mm and 9.42 ± 0.56 mm, respectively. The mean wing span, tibia,

calcar, tail and hind foot was 39.05 ± 3.63 mm, 26.83 ± 1.66 mm, 18.88 ± 2.33 mm, 53.02 ± 3.79

mm and 12.48 ± 0.73 mm, respectively (Table 3.8.1). The skull of Asiatic Greater Yellow House

Bat captured from Head Koper (Bat Lab No. 109) is shown in Fig. 3.8.2. The mean greatest

length of skull, breadth of braincase, zygomatic breadth, post-orbital constriction and condylo-

canine length of the nine specimens was 23.12 ± 0.46 mm, 10.38 ± 0.28 mm, 15.55 ± 0.31 mm,

5.49 ± 0.18 mm and 20.62 ± 0.28 mm, respectively. Anterior and posterior palatal widths

measured 7.62 ± 0.21 mm and 9.88 ± 0.28 mm, respectively. The maxillary toothrow length,

mandibular toothrow length and mandible length was 7.87 ± 0.16 mm, 8.93 ± 0.16 mm and16.62

± 0.19 mm, respectively (Table 3.8.2). Total baculum length and shaft length of five specimens

was 1.74 ± 0.12 mm and 1.42 ± 0.14 mm, respectively. The proximal branch length, distal

branch length, proximal branch width and distal branch width was 0.02 ± 0.01 mm, 0.01 ± 0.00

mm, 0.79 ± 0.23 mm and 0.58 ± 0.17 mm. The width of proximal extreme, width of distal

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extreme and width of middle extreme was 0.88 ± 0.14 mm, 0.83 ± 0.07 mm and 0.79 ± 0.11 mm

respectively. The bacula was 0.29 ± 0.03 mm high (Table 3.8.3, Fig. 3.8.2g).

Fig.3.8.2. A Scotophilus heathii captured in the hand (a), its dorsal (b) ventral (c), and

lateral (d), view of the skull. The dorsal (e) and lateral (f) view of lower jaw and

its baculum (g) are also shown in this picture.

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Asiatic Lesser Yellow House Bat Scotophilus kuhlii LEACH, 1821

Two bats were captured through mist net in Head Koper (N34º 24.454′ E71º 50.061′) and Kot

(N34º 29.778′ E71º 43.501′) in Malakand district during this study. It,s small in size than

Scotophilus heathii. The pelage is chestnut brown above; paler below but usually without the

characteristic yellowish tinge of S. heathii. The dental formula was 1113/3123=30. The mean

body mass, head and body, ear, thumb and forearm length of two Asiatic Lesser Yellow House

Bats was 14.50 ± 2.12 g, 66.13 ± 2.81 mm, 14.61 ± 2.11 mm, 7.01 mm ± 1.41 (SD) and 50.06 ±

7.13 mm, respectively. The tragus and anti-tragus height was 7.52 ± 0.71 mm and 3.52 ± 0.70

mm respectively. The length of 2nd


nd phalanx was on 2

nd metacarpal was

45.06 ± 0.06 mm, 5.03 ± 1.42 mm and 11.01 ± 1.41 mm, respectively. The mean length of 3rd

metacarpal was 45.58 ± 0.76 mm while that of 1st, 2

nd and 3

rd phalanges on 3

rd metacarpal were

13.03 ± 1.42 mm, 9.54 ± 0.70 mm and 8.02 ± 0.01 mm, respectively. The mean length of 4th


nd phalanges on 4

th metacarpal was 44.61 ± 0.69 mm, 11.52 ± 0.71 mm and

9.02 ± 0.01 mm, respectively. The mean length of 5th


nd phalanx on 5

th

metacarpal was 42.61 ± 0.71 mm, 9.02 ± 0.01 mm and 7.57 ± 0.63 mm, respectively. The mean

wing span, tibia, calcar, tail and hind foot was 496.02 ± 1.43 mm, 20.51 ± 0.71 mm, 13.52 ± 2.11

mm 40.61 ± 0.69 mm and 10.56 ± 0.64 mm, respectively (Table 3.8.1). The skull of an Asiatic

Lesser Yellow House Bats captured from Head Koper (BatLab No. 71) is shown in Fig. 3.8.3a.

The mean greatest length of skull, breadth of braincase, zygomatic breadth and condylo-canine

length of the two specimens was 19.24 ± 0.71 mm, 8.81 ± 0.01 mm, 12.63 ± 0.26 mm and 17.41

± 0.83 mm, respectively. The post-orbital constriction, anterior and posterior palatal width was

4.67 ± 0.03 mm, 6.12 ± 0.01 mm and 8.15 ± 0.04 mm, respectively. The maxillary toothrow

length, mandibular toothrow length and mandible length was 6.49 ± 0.11 mm, 7.42 ± 0.01 mm

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and 13.78 ± 0.47 mm (Table 3.8.2). Total baculum length, shaft length, proximal branch length,

proximal branch width, distal branch width, width of proximal extreme and width of distal

extreme of two specimens was 1.20 ± 0.25 mm, 1.08 ± 0.21 mm, 0.01 ± 0.00 mm, 0.02 ± 0.00

mm, 0.54 ± 0.05 mm, 0.51 ± 0.02 mm and 0.61 ± 0.02 mm, respectively (Table 3.8.3, Fig.3.8.4).

Fig. 3.8.3. Dorsal (a), ventral (b) and lateral (c) view of the skull of Scotophilus kuhlii. The

dorsal (e) and lateral view of the lower jaw are also given in the same plate.

Fig. 3.8.4. A photograph of the stained baculum of Scotophilus kuhlii.

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Serotine Eptesicus serotinus (SCHREBER, 1774)

Fifteen bats were captured through mist net in Head Koper (N34º 24.454′ E71º 50.061′), Bakrai

(N34º 23.939′ E71º 52.202′), Astanadaro Kalay (N34º 24.913′ E71º 49.466′), Barcharai Daim

(N34º 33.737′ E71º 44.872′), Amlok Dara (N34º 43.773′ E71º 52.502′) and Pull Saokai (N34º

38.553′ E72º 01.749′) in Malakand division during this study. This is a large Eptesicus. The tail

is long with its tip protruding from the interfemoral membrane for about 5 mm. the glandular

swellings of the muzzle are black and nearly naked; the upper lip is fringed with fine hairs. The

ears are dark, moderately tall and with about six transverse ridges. The anterior border of each

ear has a strong, almost angular convexity just below half of its height and is nearly straight

above to the rounded-off tip; the posterior border is almost straight beneath the tip and then

convex below, where it is inserted at the base of the antitragal lobe. The tragus is less than half

the height of the pinna; its anterior border is straight, the tip is bluntly pointed and the posterior

border gently convex, with a distinct notch just above the basal lobe. The wings are broad in

relation to their length; the fifth metacarpal is shorter than the third and fourth. The wing

membranes are inserted on the base of the outer toe of each foot. The interfemoral and wing

membranes are uniformly dark brown/black. The upper surface of the interfemoral membrane is

lightly haired adjacent to the body and femora; there are also a few hairs on the ventral surface of

each wing alongside the forearm. In general, the pelage is fine, dense and silky with a distinct

gloss on the back. The dorsal surface is essentially dark brown, although in some individuals

there is a golden tinge on the head and shoulders and/or a light frosting of paler hair tips. The

throat and belly are paler, a uniform grey in some individuals, buffy grey in others, the hair bases

are usually dark above and below. The baculum is very small with a simple tip and bilobate base.

The dental formula was 2112/3123=32. The mean body mass, head and body length, ear length,

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thumb and forearm length of fifteen serotine was 22.23 ± 4.18 g, 69.80 ± 5.10 mm, 19.65 ± 0.96

mm, 8.92 ± 0.32 mm and 53.37 ± 1.39 mm, respectively (Table 3.8.1). The tragus and anti-tragus

height was 8.27 ± 0.10 mm and 3.94 ± 0.08 mm, respectively. The length of 2nd

metacarpal, 1st

and 2nd

phalanx on 2nd

metacarpal was 48.93 ± 2.33 mm, 4.33 ± 0.38 mm and 14.65 ± 1.58 mm,

respectively. The mean length of 3rd

metacarpal, 1st, 2

nd and 3

rd phalanges on 3

rd metacarpal was

50.51 ± 2.13 mm, 19.00 ± 1.77 mm, 16.48 ± 1.49 mm and 9.93 ± 1.09 mm, respectively. The

mean length of 4th


nd phalanges on 4

th metacarpal was 49.74 ± 2.95 mm,

16.95 ± 1.44 mm and 13.09 ± 1.58 mm, respectively. The mean length of 5th

metacarpal was

48.13 mm ± 1.99 (SD) while that of 1st and 2

nd phalanx on 5

th metacarpal was 13.45 ± 0.71 mm

and 9.01 ± 0.66 mm, respectively. The mean wing span, tibia, calcar, tail and hind foot was

364.27 ± 17.43 mm, 22.92 ± 0.77 mm, 14.21 ± 1.96 mm, 49.74 ± 2.99 mm and 11.36 ± 0.77 mm,

respectively (Table 3.8.1). The skull of an Serotine captured from Head Koper (BatLab No. 121)

is shown in Fig.3.8.5. The mean greatest length of skull, breadth of braincase, post-orbital

constriction and condylo-canine length of the fifteen specimens was 21.40 ± 0.70 mm, 9.69 ±

0.22 mm, 4.72 ± 0.14 mm and 19.13 ± 0.54 mm, respectively. (SD). Anterior and posterior

palatal width measured 6.60 ± 0.27 mm and 9.06 ± 0.29 mm, respectively. The maxillary

toothrow length, mandibular toothrow length and mandible length was 7.84 ± 0.21 mm, 9.28 ±

1.95 mm 15.51 ± 1.94 mm (Table 3.8.2. Fig.3.8.5). Total baculum length, shaft length, width of

proximal extreme and distal branch width of seven specimens was 1.00 ± 0.15 mm, 0.89 ± 0.13

mm, 0.59 ± 0.06 mm and 0.14 ± 0.16 mm (Table 3.8.3, Fig.3.8.6).

Identification of bats was carried out analyzing the external features, cranial and bacular

measurements. In addition to this dental formula was used along with the external measurements

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142

for confirmation. The data were compared with Roberts (1997), Bates and Harrison (1997),

Srinivasulu et al. (2010), Javid et al (2014) and Shahbaz et al. (2014).

Fig.3.8.5. Dorsal (a), ventral (b) and lateral (c) view of the skull of Eptesicus serotinus. The


Fig. 3.8.6. A photograph of the stained baculum of Eptesicus serotinus.

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Table 3.8.1. External body measurements (mm) of four species of family Vespertilionidae captured from Malakand Division.

Body Parameters Barbastella leucomelas (n=1) Mean±SD (Range)

Scotophilus heathii (n=22) Scotophilus kuhlii (n=2) Eptesicus

Serotinus (n=15)

Body mass 9.20 43.30±7.91 29.40-70.00 14.50±2.12 13.00-16.00 22.23±4.18 15.40-27.80

Head and body 51.00 84.61±2.71 80.12-90.12 66.13±2.81 64.14-68.11 69.80±5.10 60.00-76.00

Ear 15.87 17.26±1.14 15.01-19.14 14.61±2.11 13.12-16.10 19.65±0.96 17.05-21.12

Tragus height 10.32 8.69±0.81 7.05-10.00 7.52±0.71 7.01-8.02 8.27±0.10 8.01-8.39

Antitragus 3.71±0.47 3.01-4.10 3.52±0.70 3.02-4.01 3.94±0.08 3.81-4.12

Forearm 42.88 62.25±1.76 58.12-65.01 50.06±7.13 45.01-55.10 53.37±1.39 50.10-55.13

Thumb with claw 5.65 9.06±0.41 8.12-10.01 7.01±1.41 6.01-8.01 8.92±0.32 8.52-9.46

2nd

metacarpal 40.14 59.40±1.37 56.12-61.01 45.06±0.06 45.02-45.10 48.93±2.33 45.51-52.69

1st Phalanx on 2

nd metacarpal 2.01 5.80±0.73 5.01-7.00 5.03±1.42 4.02-6.03 4.33±0.38 3.74-4.93

2nd

Phalanx on 2nd

metacarpal 2.96 14.04±0.85 13.01-15.02 11.01±1.41 10.01-12.01 14.65±1.58 12.55-17.30

3rd

metacarpal 41.45 60.80±1.46 58.22-64.01 45.58±0.76 45.04-46.11 50.51±2.13 46.45-53.70

1st Phalanx on 3

rd metacarpal 15.16 20.00±0.90 19.01-22.01 13.03±1.42 12.02-14.03 19.00±1.77 15.57-22.36

2nd

Phalanx on 3rd

metacarpal 17.84 16.27±0.70 14.12-17.02 9.54±0.70 9.04-10.03 16.48±1.49 13.56-18.86

3rd

phalanx on 3rd

metacarpal 6.86 10.63±0.77 9.13-12.01 8.02±0.01 8.02-88.01 9.93±1.09 7.85-11.01

4th

metacarpal 38.55 59.53±1.49 57.10-62.14 44.61±0.69 44.12-45.10 49.74±2.95 43.45-53.66

1st Phalanx on 4

th metacarpal 12.71 15.81±1.48 10.05-17.01 11.52±0.71 11.01-12.02 16.95±1.44 14.52-19.62

2nd

Phalanx on 4th

metacarpal 12.36 12.91±0.92 11.04-14.01 9.02±0.01 9.01-9.02 13.09±1.58 10.96-15.51

5th

metacarpal 37.33 56.02±1.59 53.13-59.01 42.61±0.71 42.10-43.11 48.13±1.99 43.98-51.46

1st phalanx on 5

th metacarpal 12.84 11.08±0.58 10.11-12.01 9.02±0.01 9.01-9.02 13.45±0.71 12.56-14.86

2nd

phalanx on 5th

metacarpal 8.39 9.42±0.56 8.55-11.10 7.57±0.63 7.12-8.01 9.01±0.66 8.25-10.11

Wing span 300.00 39.05±3.63 28.20-44.50 496.02±1.43 495.01-497.03 364.27±17.43 320.00-390.00

Tibia 20.43 26.83±1.66 21.15-29.10 20.51±0.71 20.01-21.01 22.92±0.77 21.56-24.21

Calcar 13.42 18.88±2.33 13.23-23.13 13.52±2.11 12.02-15.01 14.21±1.96 10.76-17.45

Hind Foot 7.35 12.48±0.73 11.10-14.01 10.56±0.64 10.11-11.01 11.36±0.77 10.25-13.07

Tail 46.34 53.02±3.79 45.30-65.30 40.61±0.69 40.12-41.10 49.74±2.99 45.45-54.47

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Table 3.8.2. Cranial measurements (mm) of four species of family Vespertilionidae captured from Malakand Division.

Cranial

Measurements

Barbastella leucomelas

(n=1)

Mean±SD (Range)

Scotophilus heathii (n=10) Scotophilus kuhlii

(n=2)

Eptesicus Serotinus (n=15)

Condylo-canine length 14.19 20.62±0.28 20.22-21.02 17.41±0.83 16.82-18.00 19.13±0.54 18.32-20.07

Condylobasal length 15.05 20.96±0.44 20.36-21.82 - - - -

Maxillary toothrow 4.91 7.87±0.16 7.55-8.06 6.49±0.11 6.41-6.57 7.84±0.21 7.54-8.16

Mandibular toothrow 5.43 8.93±0.16 8.76-9.22 7.42±0.01 7.41-7.43 9.28±1.95 8.26-16.17

Greatest length of skull 15.87 23.12±0.46 22.20-23.79 19.24±0.71 18.74-19.74 21.40±0.70 20.24-22.65

Mandible length 10.02 16.62±0.19 16.25-16.86 13.78±0.47 13.44-14.11 15.51±1.94 8.73-16.92

Posterior palatal width 5.61 9.88±0.28 9.46-10.39 8.15±0.04 8.12-8.18 9.06±0.29 8.45-9.59

Zygomatic breadth 7.59 15.55±0.31 15.26-16.25 12.63±0.26 12.44-12.81 14.32±0.68 13.25-15.27

Breadth of braincase 7.53 10.38±0.28 9.77-10.70 8.81±0.01 8.80-8.82 9.69±0.22 9.33-10.05

Postorbital constriction 3.98 5.49±0.18 5.22-5.86 4.67±0.03 4.65-4.69 4.72±0.14 4.50-4.94

Anterior palatal width 2.39 7.62±0.21 7.36-8.04 6.12±0.01 6.11-6.12 6.60±0.27 6.03-6.93

Table 3.8.3. Mean bacular measurements (mm) of three species of family Vespertilionidae captured from Malakand Division.

Bacular Parameters

Mean± SD (Range)

Scotophilus heathii (n=5) Scotophilus kuhlii

(n=2)

Eptesicus serotinus

(n=7)

Total baculum length 1.74±0.12 1.58-1.88 1.20±0.25 1.03-1.38 1.00±0.15 0.73-1.15

Shaft length 1.42±0.14 1.18-1.55 1.08±0.21 0.93-1.23 0.89±0.13 0.68-1.08

Proximal branch length 0.02±0.01 0.01-0.02 0.01±0.00 0.01-0.01 - -

Distal branch length 0.01±0.00 0.01-0.01 0.01±0.00 0.01-0.02 - -

Proximal branch Width 0.79±0.23 0.55-1.08 0.02±0.00 0.02-0.02 - -

Distal branch width 0.58±0.17 0.43-0.83 0.54±0.05 0.50-0.58 0.14±0.16 0.01-0.33

Width of proximal extreme 0.88±0.14 0.73-1.08 0.51±0.02 0.50-0.53 0.59±0.06 0.50-0.65

Width of middle extreme 0.79±0.11 0.65-0.90 - - - -

Width of distal extreme 0.83±0.07 0.75-0.93 0.61±0.02 0.60-0.63 - -

Baculum height 0.29±0.03 0.25-0.33 - - - -

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Ellerman, J. R. and T. C. S. Morrison-Scott. 1951. Checklist of Palearctic and Indian Mammals

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Etemad, E. 1969. Notes on bats from Iran. Mammalia, 31: 275-280.

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Vespertilionidae). Senckenbergiana Biologica, 52(6): 371-376.


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Horsfield, T. 1831. Observations on two species of bats from Madras….Proceedings Zool. Soc.

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Javid, A., M. Mahmood-Ul-Hassan, S. M. Hussain and K. J. Iqbal. 2014. Recent record of the

Asiatic lesser yellow house bat (Scotophilus kuhlii) from Punjab, PakistanMammalia, 78: 133-

137.

Kunz, T. H. 1988. Ecological and behavioural methods for the study of bats. Washington:

Smithsonian Institution Press.

Leach, W. E. 1821. The character of three new genera of bats without foliaceous appendages to

the nose. Transactions Linn. Soc.Lond. 13: 69-72.


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Lidicker, W. and Yang, A. 1986. Morphology of the penis in the Taiga vole (Microtus

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Mahmood-ul-Hassan, M., G. Jones and C. Dietz. 2009. Bats of Pakistan. The least known

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Meyer-Oehme, D.A. Von. 1965. Die Saugetiere Afghanistans (Teil 3) Chiroptera, Science,

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MORPHOLOGICAL FEATURES OF THE BATS OF GENUS PIPISTRELLUS FROM

MALAKAND DIVISION, KHYBER PAKHTUNKHWA, PAKISTAN


2, Faiz-ur-Rahman

3 and FarmanUllah

4







(This paper has been submitted for publication in Mammalia journal)

ABSTRACT

A 3-year survey, extending from 2010 through 2013 was conducted at Malakand division in

Khyber Pakhtunkhwa (KP), Pakistan to ascertain the presence of species belonging to the genus

Pipistrellus. Five congeners namely common Pipistrelle Pipistrellus pipistrellus (Schreber,

1774), Javan Pipistrelle Pipistrellus javanicus (Gray, 1838), Coromandel Pipistrelle Pipistrellus

coromandra (Gray, 1838), Least Pipistrelle Pipistrellus tenuis (Temminck, 1840) and Dormer‟s

bat Pipistrellus dormeri (Dobson, 1875) were identified from the study area. P. javanicus and P.

dormeri are reported for the first time from the Malakand. A brief description of external body,

cranial and bacular features of the captured species are documented in this paper to highlight

variations among the congeners.

Key words: Pipistrellus; Forearm; Distribution; Malakand; Pakistan.

INTRODUCTION

Chiropterans (bats) are unique among all vertebrate mammals and are equipped for true flight.

They comprise around 25% of all the mammals found on the planet today (Mickleburgh et al.

2002). According to Simmons and Geisler (1998) bats evolved during early Eocene period. They

are considered as key stone species responsible for seed dispersers and pollination (Cox et al.

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1991, Fujita and Tuttle 1991, Rainey et al. 1995). Insectivorous bats consume thousands of

insects in one night and diminish the pests and other vectors of several diseases (Adams 2003).

The genus Pipistrellus is geographically widespread with a range that extends from central

southern Africa, throughout Eurasia to Japan, Indonesia, New Guinea, the Solomon Islands and

northern Australia. It also occurs in Canada, USA and Mexico. Of the 51 species currently

recognized (Koopman, 1993), twelve occur within the Indian subcontinent.


The taxonomic status of this bat species is unknown from Pakistan. The species is distributed in

British Isles, S Denmark, W Europe to the Volga and Caucasus, Morocco; Greece, Turkey, Israel

and Lebanon to Afghanistan, Kashmir, Kazakhstan, Pakistan, Burma, Sinkiang (China), perhaps

Korea, Japan and Taiwan. The Brisitsh Museum has one specimen that was collected from

Kashmir in the beginning of 19th

century. Two other specimens were collected from Gilgit by an

expedition carried out by University of Marryland in 1965 (Robers, 1997). The species has a

restricted range in the Indian subcontinent (Bates and Harrison, 1997) and seems to be common

in Pakistan as there has been no further field studies on bats in Kashmir or Gilgit (Roberts,

1997). The species is considered to be „Least Concerned‟ (IUCN, 2008). Pipistrelles in Europe

have recently been shown to comprise two cryptic species P. pipistrellus which echolocates with

most energy around 45 kHz, and P. pygmaeus, with most energy at 55 kHz (Jones and Parijs,

1993; Barratt et al. 1997).


Pipistrellus javanicus distributed in East Afghanistan, North Pakistan, North and Central India,

South and East Tibet (China), Burma, Thailand, Vietnam, Through SE Asia to Lesser Sunda

Isles and Philippines; perhaps Australia. No literature is available on the distribution of this

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species in Pakistan however a single specimen was collected from Gharial, Murree Hills

(Mahmood-ul-Hassan et al. 2009).


Ten specimens of Pipistrellus coromandra has been collected from Chitral and seventeen

specimens from Saidu Sharif in Swat, the mean head and body length was 43 mm. The mean tail

length was 35 mm. The mean hind foot and ear length were 7 mm and 11 mm, respectively. The

mean forearm length was 32 mm. The Swat specimens averaged 6 gm in weight (Roberts, 1997).

These Pakistan specimens and also those from Afghanistan (Jalalabad) (Gaisler, 1970) appear to

average slightly larger than the population from central India (Brosset, 1962). The species also

has been collected from Dir, Yakh Tangai in Khyber Pakhtunkhwa and from Chakri in Punjab

(Bates and Harrison, 1997). This is a widely distributed and apparently common species in

southern Asia.


Pipistrellus tenuis is the smallest pipistrelle found within the subcontinent with an average

forearm length of 27.7 mm. The species is hard to differentiate from smaller individuals of P.

coromandra on the basis of forearm length. Its body weight averages about 2 g (Gopalakrishna

and Karim, 1972). The species is distributed in Afghanistan to the Moluccas; S China, Laos,

Vietnam, Cocos eeling Isles and Christmas Isle (Indian Ocean). The species has been recorded

from Malakand (Roberts, 1997), Chitral (Sinha, 1980), Multan and Chaklala (Hinton and

Thomas, 1926), Chakri, Gambat, Sukkur (Siddiqui, 1961), Karachi, Malir (Walton, 1974).


Pipistrellus dormeri is confined to India and Pakistan Bates and Harrison (1997). It is restricted

to the Indian Subcontinent where it is an abundant species in areas such as Rajasthan Advani

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(1983). The species has been collected from Sialkot in Punjab and Shikarpur in Sindh (Sinha,

1980) (Fig.3.9.1).

Status. All the above five species of the genus Pipistrellus was categorized as “Least

Concerned” (CAMP, 2002 and IUCN, 2008).

Present study was conducted in Malakand division, KP to ascertain presence or absence of

species of the genus Pipistrellus.

Fig. 3.9.1. Distribution map of five species of the genus Pipistrellus in Pakistan.


Study Area: The study was carried out at Malakand Division situated between the Himalayan

and Hindu Kush foothills and with geographical position 34˚20ˊ and 35˚ 20ˊ North latitudes and

71˚-15ˊ and 72 ˚30′ East longitudes. The total area was 29,800 km2 and was characterized as sub-

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tropical dry mixed deciduous scrub forest and dry subtropical temperate semi-evergreen scrub

forest (Roberts, 1997). Average maximum and minimum temperature are recorded 30℃ and

17℃, respectively and humidity 54%. On the basis of altitudinal gradient the area can be divided

into different zones viz. (i) semi-arid humid-temperate zone, (450-600m), (ii) warm temperate

zone (600-1100m), (iii) temperate zone (1100-1500m), (iv) cool temperate zone (1500-1900 m),

(v) cold temperate zone (1900-3200m), (vi) alpine pastures (2300-4700m), and (vii) snow and

ice zone (4700-7690m).

Study period: The study was carried out from 2010 through 2013 and bats were recorded

through direct observations. For proper identification, the bats were captured and their external

body, cranial body and bacular features were observed.

Apparatus: Mist nets, global positioning system device (Garmin etrax H GPS), dissecting

microscope, stage and ocular micrometer, Pesola balance 10050 Swiss made, digital calipers,

forceps, test tube, glycerin, absolute alcohol, potassium hydroxide (KOH), alizarin red powder

and acetone.

Method: Mist nets were used to capture bats from various habitats like cultivated lands,

grasslands, wetlands, woodlands, fruit gardens, open fields, caves and old buildings providing

suitable habitats for bats. Captured bats were disentangled from the mist nets and were kept in a

cotton bag. The sexes were differentiated by the presence of external genital organs and

reproductive stages (adult/ Juvenile) were determined on the basis of ossification of finger bones

(Kunz, 1988). Baculum preparation was carried out for taking different parameters by following

Lidicker and Yang (1986).

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153

Identification: Identification of bats was carried out analyzing the external features, cranial and

bacular measurements. In addition to this dental formula was used along with the external

measurements for confirmation.


A total of 53 bat specimens representing 5 species of the genus Pipistrellus were recorded from

the study area. These congeners include P. pipistrellus, P. javanicus, P. coromandra, P. tenuis

and P. dormeri. Description of each of these species are mentioned below.


Distribution. Only a single specimen was captured through mist net in Lamin Bala (N35º

27.802′ E72º 14.310′) in Upper Dir district during this study.

Morphology. The wings are relatively narrow. The tail is rather short, shorter than the head and

body with only its extreme tip projecting from the membrane. The tibiae are short and the feet

small. The pararhinal glandular swellings on the muzzle are well developed. The ears are short

and broad; the anterior border of each is evenly convex; the tip is rounded and there is a

concavity on the posterior border. The tragus is almost half the height of the pinna. The pelage is

fine, dense and silky; it is a uniform buffy to chestnut brown on the head and back, with

distinctly darker hair bases. The throat and belly are slightly paler but also have dark grey/black

hair bases. The interfemoral and wing membranes are a uniform brown and essentially naked,

although there are some hairs adjacent to the body and legs on the upper surface of the

interfemoral membrane. The dental formula was 2123/3123=34.

Body Mass and External Body Measurements. The body mass of a single Common Pipistrelle

was 4.60 g (Table 3.9.1). Their head and body length was 40.22 mm while their ear was 11.06

mm long. Thumb and forearm length was 4.01 mm and 31.06 mm, respectively. The tragus

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154

height was 5.02 mm. The antitragus was 1.01 mm. The length of 2nd

metacarpal was 29.10 mm.

The length of 1st phalanx on 2

nd metacarpal was 2.01 mm. The length of 2

nd phalanx on 2

nd

metacarpal was 9.04 mm. The length of 3rd


nd

phalanges on 3rd

metacarpal were 11.11 mm and 9.10 mm, respectively. The length of 3rd

phalanx on 3rd

metacarpal was 8.01 mm. The length of 4th

metacarpal was 28.85 mm. The length

of 1st and 2

nd phalanges on 4

th metacarpal was 10.02 mm and 8.02 mm, respectively. The length

of 5th

metacarpal was 28.52 mm while that of 1st phalanx on 5

th metacarpal was 7.02 mm. The

length of 2nd

phalanx on 5th

metacarpal was 4.01 mm. The wing span was 220.00 mm. Their tibia

and calcar were 12.01 mm and 7.01 mm, respectively while the length of hind foot was 6.44 mm.

The tail length was 32.12 mm (Table 3.9.1).

Cranial Measurements. The skull of an Common Pipistrelle captured from Lamin Bala (BatLab

No. 262) is shown in Fig.3.9.2. The greatest length of skull of a single specimen was 12.14

mm.The breadth of braincase was 6.33 mm while that of zygomatic bone was 7.47 mm. The

post-orbital constriction was 3.39 mm long. The condylo-canine length was 10.89 mm. The

condyle-basal length was 11.47 mm. Anterior and posterior palatal width measured 3.53 mm and

4.96 mm, respectively. The maxillary toothrow length was 4.22 mm. The mandibular toothrow

length was 4.45 mm. The mandible length was measured as 8.27 mm. (Table 3.9.1).

Bacular measurements. The total baculum length of a single specimen was 1.53 mm. The width

of middle extreme was 0.01 mm. The width of distal extreme of the baculum was 0.35 mm. The

shaft length was 1.18 mm. The proximal branch length was 0.01 mm. The distal branch length

was 0.33 mm. The proximal branch width was 0.01 mm. The distal branch width was 0.33 mm.

The baculum was 0.50 mm high (Table 3.9.3, Fig.3.9.3).

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Fig.3.9.2. Dorsal (a), ventral (b) and lateral (c) view of the skull of Pipistrellus pipistrellus. The


Fig.3.9.3. The bacula of Common Pipistrelle (Pipistrellus pipistrellus) captured from Lamin Bala in

Upper Dir district.


Distribution. Only one bat was captured through mist net in Malakand University (N34º 40.054′

E72º 03.653′) in Malakand district during this study.

Morphology. A uniform chestnut brown on the dorsal surface, a darker clove brown with a light

frosting of paler brown on the hair tips. The hair tips are buffy brown on the ventral surface with

the hair roots black or almost black. The ears and wing and interfemoral membranes are a

uniform dark brown and essentially naked. The dental formula was 2123/3123=34.

Body Mass and External Body Measurements. The body mass of a single Javan Pipistrelle

was 5.50 g (Table 3.9.1). Their head and body length was 45.22 mm while their ear was 12.13

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156

mm long. Thumb and forearm length was 4.02 mm and 32.01 mm, respectively. The tragus

height was 5.02 mm. The length of 2nd

metacarpal was 32.11 mm. The length of 1st phalanx on

2nd

metacarpal was 3.03 mm. The length of 2nd

phalanx on 2nd

metacarpal was 10.02 mm. The

length of 3rd


nd phalanges on 3

rd metacarpal were

13.00 mm and 10.03 mm, respectively. The length of 3rd

phalanx on 3rd

metacarpal was 10.01

mm. The length of 4th


nd phalanges on 4

th

metacarpal was 12.11 mm and 5.04 mm, respectively. The length of 5th

metacarpal was 32.15

mm while that of 1st phalanx on 5

th metacarpal was 8.05 mm. The length of 2

nd phalanx on 5

th

metacarpal was 7.21 mm. The wing span was 230.00 mm. Their tibia and calcar were 13.02 mm

and 10.11 mm, respectively while the length of hind foot was 6.05 mm. The tail length was 37.04

mm.

Cranial Measurements. The skull of an Javan Pipistrelle captured from Lamin Bala (BatLab

No. 277) is shown in Fig.3.9.4. The greatest length of skull of a single specimen was 13.13 mm.

The breadth of braincase was 6.68 mm while that of zygomatic bone was 8.37 mm. The post-

orbital constriction was 3.47 mm long. The condylo-canine length was 12.10 mm. Anterior and

posterior palatal width measured 4.16 mm and 5.71 mm, respectively. The maxillary toothrow

length was 4.60 mm. The mandibular toothrow length was 5.20 mm. The mandible length was

measured as 9.46 mm (Table 3.9.3).

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Fig.3.9.4. The dorsal (a), ventral (b) lateral (c) view of upper jaw, andthe lateral view (d) of the

lower jaw of the skull of Pipistrellus javanicusare also given in the same plate.


Distribution. A total of eight specimen was captured through mist net in Barcharai Daim(N34º

33.737′ E71º 44.872′), University of Malakand (N34º 40.054′ E72º 03.653′), Koza Agra (N34º

35.171′ E71º 41.802′) in Malakand district and from Shaheed Benazir Bhutto University

Sheringal (N35º 16.204′ E72º 00.172′), Thal (N35º 28.812′ E72º 14.588′), Dir (N35º 12.327′

E71º 52.540′) and Mian Banda (N34º 50.378′ E71º 51.984′) in Dir district during this study.

Morphology. Pelage colour is a uniform brown on the dorsal surface, ranging from chestnut to

dark clove brown. The ventral surface is conspicuously paler, with beige brown or cinnamon

brown tips to the hairs, the hair roots are dark. The ears and membranes are mid to dark brown

and essentially naked, although there are some hairs on the interfemoral membrane adjacent to

the body and the tail, above and below. The dental formula was 2123/3123=34.

Body mass and external body measurements. The mean body mass of eight Coromandel

Pipistrelle was 5.50g ± 0.77 (SD) (Table 3.9.1). Their head and body length was 43.32 mm ±

2.10 (SD) while their ear was 12.04 mm ± 1.07 (SD) long. Mean thumb and forearm length was

4.70 mm ± 0.45 (SD) and 32.28 mm ± 1.17 (SD), respectively. The tragus height was 4.89 mm ±

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158

0.34 (SD). The anti-tragus height was 2.01 mm ± 0.01 (SD). The length of 2nd

metacarpal was

29.41mm ± 1.02 (SD). The mean length of 1st phalanx on 2

nd metacarpal was 2.77 mm ± 0.44

(SD). The mean length of 2nd

phalanx on 2nd

metacarpal was 9.79 mm ± 0.86 (SD). The mean

length of 3rd

metacarpal was 30.61 mm ± 1.10 (SD) while that of 1st and 2

nd phalanges on 3

rd

metacarpal were 12.06 mm ± 0.74 (SD) and 9.15 mm ± 0.35 (SD), respectively. The mean length

of 3rd

phalanx on 3rd

metacarpal was 7.74 mm ± 0.80 (SD). The mean length of 4th

metacarpal

was 30.61 mm ± 1.01 (SD). The mean length of 1st and 2

nd phalanges on 4

th metacarpal was

11.54 mm ± 0.73 (SD) and 8.50 mm ± 0.88 (SD), respectively. The mean length of 5th

metacarpal was 29.84 mm ± 0.97 (SD) while that of 1st phalanx on 5

th metacarpal was 8.01 mm ±

0.01 (SD). The length of 2nd

phalanx on 5th

metacarpal was 6.17 mm ± 0.34 (SD). The mean

wing span was 222.50 mm ± 10.78 (SD). Their tibia, calcar and tail were 12.90 mm ± 0.28 (SD),

10.35 mm ± 0.79 (SD) and 32.97 mm ± 1.86 (SD), respectively while the length of hind foot was

6.21 mm ± 0.33 (SD) (Table 3.9.1).

Cranial Measurements. The skull of an Coromandel Pipistrelle captured from Tura Gata (Bat

Lab No. 203) is shown in Fig.3.9.5. The mean greatest length of skull of the eight specimens was

12.67 mm ± 0.40 (SD) (Table 3.9.2). The breadth of braincase was 6.44 mm ± 0.18 (SD) while

that of zygomatic bone was 8.17 mm ± 0.09 (SD) (Table 3.9.2). The post-orbital constriction was

3.61 mm ± 0.13 (SD) long. The mean condylo-canine length was 11.52 mm ± 0.39 (SD).

Anterior and posterior palatal width measured 4.21 mm ± 0.19 (SD) and 5.63 mm ± 0.18 (SD),

respectively. The maxillary toothrow length was 4.44 mm ± 0.24 (SD). The mandibular toothrow

length was 4.74 mm ± 0.23 (SD). The mandible length was measured as 9.13 mm ± 0.46 (SD).

The rostral width was 4.91 mm ± 0.20 (SD) (Table 3.9.2).

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Bacular measurements. Total baculum length of six specimens was 5.16 mm ± 0.41 (SD). The

shaft length was 4.16 mm ± 0.44 (SD). The proximal branch length was 0.38 mm ± 0.06 (SD).

The distal branch length was 0.78 mm ± 0.50 (SD). The proximal branch width was 0.41 mm ±

0.04 (SD). The distal branch width was 0.88 mm ± 0.23 (SD) (Table 3.9.3, Fig.3.9.6).

Fig.3.9.5. Dorsal (a) and lateral (b) view of the skull of Pipistrellus coromandra. The dorsal (c) and

lateral (d) view of the lower jaw are also given in the same plate.

Fig. 3.9.6. (1) Dorsal view (2) Lateral view of the bacular of Pipistrellus coromandra captured from

different localities in Malakand and Dir districts.

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Distribution. 35 bats were captured through mist net in Bakrai (N34º 23.939′ E71º 52.202′),

Timergara (N34º 49.471′ E71º 50.396′), koz koper (N34º 24.399′ E71º 50.171′), Matkani (N34º

37.380′ E71º 51.055′), Head Koper (N34º 24.454′ E71º 50.061′), Malakand Tunnel (N34º

33.158′ E71º 54.168′), Maina (N34º 29.765′ E71º 44.585′), Kot (N34º 29.778′ E71º 43.501′),

Manzaray Baba (N34º 29.480′ E71º 42.353′), Qadar Kalay (N34º 24.076′ E71º 50.723′), Shaheed

Benazir Bhutto University Sheringal (N35º 16.204′ E72º 00.172′), Astanadaro Kalay (N34º

24.913′ E71º 49.466′), Thana (N34º 38.334′ E72º 04.233′), Daim (N34º 36.647′ E71º 47.704′),

Tutakan (N34º 36.978′ E71º 49.511′), Community Game Reserve Brah (N34º 29.820′ E71º

46.327′), Ziarat Kalay (N34º 37.213′ E71º 48.715′), Kas kalay (N34º 24.573′ E71º 48.978′),

Fishing Hut (N34º 38.900′ E72º 01.941′), Faqeer Abad (N34º 23.323′ E71º 53.324′), Haryan Kot

(N34º 29.382′ E71º 47.871′) and Mola Misray (N34º 25.251′ E71º 49.085′) in Malakand Division

during this study.

Morphology. The dorsal pelage is a uniform brown, varying in tone from mid brown to a deep

clove brown. The ventral surface is paler; the hair tips are buffy brown; the roots are dark

throughout and essentially naked. The dental formula was 2123/3123=34.

External body measurements. The mean body mass of 35 least pipistrelle was 3.80g ± 0.74

(SD) (Table 3.9.1). Their head and body length was 39.46 mm ± 1.57 (SD) while their ear was

10.44 mm ± 0.70 (SD) long. Mean thumb and forearm length was 4.43 mm ± 0.47 (SD) and

29.24 mm ± 1.03 (SD), respectively. The tragus height was 5.30 mm ± 6.07 (SD). The anti-

tragus height was 1.37 mm ± 0.42 (SD). The length of 2nd


(SD). The mean length of 1st phalanx on 2

nd metacarpal was 2.52 mm ± 0.55 (SD). The mean

length of 2nd

phalanx on 2nd

metacarpal was 8.65 mm ± 0.77 (SD). The mean length of

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161

3rd


nd phalanges on 3

rd metacarpal

were 10.92 mm ± 0.62 (SD) and 8.78 mm ± 0.66 (SD), respectively. The 3rd

phalanx on 3rd



(SD). The mean length of 1st and 2

nd phalanges on 4

th metacarpal was 10.41 mm ± 0.46 (SD) and

7.80 mm ± 1.13 (SD), respectively. The mean length of 5th


(SD) while that of 1st phalanx on 5

th metacarpal was 7.74 mm ± 0.56 (SD). The length of 2

nd

phalanx on 5th

metacarpal was 5.62 mm ± 0.73 (SD). The mean wing span was 197.83 mm ±

13.08 (SD). Their tibia, calcar and tail were 12.29 mm ± 0.56 (SD), 9.97 mm ± 1.53 (SD) and

29.70 mm ± 1.81 (SD), respectively while the length of hind foot was 5.81 mm ± 0.49 (SD)

(Table 3.9.1).

Cranial Measurements. The skull of aleast pipistrelle captured from Fishing Hut is shown in

Fig.3.9.7. The mean greatest length of skull of the 23 specimens was 11.56 mm ± 0.25 (SD)

(Table 3.9.2). The breadth of braincase was 6.01 mm ± 0.12 (SD) while that of zygomatic bone

was 7.42 mm ± 0.13 (SD) (Table 3.9.2). The post-orbital constriction was 3.48 mm ± 0.10 (SD)

long. The mean condylo-canine length was 10.30 mm ± 0.19 (SD). Anterior and posterior palatal

widths measured 3.62 mm ± 0.18 (SD) and 4.99 mm ± 0.16 (SD), respectively. The maxillary

toothrow length was 3.87 mm ± 0.09 (SD). The mandibular toothrow length was 4.10 mm ± 0.06

(SD). The mandible length was measured as 7.89 mm ± 0.60 (SD) (Table 3.9.2).

Bacular measurements. Total baculum length of fourteen specimens was 3.08 mm ± 0.22 (SD).

The shaft length was 2.09 mm ± 0.16 (SD). The proximal branch length was 0.23 mm ± 0.12

(SD). The distal branch length was 0.76 mm ± 0.17 (SD). The proximal branch width was 0.32

mm ± 0.02 (SD). The distal branch width was 0.73 mm ± 0.09 (SD). The bacolum was 0.86 ±

0.13 (SD) high (Table 3.9.3, Fig.3.9.8).

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Fig.3.9.7. Dorsal (a), ventral (b) and lateral (c) view of the skull of Pipistrellus tenuis. The dorsal

(d) and lateral (e) view of the lower jaw are also given in the same plate.

Fig.3.9.8. Baculum of Pipistrellus tenuis captured from Head Koper in Malakand Division.


Distribution. Only eight bats were captured through mist net in Dir (N35º 12.327′ E71º 52.540′),

Fishing Hut (N34º 38.900′ E72º 01.941′), Head Koper (N34º 24.454′ E71º 50.061′) and

Malakand Top (N34º 34.007′ E71º 55.736′) during this study.

Morphology. This is rather a small and delicately built bat with a very striking body colour. The

dorsal fur is long and silky and of a blackish grey colour basally, with the extreme tips of hairs a

pale golden brown giving it a hoary appearance. The belly fur is paler grayish brown. The ears

are large and conspicuous being rather a squarish in outline and forward slanting. The tragus is

half the height of the ear and triangular in shape. The posterior margin of the ear lack any

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projections or notches. There is an extensive inter femoral membrane with a rather small calcar

and inconspicuous lobe below the calcar. The dorsal surface of the hair is sparsely haired and

shows two dark lines or veins extending from the heel of the hind foot up to the base of the

pelvis. The dental formula was 2123/3123=34.

Body Mass and External Body Measurements. The body mass of eight Dormer‟s Bat was

7.81g ± 3.07 (SD) (Table 3.9.1). Their head and body length was 48.76 mm ± 3.65 (SD) while

their ear was 12.30 mm ± 0.71 (SD) long. Mean thumb and forearm length was 5.28 mm ± 0.70

(SD) and 34.30 mm ± 1.25 (SD), respectively. The tragus height was 4.93 mm ± 0.37 (SD). The

anti-tragus height was 2.28 mm ± 0.45 (SD). The length of 2nd


(SD). The mean length of 1st phalanx on 2

nd metacarpal was 2.81 mm ± 0.43 (SD). The mean

length of 2nd

phalanx on 2nd

metacarpal was 10.34 mm ± 0.58 (SD). The mean length of 3rd


nd phalanges on 3

rd metacarpal were

12.25 mm ± 0.74 (SD) and 10.12 mm ± 0.41 (SD), respectively. The mean length of 3rd

phalanx

on 3rd


metacarpal was 32.78 mm ±

1.20 (SD). The mean length of 1st and 2

nd phalanges on 4

th metacarpal was 11.37 mm ± 0.57

(SD) and 9.27 mm ± 0.91 (SD), respectively. The mean length of 5th

metacarpal was 32.18 mm ±

1.40 (SD) while that of 1st phalanx on 5

th metacarpal was 8.32 mm ± 0.43 (SD). The length of

2nd

phalanx on 5th

metacarpal was 6.18 mm ± 0.62 (SD). The mean wing span was 240.48 mm ±

2.15 (SD). Their tibia, calcar and tail were 13.02 mm ± 0.01 (SD), 10.44 mm ± 0.48 (SD) and

33.61 mm ± 1.22 (SD), respectively while the length of hind foot was 6.85 mm ± 0.83 (SD)

(Table 3.9.1).

Cranial measurements. The skull of an Dormer‟s Bat captured from different localities in

Malakand Division (BatLab No. 214). The mean greatest length of skull of three specimens was

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13.77 mm ± 0.11 (SD) (Table 3.9.3). The breadth of braincase was 6.96 mm ± 0.26 (SD) while

that of zygomatic bone was 9.61 mm ± 0.01 (SD) (Table 3.9.3). The post-orbital constriction was

3.86 mm ± 0.29 (SD) long. The mean condylo-canine length was 12.96 mm ± 0.20 (SD).

Anterior and posterior palatal widths measured 4.53 mm ± 0.01 (SD) and 6.65 mm ± 0.02 (SD),

respectively. The maxillary toothrow length was 5.33 mm ± 0.02 (SD). The mandibular toothrow


The mean rostral width was 5.62 mm ± 0.02 (SD) (Table 3.9.3).

The morphological features of the captured specimens are in line with the findings of Roberts

(1997); Bates and Harrison (1997), Srinivasulu et al. (2010) and Javid et al. (2011).

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Table 3.9.1. Mean body mass (g) and external body measurements (mm) of five species of the genus Pipistrellus captured from

Malakand Division.

Body Parameters Pipistrellus

Pipistrellus (n=1) Pipistrellus javanicus (n=1)

Pipistrellus coromandra (n=8) Pipistrellus tenuis (n=35) Pipistrellus dormeri (n=8)

Mean±SD Range Mean±SD Range Mean±SD Range

Body mass 4.60 5.50 5.50±0.77 4.30-6.40 3.80±0.74 2.80-6.00 7.81±3.07 4.90-13.20

Head and body 40.22 45.22 43.32±2.10 41.03-46.02 39.46±1.57 35.33-43.23 48.76±3.65 45.11-54.14

Ear 11.06 12.13 12.04±1.07 10.02-13.02 10.44±0.70 9.04-11.00 12.30±0.71 11.02-13.11

Tragus 5.02 5.02 4.89±0.34 4.04-5.01 5.30±6.07 4.01-40.10 4.93±0.37 4.02-5.22

Antitragus 1.01 - 2.01±0.01 2.00-2.01 1.37±0.42 1.01-2.00 2.28±0.45 2.01-3.01

Forearm 31.06 32.01 32.28±1.17 31.00-34.00 29.24±1.03 26.22-30.11 34.30±1.25 33.02-36.01

Thumb with claw 4.01 4.02 4.70±0.45 4.03-5.10 4.43±0.47 4.01-5.00 5.28±0.70 4.01-6.01

2ndmetacarpal 29.10 32.11 29.41±1.02 28.10-31.01 26.54±0.91 24.55-29.00 31.15±1.24 30.01-33.02

1st Phalanx on 2nd metacarpal 2.01 3.03 2.77±0.44 2.01-3.02 2.52±0.55 2.01-4.00 2.81±0.43 2.11-3.10

2nd Phalanx on 2nd metacarpal 9.04 10.02 9.79±0.86 8.12-11.00 8.65±0.77 7.01-10.03 10.34±0.58 9.55-11.01

3rd metacarpal 29.54 33.22 30.61±1.10 29.14-32.22 27.38±1.01 25.01-29.00 32.87±1.18 32.01-35.14

1st Phalanx on 3rd metacarpal 11.11 13.00 12.06±0.74 11.01-13.00 10.92±0.62 10.01-12.11 12.25±0.74 11.15-13.02

2nd Phalanx on 3rd metacarpal 9.10 10.03 9.15±0.35 9.00-10.00 8.78±0.66 8.10-10.00 10.12±0.41 9.55-11.01

3rd Phalanx on 3rd metacarpal 8.01 10.01 7.74±0.80 6.55-9.00 6.92±0.68 6.01-8.14 8.29±0.77 7.05-9.15

4th metacarpal 28.85 32.12 30.61±1.01 29.10-32.00 27.27±1.07 25.12-29.11 32.78±1.20 31.62-35.05

1st Phalanx on 4th metacarpal 10.02 12.11 11.54±0.73 11.01-13.00 10.41±0.46 10.01-11.01 11.37±0.57 10.51-12.01

2nd Phalanx on 4th metacarpal 8.02 5.04 8.50±0.88 7.24-10.00 7.80±1.13 5.45-11.00 9.27±0.91 8.01-10.01

5th metacarpal 28.52 32.15 29.84±0.97 28.22-31.00 26.82±0.96 25.01-28.02 32.18±1.40 31.25-35.00

1st phalanx on 5th metacarpal 7.02 8.05 8.01±0.01 8.00-8.02 7.74±0.56 7.04-9.00 8.32±0.43 8.01-9.01

2nd phalanx on 5th metacarpal 4.01 7.21 6.17±0.34 6.00-7.00 5.62±0.73 4.51-7.00 6.18±0.62 5.11-7.04

Wing span 220.00 230.00 222.50±10.78 205.00-235.00 197.83±13.08 175.00-222.00 240.48±2.15 238.11-245.12

Tibia 12.01 13.02 12.90±0.28 12.22-13.01 12.29±0.56 11.01-13.00 13.02±0.01 13.01-13.04

Calcar 7.01 10.11 10.35±0.79 9.44-12.00 9.97±1.53 6.13-14.00 10.44±0.48 10.02-11.01

Hind foot 6.44 6.05 6.21±0.33 6.00-7.00 5.81±0.49 5.01-7.00 6.85±0.83 6.11-8.00

Tail 32.12 37.04 32.97±1.86 30.23-35.00 29.70±1.81 26.12-35.00 33.61±1.22 32.01-35.14

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Table 3.9.2. Cranial measurements (mm) of five species of the genus Pipistrellus captured from Malakand Division.

Cranial Parameters

Pipistrellus

pipistrellus

(n=1)

Pipistrellus

javanicus

(n=1)

Pipistrellus coromandra

(n=8) Pipistrellus tenuis (n=23) Pipistrellus dormeri (n=3)

Mean± SD Range Mean± SD Range Mean± SD Range

Condylo-canine length 10.89 12.10 11.52±0.39 10.64-11.89 10.30±0.19 9.97-10.63 12.96±0.20 12.80-13.18

Condylo-basal length 11.47 - - - - - - -

Maxillary toothrow 4.22 4.60 4.44±0.24 3.90-4.60 3.87±0.09 3.75-4.06 5.33±0.02 5.32-5.35

Mandibular toothrow 4.45 5.20 4.74±0.23 4.25-5.01 4.10±0.06 4.01-4.30 5.56±0.07 5.51-5.64

Greatest length of skull 12.14 13.13 12.67±0.40 11.86-13.10 11.56±0.25 10.98-11.96 13.77±0.11 13.70-13.90

Mandible length 8.27 9.46 9.13±0.46 8.05-9.50 7.89±0.60 5.22-8.28 10.53±0.09 10.45-10.63

Posterior palatal width 4.96 5.71 5.63±0.18 5.34-5.86 4.99±0.16 4.72-5.22 6.65±0.02 6.64-6.67

Zygomatic breadth 7.47 8.37 8.17±0.09* 7.96-8.23 7.43±0.14 7.30-7.67 9.61±0.01 9.60-9.61

Breadth of braincase 6.33 6.68 6.44±0.18 6.22-6.70 6.01±0.12 5.78-6.21 6.96±0.26 6.80-7.26

Postorbital constriction 3.39 3.47 3.61±0.13 3.45-3.80 3.48±0.10 3.30-3.71 3.86±0.29 3.60-4.18

Anterior palatal width 3.53 4.16 4.21±0.19 3.76-4.42 3.62±0.18 3.23-3.83 4.53±0.01 4.53-4.54

Rostral width 4.54 5.04 4.91±0.20 4.53-5.17 4.44±0.17 3.90-4.77 5.62±0.02 5.60-5.64

Table 3.9.3. Bacular measurements (mm) of five species of the genus Pipistrellus captured from Malakand Division.

Bacular Parameters Pipistrellus pipistrellus

(n=1)

Pipistrellus javanicus

(n=1)

Pipistrellus coromandra (n=6) Pipistrellus tenuis (n=14) Pipistrellus dormeri (n=3)

Mean± SD Range Mean± SD Range Mean± SD Range

Total baculum length 1.53 - 5.16±0.41 4.68-5.63 3.08±0.22 2.63-3.40 - -

Width of middle extreme 0.01 - - - - - - -

WDE 0.35 - - - - - - -

Shaft length 1.18 - 4.16±0.44 3.65-4.85 2.09±0.16 1.88-2.38 - -

Proximal branch length 0.01 - 0.38±0.06 0.30-0.46 0.23±0.12 0.02-0.36 - -

Distal branch length 0.33 - 0.78±0.50 0.23-1.43 0.76±0.17 0.53-1.25 - -

Proximal branch Width 0.01 - 0.41±0.04 0.36-0.45 0.32±0.02 0.30-0.38 - -

Distal branch width 0.33 - 0.88±0.23 0.45-1.10 0.73±0.09 0.60-0.88 - -

Baculum height 0.50 - - - 0.86±0.13 0.53-1.10 - -

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Bates, P. J. J. and D. L. Harrison. 1997. Bats of the Indian Subcontinent. Harrison Zoological

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CAMP. 2002. Status of South Asian Chiroptera: Conservation Assessment and Management

Plan (C.A.M.P.) Workshop Report, 2002. Zoo Outreach Organisation, CBSG South Asia and

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454.

Dobson, G. E. 1875. Descriptions of new species of Vespertilionidae. Annals Mag.

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Fujita, M.S., Tuttle, M.T. 1991. Flying foxes (Chiroptera Pteropodidae): Threatened animals of

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Gray, J. E. 1838. A revision of the genera of bats…Magazine Zool. Bot. 2:483-505.


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FIRST PROVINCIAL RECORD OF DESERT YELLOW BAT SCOTOECUS PALLIDUS

(DOBSON, 1876) FROM KHYBER PAKHTUNKHWA, PAKISTAN


2, Ali Hussain

2 and Faiz-ur-Rahman

3





Corresponding Author‟s Email: [email protected]


Zoology)

ABSTRACT

A two year survey extending from June 2010 through May 2012 was conducted in Malakand,

Dir and Swat districts in Malakand division, Khyber Pakhtunkhwa (KPK). Twenty two desert

yellow bat (Scotoecus pallidus) specimens were captured using mist and hand nets. The

morphological features of the captured specimens were compared with available literature. This

paper documents first record of S. pallidus from Khyber Pakhtunkhwa.

Key words: Morphometrics, Scotoecus pallidus, Lahore, Malakand

INTRODUCTION

The genus Scotoecus is represented by two African species and has distribution ranges from

Senegal to Ethiopia south to Angola and Mozambique (Hill, 1974). In Asia, only one species,

Scotoecus pallidus is reported from India and Pakistan (Koopman, 1993; Roberts, 1997; Bates

and Harrison, 1997). In Pakistan, the species was first reported by Dobson in 1876 from Mir Pur

near Lahore. Specimens were further collected from Kashmor, Mirpur, Naundero (Wroughton,

1916), Khairpur Nathan Shah in Sindh (Siddiqi, 1961) and Mian Mir, Muzaffargarh, Sialkot


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(USNM; Bates and Harrison, 1997), Gujranwala, Mandi Bhauddin and Hafizabad districts

(Shahbaz et al., 2015) in Punjab province. Roberts (1997) collected sixteen specimens of S.

pallidus from Sindh and Punjab. Average head and body length, tail length, hind foot length and

ear length of the captured specimens was 54 mm, 37 mm, 8 mm and 13 mm, respectively.

Although, S. pallidus is an endemic species to the Indian subcontinent, the population

status of the species is still unknown. The species is declining due to loss of habitat, threats from

invasive species and urbanization (Molur et al., 2002). Proper monitoring and research can help

in conservation of bat species (Meyer et al., 2010). Prior to the present study, S. pallidus has

never been reported from Khyber Pakhtunkhwa (KPK), Pakistan. The present survey was

therefore planned to ascertain the presence or absence of the species from Malakand division in

KPK.


Study area: Present survey extending from June 2010 through May 2012 was conducted in

Malakand, Swat and Dir districts in Malakand division, KPK. Division Malakand is famous for

its valleys and elevated tops (ranging from 500m to 2500m) in the Himalayan and Hindukush

mountains. The diverse ecological zones comprising of extensive agricultural lands, dry and icy

mild valleys provide habitats to a variety of animal species. Peach, apple, persimmon, walnut,

citrus, pear, plum and apricot are the common fruit trees in the study areas. The cultivated

vegetables include onion, tomato, potato, peas, okra, cucurbits, radish, pepper, turnips and

verdant while maize, wheat and rice are amongst the common cereal crops. River Swat flows

through Malakand and Charsadda districts and finally joins Kabul River (Ali et al., 2013).

Sampling strategy: The croplands, ranches, precipitous holes, old structures, abandoned wells,

ruins, houses, under tree bark, crevices, old scaffolds, water channels and under bridges were

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searched to ascertain the presence or absence of Scotoecus pallidus in the study area. Information

regarding possible bat roosts was also collected from the local people of the study area. Once

located, the GPS coordinates of the location were recorded through GPS. Mist and hand nets

were used to capture the bat specimens from the study area following Javid (2011).

Morphological measurements: The captured specimens were weighed up to 0.1 g through

pesola balance 10050, Swiss made and their external body parameters were recorded following

Bates and Harrison (1997). The skull and bacula of the bats captured during present survey were

processed and measured according to Bates et al. (2005) and Javid (2011). The external features

of the bat specimens were noted with vernier calipers measuring up to 0.01mm accuracy and

these measurements were compared with Roberts (1997), Bates and Harrison (1997) and

Shahbaz et al. (2015).


During present survey, twenty two Scotoecus pallidus specimens were captured through mist and

hand nets from Manzaray Baba (N34º 29.480′ E71º 42.353′), Dir (N35º 12.327′ E71º 52.540′),

Jrandy (N34º 24.808′ E71º 48.202′), Koz Koper (N34º 24.399′ E71º 50.171′), Mola Misray

(N34º 25.251′ E71º 49.085′), Astanadaro Kalay (N34º 24.913′ E71º 49.466′), Malakand Top

(N34º 34.007′ E71º 55.736′), Badraga (N34º 23.314′ E71º 50.295′), Head Koper (N34º 24.454′

E71º 50.061′), Pull Saokai (N34º 38.553′ E72º 01.749′), Qadar Kalay (N34º 24.076′ E71º

50.723′), Kot (N34º 29.778′ E71º 43.501′), Fishing Hut (N34º 38.900′ E72º 01.941′) and Matkani

(N34º 37.380′ E71º 51.055′). Figure 3.10.1 shows new distribution map of the species from

Pakistan. The external body, cranial and bacular measurements of the captured specimens were

recorded and compared with Roberts (1997), Bates and Harrison (1997) and Shahbaz et al.

(2015).

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The wing and tail membranes of the captured specimens were grey brown while the belly

fur was pale in color. The ears were square in outline; the tragus was curving backward with

anterior intended and near half of the ear pinna height. Similar findings have been documented

by Roberts (1997).

The external body measurements of the captured specimens (Table 3.10.1) are aligned with

Roberts (1997), Bates and Harrison (1997) and Shahbaz et al. (2015).

The skulls of the captured specimens were robust with small postorbital processes. The

upper jaw contained one pair of incisors, zygomatic arch was very delicate. Palate anterior

emargination was wide and U-shaped; the post palatal extension was narrow with a small,

delicate, palatal spine (Figure 3.10.2). These features were similar as described by Bates and

Harrison (1997) and Shahbaz et al. (2015).

The average condylo-canine length of the S. pallidus specimens captured during present

study was 14.24±0.26 mm, maxillary toothrow length 5.66±0.10 mm, mandibular tooth row

length 6.11±0.12 mm, greatest length of skull 15.00±0.26 mm, mandible length 11.35±0.23 mm,

posterior palatal width 6.85±0.17 mm, zygomatic breadth 10.51±0.01 mm, breadth of braincase

7.90±0.22 mm, postorbital constriction 4.46±0.09 mm and anterior palatal width was 5.28±0.13

mm. These measurements matched findings of Bates and Harrison (1997) and Shahbaz et al.

(2015) (Table 3.10.2).

The penis of the male specimens (n = 15) captured during present study were enlarged

with a long narrow shaft, a small bifid tip and a bilobate base. Total baculum length of male S.

pallidus specimens was 4.65 ± 0.17 mm and the length of shaft was 4.14 ± 0.35 mm. The

proximal branch length was 0.13 ± 0.12 mm, proximal branch width 0.41 ± 0.02 mm, baculum

height1.31±0.08 mm, distal branch length 0.24 ± 0.24 mm and distal branch width were recorded

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0.77 ± 0.19. Similar bacular measurements have been documented by Shahbaz et al. (2015)

(Table 3.10.2).

This paper documents first record of S. pallidus from Khyber Pakhtunkhwa from where the

species was not reported prior to the present study indicating range extension. The species is

considered local having restricted distribution range and has not been reported from Iran and

Afghanistan. However, it can be recorded from sub-tropical latitudes and semi-desert habitats.

Figure 3.10.1. Distribution map of the lesser yellow house bat Scotoecus pallidus in Pakistan

showing it as new record from Malakand.

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Figure 3.10.2. Dorsal (a), ventral (b) and lateral (c) view of the skull of Scotoecus pallidus

captured from Malakand, KPK. The dorsal (d) and lateral (e) view of the lower

jaw.

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Table 3.10.1. Comparison of body mass (g) and external body measurements (mm) of Scotoecus pallidus specimens captured from

different localities in Malakand division, KPK with available.

Body Parameters Bates and

Harrison, 1997 Roberts, 1997 Shahbaz et al. (2015). Present Study

Body mass - - 11.5 (9-14.3) 11.66±1.53 (9.10-14.40)

Head and body length 52.8±2.5 (50.0-58.0) 54 (50-59) 55.9 (47-59) 55.97±1.41 (53.33-58.00)

Ear length 12.0-15.0 13 11.2 (9-13.5) 12.98±0.76 (12.01-14.30)

Tragus height - - 4.2(3.4-4.8) 5.71±0.45 (5.01-6.01)

Forearm length 36.2±0.9 (34.1-37.3) - 37(34-39.5) 36.83±0.42 (36.01-37.20)

Thumb with claw - - - 6.26±0.41 (6.01-7.00)

Length of 2nd

metacarpal - - - 33.26±0.90 (32.00-35.00)

1st phalanx on 2

nd metacarpal - - - 2.78±0.41 (2.01-3.00)

2nd

phalanx on 2nd

metacarpal - - - 9.12±0.75 (7.12-10.00)

Length of 3rd

metacarpal 34.6±1.0 (33.5-36.0) - 35.2(34-39) 34.97±0.50 (34.11-36.00)

1st phalanx on 3

rdmetacarpal - - 12(7-13) 11.49±0.50 (11.01-12.10)

2nd

phalanx on 3rd

metacarpal - - 10(6.1-11) 9.79±0.39 (9.03-10.00)

3rd

phalanx on 3rd

metacarpal - - - 8.10±0.77 (6.08-10.00)

Length of 4th

metacarpal 34.2±0.9 (32.8-35.4) - 34.7(31-38.5) 34.72±0.44 (34.01-35.11)

1st phalanx on 4

th metacarpal - - 11.3(10.2-12.5) 10.79±0.49 (9.51-11.22)

2nd

phalanx on 4th

metacarpal - - 8.98(7-10.7) 10.07±0.48 (9.51-11.00)

Length of 5th

metacarpal 33.7±0.8 (32.6-34.9) - 34.3(33.2-35.4) 34.07±0.06 (34.01-34.20)

1st phalanx on 5

th metacarpal - - 9.3(5.8-11.5) 8.71±0.44 (8.01-9.02)

2nd

phalanx on 5th

metacarpal - - - 5.96±0.54 (5.02-7.00)

Wingspan - - 25(21.6-32.8) 247.32±13.01 (217.00-264.00)

Tibia length - - 13.3(8.5-15) 13.91±0.68 (12.00-15.00)

Calcar length - - 5.7(3.5-8) 11.09±1.31 (9.00-14.00)

Hind foot length 8.3±1.4 (6.0-10.0) 8 9.5(7.5-11) 8.27±0.63 (7.01-10.00)

Tail length 36.9±2.2 (34.0-41.0) 37 (31-41) 33.2(27.2-38) 34.14±0.21 (34.00-35.00)

Mean±SD (Range)

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Table 3.10.2. Comparison of cranial and bacular measurements (mm) of Scotoecus pallidus specimens captured from different

localities in Malakand division with available literature.

Cranial Parameters Present study Bates and Harrison, 1997 Shahbaz et al. (2015)

Condylo-basal length 14.24±0.26 (13.83-14.68) 14.1±0.3 (13.8-14.8) 14.3(13.7-15.2)

Maxillary toothrow length 5.66±0.10 (5.50-5.86) 5.6±0.2 (5.5-5.9) 4.9(4.2-5.5)

Mandibular toothrow length 6.11±0.12 (5.91-6.34) 6.1±0.2 (5.9-6.4) 5.4(4.8-5.7)

Greatest length of skull 15.00±0.26 (14.53-15.43) 15.1±0.5(14.5-16.1) 14.8(14.3-15.2)

Mandible length 11.35±0.23 (10.94-11.87) 11.4±0.3 (10.9-12.0) 10.8(10.3-11.2)

Posterior palatal width 6.85±0.17 (6.60-7.19) 6.9±0.2 (6.6-7.2) 6.0(5.3-6.4)

Zygomatic breadth 10.51±0.01 (10.50-10.54) 10.5± - (10.5-10.5) 10.1(9.8-10.4)

Breadth of braincase 7.90±0.22 (7.54-8.20) 7.7±0.2 (7.5-8.2) 7.2(6.4-8.0)

Postorbital constriction 4.46±0.09 (4.25-4.69) 4.3±0.1 (4.2-4.5) 4.3(3.9-4.8)

Anterior palatal width 5.28±0.13 (5.03-5.49) - 4.5(4.2-4.7)

Bacular Parameters Mean± SD (n=15) -

Total baculum length 4.65±0.17 (4.35-5.10) - 4.9(4.7-5.2)

Shaft length 4.14±0.35 (3.55-4.70) - 4.1(3.6-4.7)

Proximal branch length 0.13±0.12 (0.02-0.30) - 0.5(0.46-0.7)

Distal branch length 0.24±0.24 (0.01-0.63) - 0.4(0.34-0.4)

Proximal branch Width 0.41±0.02 (0.38-0.43) - 1.2(0.8-1.7

Distal branch width 0.77±0.19 (0.40-1.00) - 0.5(0.47-0.53)

Width of middle extreme 0.36±0.04 (0.30-0.43) - -

Width of distal extreme 0.97±0.03 (0.93-1.00) - -

Baculum height 1.31±0.08 (1.13-1.45) - 0.5(0.4-0.6)

Mean±SD (Range)

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CHAPTER 4

SUMMARY

The present study was conducted from 2010 to 2013 in three districts (Malakand, Dir and Swat)

of Malakand Division. A total of 49 stations were sampled for bats where total 1982 bats were

recorded. A total of 21 species of bats belonging to six families, fourteen genera were recorded.

These includes the Indian flying fox (Pteropus giganteus), the greater short-nosed fruit bat

(Cynopterus sphinx), the fulvous fruit bat (Rousettus leschenaultia), the greater mouse-tailed bat

(Rhinopoma microphyllum), the lesser mouse tailed bat (Rhinopoma hardwickii), the greater

false vampire (Megaderma lyra), the greater horseshoe bat (Rhinolophus ferrumequinum), the

Blyth‟s horseshoe bat (Rhinolophus Lepidus), the fulvous leaf-nosed bat (Hipposideros fulvus),

the Hodgson‟s bat (Myotis formosus), the Asian barbastelle (Barbastella leucomelas), the Asiatic

greater yellow house bat (Scotophilus heathii), the Asiatic lesser yellow house bat (Scotophilus

kuhlii), the serotine (Eptesicus serotinus), the common pipistrelle (Pipistrellus pipistrellus), the

javan pipistrelle (Pipistrellus javanicus), the coromandel pipistrelle (Pipistrellus coromandra),

the least pipistrelle (Pipistrellus tenuis), the Dormer‟s bat (Pipistrellus dormeri), the desert

yellow bat (Scotoecus pallidus) and the Schreiber‟s long-fingered bat (Miniopterus fuliginosus)

were recorded throughout the study area.

M. formosus was common to all the three districts while B. leucomelas and P. pipistrellus were

captured only from Dir district. The Hodgson‟s bat (M. formosus) and the Schreiber‟s long-

fingered bat (M. fuliginosus) were captured from Malakand and Swat districts. The skeleton of

C. sphinx was recorded only from adjacent area of Malakand district. The Indian flying fox

(Pteropus giganteus) was not previously recorded from Khyber Pakhtunkhwa while it has been

reported from Punjab and Sindh province of the country. There are only six species which has

Summary

181

previously been reported from Khyber Pakhtunkhwa while thirteen bats were newly recorded

from the study area. Only two bats were newly recorded for the first time in the country.

The mean forearm length of the three P. giganteus was 152.23 mm ± 3.72 (SD). The mean

greatest skull length was 65.96 mm ± 1.42 (SD). The maxillary toothrow length was 24.91 mm ±

0.84 (SD). The mandible and mandibular toothrow length were 50.78 mm ± 0.87 (SD) and 27.41

mm ± 0.66 (SD), respectively.

The thumb and forearm length of one C. sphinx was 25.80 mm and 65.48 mm, respectively. The

greatest length of skull was 32.20 mm. The maxillary and mandibular toothrow length were

10.86 mm and 12.64 mm. The mandible was 24.75 mm long.

The mean forearm and thumb of R. leschenaultii was 80.23 mm ± 3.26 (SD) and 27.79 mm ±

1.22 (SD), long, respectively. The mean greatest skull length was 36.97 mm ± 1.11 (SD). The

mean mandible, maxillary and mandibular toothrow length were 28.95 mm ± 0.90 (SD), 14.08

mm ± 0.44 (SD) and 15.51 mm ± 0.47 (SD), respectively.

Mean thumb and forearm length of three R. microphyllum was 8.80 mm ± 0.95 (SD) and 67.45

mm ± 4.60 (SD), respectively. The mean greatest length of skull was 20.15 mm ± 0.64 (SD). The

mandible, maxillary and mandibular toothrow length were 7.30 mm ± 0.18 (SD), 8.11 mm ±

0.11 (SD) and 14.38 mm ± 0.63 (SD), respectively.

Mean thumb and forearm length of R. hardwickii was 8.23 mm ± 0.38 (SD) and 59.90 mm ±

1.21 (SD), respectively. The mean greatest length of skull of the four specimens was 18.20 mm ±

0.48 (SD). The maxillary and mandibular toothrow length were 6.08 mm ± 0.07 (SD) and 6.72

mm ± 0.13 (SD), respectively. The mandible length was measured as 12.38 mm ± 0.0.23 (SD).

Mean thumb and forearm length of M. lyra was 11.80 mm ± 0.44 (SD) and 70.06 mm ± 0.69

(SD), respectively. Mean greatest length of skull of the three specimens was 29.60 mm ± 0.46

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182

(SD). The maxillary toothrow length was 11.40 mm ± 0.10 (SD). The mandibular toothrow


Mean thumb and forearm length of R. ferrumequinum was 4.01 mm ± 0.01 (SD) and 60.01 mm ±

1.41 (SD), respectively. The mean greatest length of skull of the two specimens was 23.35 mm ±

0.20 (SD). The maxillary toothrow length was 9.18 mm ± 0.02 (SD). The mandibular toothrow


The mean thumb and forearm length of R. lepidus was 3.87 mm ±0.13 (SD) and 38.02 mm ±

0.63 (SD), respectively. The mean greatest length of skull of the two specimens was 15.94 mm ±



Mean thumb and forearm length of H. fulvus was 4.91 mm ± 0.17 (SD) and 41.41 mm ± 0.97

(SD), respectively. The mean greatest length of skull of the thirteen specimens was 18.45 mm ±



Mean thumb and forearm length of M. formosus was 9.26 mm ± 0.70 (SD) and 48.74 mm ± 2.02

(SD), respectively. The mean greatest length of skull of the three specimens was 17.81 mm ±



Thumb and forearm length of B. leucomelas was 5.65 mm and 42.88 mm, respectively. The

tragus height was 10.32 mm. The greatest length of skull of a single specimen was 15.87 mm.

The maxillary toothrow length was 4.91 mm. The mandibular toothrow length was 5.43 mm. The

mandible length was measured as 10.02 mm.

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183

Mean thumb and forearm length of S. heathii was 9.06 mm ± 0.41 (SD) and 62.25 mm ± 1.76

(SD), respectively. The mean greatest length of skull of the nine specimens was 23.12 mm ± 0.46

(SD). The maxillary toothrow length was 7.87 mm ± 0.16 (SD). The mandibular toothrow length

was 8.93 mm ± 0.16 (SD). The mandible length was measured as 16.62 mm ± 0.19 (SD).

Mean thumb and forearm length of S. kuhlii was 7.01 mm ± 1.41 (SD) and 50.06 mm ± 7.13

(SD), respectively. The mean greatest length of skull of the two specimens was 19.24 mm ± 0.71



Mean thumb and forearm length of E. serotinus was 8.92 mm ± 0.32 (SD) and 53.37 mm ± 1.39

(SD), respectively. The mean greatest length of skull of the fifteen specimens was 21.40 mm ±



Thumb and forearm length of P. pipistrellus was 4.01 mm and 31.06 mm, respectively. The

greatest length of skull of a single specimen was 12.14 mm. The maxillary toothrow length was

4.22 mm. The mandibular toothrow length was 4.45 mm. The mandible length was measured as

8.27 mm.

Thumb and forearm length of P. javanicus was 4.02 mm and 32.01 mm, respectively. The

greatest length of skull of a single specimen was 13.13 mm. The maxillary toothrow length was

4.60 mm. The mandibular toothrow length was 5.20 mm. The mandible length was measured as

9.46 mm.

Mean thumb and forearm length of P. coromandra was 4.70 mm ± 0.45 (SD) and 32.28 mm ±

1.17 (SD), respectively. The mean greatest length of skull of the eight specimens was 12.67 mm

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184

± 0.40 (SD). The maxillary toothrow length was 4.44 mm ± 0.24 (SD). The mandibular toothrow


Mean thumb and forearm length of P. tenuis was 4.43 mm ± 0.47 (SD) and 29.24 mm ± 1.03

(SD), respectively. The mean greatest length of skull of the 23 specimens was 11.56 mm ± 0.25



Mean thumb and forearm length of P. dormeri was 5.28 mm ± 0.70 (SD) and 34.30 mm ± 1.25

(SD), respectively. The mean greatest length of the skull was 13.77 mm ± 0.11 (SD). The

mandible, maxillary and mandibular toothrow length were measured as 10.53 mm ± 0.09 (SD),

5.33 mm ± 0.02 (SD) and 5.56 mm ± 0.07 (SD), respectively.

Mean thumb and forearm length of S. pallidus was 6.26 mm ± 0.41 (SD) and 36.83 mm ± 0.42

(SD), respectively. The mean greatest length of skull of the twenty two specimens was 15.00 mm

± 0.26 (SD). The maxillary toothrow length was 5.66 mm ± 0.10 (SD). The mandible and

mandibular toothrow length were 11.35 mm ± 0.23 (SD) and 6.11 mm ± 0.12 (SD), respectively.

Mean thumb and forearm length of M. fuliginosus bat was 6.61 mm ± 0.43 (SD) and 37.59 mm ±

5.37 (SD), respectively. The mean greatest length of skull of the six specimens was 14.48 mm ±

0.58 (SD). The maxillary toothrow length was 5.32 mm ± 0.39 (SD). The mandible and

mandibular toothrow length were 10.54 mm ± 0.65 (SD) and 5.71 mm ± 0.49 (SD), respectively.

FUTURE RECOMMENDATIONS

1. Bat surveys. This is the first extensive exploration of that small portion of the Khyber

Pakhtunkhwa which comprises of only three districts of Malakand Division i.e.

Malakand, Dir and Swat. Although more focus remained towards Malakand district, six

families, fourteen genera, twenty one species were identified. Moreover, two new country

Summary

185

records (Myotis formosus and Miniopterus fuliginosis) were also explored. Further bat

surveys in poorly surveyed parts of the country especially in KPK and Baluchistan may

result in identification of some other new bat taxa. More bat surveys involving greater

field efforts may also confirm the presence or absence of those already described from

the country.

2. Distribution ranges and species specific habitat analysis. Presence of thirteen new

locality records (Pteropus giganteus, Cynopterus sphinx, Rhinopoma hardwickii,

Megaderma lyra, Rhinolophus Lepidus, Hipposideros fulvus, Barbastella leucomelas,

Scotophilus heathii, Scotophilus kuhlii, Eptesicus serotinus, Pipistrellus javanicus,

Pipistrellus dormeri and Scotoecus pallidus) and two new country records (Myotis

formosus and Miniopterus fuliginosis) gives credence to the idea that distribution ranges

of most of the bat species has change over the past sixty years. Thus serious scientific

studies are needed to redefine distribution ranges and identify species specific habitats

using global positioning system and radio-telemetric studies.

3. Reconfirmation of bat taxonomy. Genetic analysis of none of the bat species of the

country has been made using molecular markers thus leaving behind a chance to doubt

identification of cryptic bat species. Thus molecular genetic studies of all the bat species

of the country is highly recommended which may also lead to the discovery of such bat

taxa which are new to science.

4. Bat call library. The only bat detector (Patterson D 1000X) present in the country fell

down from my hand in a water body and became out of order. So none of the bat could be

recorded. Bat call analysis has boosted bat identification throughout the world but the

Summary

186

lack of such sophisticated equipment in the country has become a major bottle neck in the

establishment of a bat call library.

5. Awareness campaigns. Majority of the countrymen are unaware of the ecological

services rendered by bats. Khyber Pakhtunkhwa is the major fruit growing region of the

country. Based on misperceptions, the locals consider all bats as vermin and kill them

ruthlessly. Conservation education to highlight the significance of bats must be included

in the curriculum of children at primary school level so that they may adopt a pro-

conservation attitude in the first few years of their personality building.

in wildlife and ecology faculty of fisheries and...

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