The Bats of Wheat-Rice Based Agroecosystem of Punjab

THE BATS OF WHEAT-RICE BASED AGROECOSYSTEM OF PUNJAB

MUHAMMAD SHAHBAZ Regd. No. 2007-VA-573

A THESIS SUBMITTED IN THE PARTIAL FULFILMENT OF THE REQUIREMENT FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN WILDLIFE AND ECOLOGY DEPARTMENT OF WILDLIFE AND ECOLOGY FACULTY OF FISHERIES AND WILDLIFE

UNIVERSITY OF VETERINARY AND ANIMAL SCIENCES LAHORE, PAKISTAN

2013 The Controller of Examinations, University of Veterinary & Animal Sciences, Lahore.

We, the Supervisory Committee, certify that the contents and form of the thesis, submitted by Muhammad Shahbaz, Registration No. 2007-VA-573 have been found satisfactory and recommend that it be processed for the evaluation by the External Examination (s) for award of the Degree.

Chairman ______Dr. Arshad Javid

Member ______Dr. Khalid Mahmood Anjum

Member ______Prof. Dr. Muhammad Ashraf TABLE OF CONTENTS Acknowledgements ii List of Tables iv List of Figures v CHAPTER 1 ...... 1 INTRODUCTION ...... 1 CHAPTER 2 ...... 6 REVIEW OF LITERATURE ...... 6 2.1. Species Account ...... 13 2.1.1. Rousettus leschenaulti …………………………………………………….……...13 2.1.2. Rhinolophus lepidus …….…………………..………………………..…………..14 2.1.3. Rhinolophus blasii ……………………………………………………………….14 2.1.4. Scotophilus heathii………………………………………………………...... 15 2.1.5. Pipistrellus paterculus…………………………………………..……..…………...... 15 2.1.6. Pipistrellus javanicus…………………...……………………….....……………..16 2.1.7. Pipistrellus tenuis ….…………...……………………………..………………….16 2.1.8. Pipistrellus ceylonicus……………………………………………………………17 2.1.9. Scotozous dormeri ……….…………………………………………….…………18 2.1.10. Scotoecus pallidus….…………………………………………………………....18 2.2. Statement of Problem.....……………………………………………………………19

LITERATURE CITIED…………….………………………………………...……………20

CHAPTER 3…...…………………………………………..………………………………..31

Experiment No. 3.1. Morphometrics of fulvous fruit bat (Rousettus leschenaulti) from Lahore, Pakistan……………………………………………...... ………....…..33 Experiment No. 3.2. First record of Blyth’s horseshoe bat, Rhinolopus lepidus from Punjab, Pakistan …………………………………………..…………………………47 Experiment No. 3.3. The Blasius’ horseshoe bat Rhinolophus blasii (Chiroptera, Rhinolophidae) still extend to Pakistan …………...…………………………………60 Experiment No. 3.4. Recent Record of Scotophilus heathii from wheat-rice based agroecosystem of Punjab …..…………………….…………………………...……...68 Experiment No. 3.5. Bat fauna of genus Pipistrellus from wheat-rice based agroecosystem of Punjab, Pakistan wheat-rice based agroecosystem of Punjab….....77 Experiment No. 3.6. Recent Record of Desert Yellow House Bat, Scotoecus pallidus (Order Chiroptera) from Punjab, Pakistan……….…………………………...……...90

CHAPTER 4…………………….……………………………………………….…….……99

Summary……………………………………...……………………………………...99

ACKNOWLEDGEMENTS All praises and thanks are due to ALMIGHTY ALLAH, Who is the Supreme and Eternal, Who is the Most Merciful, and Beneficent, Who created me in a race of human beings and most important, in Muslim community. I humbly pay my respect to The Holy Prophet Hazrat Muhammad Mustafa (Peace be upon him), who is the most perfect and excellent personality amongst ever born persons on the surface of earth, I humbly pray to my Lord grant us right love for His messenger and grant right obedience to his sayings, who is the greatest social reformer and who directed the people to acquire knowledge wherever it is. This tough task of completion of my PhD degree was not possible without the assistance, guidance and cooperation of my supervisor Dr. Arshad Javid, Assistant Professor, Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore, who is God gift for Department of Wildlife and Ecology. He is very sincere, responsive personality in this department. He is always ready to help the students with anything, anywhere, anytime and grant excellent advices and thought-provoking instructions in conducting research activities. I am grateful to my Co-Supervisor, Dr. Muhammad Mahmood-ul-Hassan, Associate Professor, Department of Zoology and Fisheries, University of Agriculture, Faisalabad and members of my supervisory committee, Dr. Khalid Mahmood Anjum, Assistant Professor, Department of Wildlife and Ecology and Prof. Dr. Muhammad Ashraf, Dean, Faculty of Fisheries and Wildlife, University of Veterinary and Animal Sciences, Lahore for their skillful guidance and critical insight. I am also thankful to Prof. Dr. Muhammad Akram, Ex-Dean, Faculty of Fisheries and Wildlife for his keen interest in my research work. Special thanks to all my friends and colleagues for their well wishes and cordial cooperation during whole study period. My sincerest thanks are extended to my father Haji Nassrullah Khan, who always inspired me to higher ideas of life. At last but not least I would like to acknowledge the prayers and well wishes of my family members, my sisters, my brothers, especially my sweet daughter, Ayesha Shahbaz and my wife, Nazir Fatima who suffered a lot during whole course of this study. They taught, loved and supported me to achieve higher goals in my life. Their concern in me can never be fully returned but will always be remembered.

The financial support by the Higher Education Commission (HEC), Pakistan (Pin

Code Bm4-314) for the completion of my PhD degree is highly acknowledged.

Muhammad Shahbaz

iii

LIST OF TABLES Table No. Title Page No. Mean external body, cranial and bacular measurements (mm) of 3.1.1. Rousettus leschenaultii captured from Badian, Lahore. (n is the 40 number of specimens). Comparison of mean external body and cranial measurements of 3.1.2. Rousettus leschenaultii (I = Roberts (1977), II = Bates and Harrison 41 (1997), III = Present study). Body weight (g), external body, cranial and bacular measurements 3.2.1. (mm) of Rhinolophus lepidus (mean and range when at least two 58 specimens were recorded) captured from Rasul Nagar, Gujranwala. External, cranial and bacular measurements (in mm, except weight 3.3.1. in g) of Rhinolophus blasii (mean and range when at least two 67 specimens were recorded). Sampling sites in three districts of wheat-rice based agroecosystem 3.4.1. 71 of Punjab. Body mass (g), external body, cranial and bacular measurements (mm) of Scotophilus heathii captured from wheat-rice based 3.4.2. 76 agroecosystem of Punjab, Pakistan (mean ± standard deviation (minimum - maximum) (n is the number of specimens). Netting stations in three districts of wheat-rice based agro- 3.5.1. 86 ecosystem of Punjab. Mean body mass (g) and external body measurements (mm) of six species of genus Pipistrellus captured from wheat rice based 3.5.2. 87 agroecosystems of Punjab, Pakistan (1 = Present study; 2 = Bates and Harrison 1997). Mean cranial measurements (mm) of six species of genus 3.5.3. Pipistrellus captured from wheat rice based agroecosystems of 88 Punjab, Pakistan (1 = Present study; 2 = Bates and Harrison 1997). Comparison of external body, cranial and bacular measurements of 3.6.1. Scotoecus pallidus captured during present study with Roberts 98 (1997) and Bates and Harrison (1997).

LIST OF FIGURES Figure No. Title Page No. 3.1.1. Cranial features of Rousettus leschenaulti captured from Lahore 41 3.1.2. Baculum of Rousettus leschenaulti captured from Lahore 41 Photographs showing (a) external view of the temple where the 3.2.1. Rhinolophus lepidus are roosting, (b) inner view, (c) facial 59 features of R. Lepidus Photograph of the baculum of Rhinolophus vepidus showing its 3.2.2. 59 shape Noseleaf (a) and baculum (b) of R. blasii from Manawa (Lahore, 3.3.1. 66 Pakistan) 3.4.1. Baculum of Scotophilus heathii showing its shape 73 Bacula of P. pipistrellus (a), P. dormeri (b), P. tenuis (c), P. 3.5.1. 89 ceylonicus (d), P. javanicus (e), P. paterculus (f)

CHAPTER 1

INTRODUCTION

Present survey on diversity and distribution of bat fauna of wheat rice based agro-ecosystem of

Punjab was conducted in three districts namely Gujranwala, Hafizabad and Mandi Bhaudin. The areas in close vicinity of these districts were also explored for collection of various bat species.

These districts lie 200 meters above sea level, hot and semi-arid climate prevails and temperature reaches 36-42 °C during summer (June to September). June is the hottest month with maximum and minimum temperatures of 40º C and 27º C, respectively. The coldest months are usually

November to February, when the temperature drops to an average of 7 °C. January is the coldest month. The maximum and minimum temperatures during this month are 19º C and 5º C, respectively. The highest precipitation months are July and August and average annual rainfall is

888 millimeters. Major crops of the area are wheat, rice, potato, sugarcane, barley, corn and millt etc. and fruits are guava and citrus. Eastern part of the study area receives more rain. Most popular trees of the area are beri (Ziziphus jabutus), popular (popolus spp), simbol (Bombax malabarium), banyan (Ficus benghalesis), dharaik (Smelia azedarach), sheesham (Dalbergia sissoo), kikar (Acacia arabica, nilotica), peepal (Ficus religosa), mulberry (Mmourus alba), mango tree (Mangifera indica), siris (Albizza abbek), jaman (eugenia jambolana), lasura

(Cordial myxa) and Amaltas (Cassia fistula). Common birds of the area include ducks, geese, partridges, grouse and quails etc.

The members of the order chiroptera are widely distributed and are found everywhere except the tundra, some deserts and few isolated islands (Hutson et al. 2001). This order is represented by 18 families, 202 genera and 1116 species (Wilson and Reeder 2005). Order

1 ……………………………………………………………………………………………………Introduction chiroptera has two sub orders, the megachiroptera and the microchiroptera. The megachiropterans are represented by a single family, Pteropodidae, members of this family are commonly known as fruit eating bats and are represented by 42 genera and 167 species. The microchiropterans are mostly insectivorous bats, comprise second most diverse group of small mammals and are represented by 17 families, 160 genera and 949 species (Koopman 1993).

Frugivorous bats are playing pivotal role in pollination of many of the plant species of economic importance (Nowak 1994). The insect eating bats are the agents for biological control of many insect populations.

The bat fauna of Pakistan is represented by 8 families, 26 genera and 54 species

(Mahmood-ul-Hassan et al. 2009) and is comparable to the any other region with similar climatic conditions and topography (Horacek et al. 2000). Out of total 54 chiropteran species in the country, 31 species representing 15 genera and 6 families belong to Palearctic region while the other belong to the Oriental or Ethiopian fauna (Roberts 1997; Mahmood-ul-Hassan et al. 2009).

However, exact number of bats in Pakistan is still uncertain (Roberts 1997; Bates and Harrison

1997; Walker and Molur 2003; Wilson and Reeder 2005). Roberts (1997) listed 50 bat species of bats representing 23 genera and 8 families. However, Walker and Molur (2003) and Mahmood- ul-Hassan et al. (2009) expect some more records because India and Pakistan share same boarder and the bats in India are represented by 8 families, 37 genera and 119 species (Nameer 2000).

Similarly, the taxonomy of many of the bat species in Pakistan is not clear for example

Pipistrelllus savi, Plecotus austriatus, P. auritus, Scotozous dormeri (Roberts 1997; Bates and

Harrison 1997; Walker and Molur, 2003; Simmons, 2005; Spitzenberg et al. 2006). In most of the cases, the information is based only on the original description of the species since it has not been collected afterwards (Mahmood-ul-Hassan et al. 2009). Additionally, many new taxa can be

……………………………………………………………………………………………………Introduction identified if the cryptic bat species are accurately identified as has been done in other parts of the world (Jones and van Parijs 1993; Davidson-Watts et al. 2006).

Bats play significant role in maintenance of ecosystems as the dispersal of seeds and pollination of many of the plants is dependent on frugivorous bats (Mickleburgh et al. 1992). The fruit and nectar eater bats are equally important for economically valuable crop plants such as bananas, avocados, dates, figs, peach and mangoes (Fujitta and Tuttle 1991). The short nosed fruit bat (Cynopterus sphinx), the Indian fruit bat (Pteropus giganteus) and fulvous fruit bat

(Rousettus leschenaulti) are reported to visit 114 plant species and act as pollen and seed disperses (Mickleburgh et al. 1992). All these three bat species are present in Pakistan but their positive role in maintenance of ecosystem has never been acknowledged. They are disliked and killed in many parts of the where they are considered pests for fruits. Microchiropterans are natural hunters and predator of many crop insects. It has been estimated that a colony of just 150

Big Brown bats (Eptesicus fuscus) can eat enough cucumber beetles each summer to protect local farmers from 33 million root worms. These insect pests cost the United States government billions of dollars annually (Bat Conservation International). Insectivorous bats also consume large number of mosquitoes in each night from peoples’ backyards, and in this way are playing crucial role in balancing night flying insect populations. Moreover, bat guano maintains is an amalgam of nitrates and phosphates and enhances soil fertility. The analysis of tropical agroecosystem indicates that bats are the real pest control agents in tropical plains and in the rain forest of India (Vanitharani 2004). Insectivorous bats are well known predators of many insect pests and are playing very important role in agriculture economy for example Myotis lucifugus

(Belwood and Fenton, 1976), Eptesicus fuscus (Whitaker 1995), Tadarida brasiliensis Mexicana

(Whitaker et al. 1996) and Pipistrellus mimus (Whitaker et al. 1999). The enormous insect

……………………………………………………………………………………………………Introduction consumption of bats is valuable to agriculture and particularly to local farmers which have attracted the farmers towards the role of bats as agricultural pest controlling agents (Murphy

1993; Whitaker 1993; Tuttle 1995). Agro-ecosystems underpin the economics of local, regional and nation and the value of pest control service rendered by bats helps to maintain the ecological integrity of agro-ecosystem. The most common insect orders consumed by bats are Coleoptera,

Lepidoptera, Diptera, Hymenoptera and Isoptera (Verts et al. 1999; Pavey et al. 2001).

Bats in Pakistan are considered fearsome and loathsome and their positive role in ecosystem has never been acknowledged in the country. Similarly, the biology and ecology of almost all chiropteran species in the country is poorly known. In the country there is serious lack of taxonomic capacity to identify bats on the basis of morphological features. There are a very few researchers who are interested to work on bats but they are poorly equipped to undertake taxonomic work. Hence the bats are rarely considered in environmental policies and educational campaigns. It is assumed that microchiropterans have descended from a common insectivorous ancestor. However, their taxonomy is continuously changing and being constantly revised as many cryptic species have been identified using sophisticated techniques and knowledge. The bats can be identified on the basis of external morphology and various skull parameters (Jacobs et al., 2006). Use of echolocation call parameters is also a useful technique for identifying morphologically similar bats (Jones and van Parijs 1993; Jacobs et al. 2006). Advancements in molecular techniques also aid taxonomists to correctly identify the species (Russo et al. 2006).

However, these techniques are less applicable due to highly priced bat detectors and expensive molecular techniques and the results are not immediately available (Weller et al. 2007). Due to these reasons, the bats biologists in most parts of the world generally and in developing countries especially use morphological characters to identify bat species (Harris 1974; Nagorsenand

……………………………………………………………………………………………………Introduction

Brigham 1993; Verts and Carraway 1998). Identification of bats on the basis of external body measurements and skull parameters is still a reliable method (Hill and Smith 1984; Vaughan et al. 2000 Jacobs et al. 2006) and use of character matrices and identification keys are authentic tools to identify different chiropteran species (Daniel 2009; Srinivasulu et al. 2010). Roberts

(1997) and Bates and Harrison (1997) are the only sources of literature in Indian region.

Although some work on bats of the country has been done in some parts of the country

(Mahmood-ul-Hassan et al. 2009; Javid 2011; Javid et al. 2012a,b; 2014) but the agroecosystems have never been explored.

Maximum diversity of bats is found in tropical belt of both the “Old” and “New” World and it is assumed that present chiropteran diversity has its origin from this belt. Hence, the bats are more abundant and diverse near Equator in tropical climates. However, a few species have successfully extended their ranges to the northern and southern temperate zones of tropics.

Human populations increased many folds during last couple of decades and resulted in to habitat modification and loss of habitats of various chiropteran species. Thus, conserving these habitats is critical to prevent further declines in bat populations (Racey and Entwistle 2003). However, in order to use this knowledge for local conservation plans detailed information on chiropteran diversity of the region is required (Hobbs 2004). In Pakistan, bats are amongst most misunderstood and feared creatures in human society. Many educated people dislike bats and view them as menacing, strange and demonic creatures. This mindset caused irremediable loss and mistreatment towards bats and they remained unexplored throughout the country

(Mahmood-ul-Hassan et al. 2009). The present work was therefore planned to explore bat fauna of the agro-ecosystems of central Punjab, as these areas have never been surveyed prior to this study.

CHAPTER 2

REVIEW OF LITERATURE

Mammalian adaptations enable them to withstand different environments and play their

ecological role in their native habitats. Hence, the biodiversity patterns and ecosystem processes

are largely affected by the native species of any area (Kalko 1997; Ramirez-Pulido et al. 2005).

One of the 26 mammalian orders, Chiroptera (bats) is well-known for its high diversity and

broad geographic distribution. The bats play different ecological roles such as seed, pollen, or

fruit eaters. Some bat species even consume small vertebrates and fish and can be found in

specific habitats (Fenton 1992; Hill and Smith 1985). The chiropterans are best environmental

indicators as they are the only mammals capable of true flight (Fenton 1992; Wilson and Reeder

1993) and found everywhere except Arctic, Antarctic and some isolated oceanic islands (Hutson

et al. 2001).

Bats generally have very specific roosting requirements, which differ among species.

They may roost in caves, crevices, trees, under logs and even in human dwellings. Bats may also use different types of roosts at different times. For example, a species that hibernates in a cave during the winter may use crevices in tree holes as roosts during warmer months (Behr and

Helversen 2004). The megachiropterans and the microchiropterans probably do not represent monophyletic lineages and are thought to have evolved separately and are regarded as two

different groups, (Bussche and Hoofer 2004). Microbats have a wider distribution than the Old

World megabats and are found in both the Old World and New World (Wund and Myers 2005).

Microbats rely on echolocation to find insects while flying quickly through the air. They do this

with startling efficiency. Under controlled conditions a Myotis bat (a small insectivorous bat

6 …………………………………………………………………………………………Review of Literature which lives near waterways) has been recorded capturing 1200 tiny fruit flies in one hour, one every three seconds, while navigating in the air. Most microbats feed on insects and are able to catch them while flying or while the insects are on a surface. Many species of microbats have chitinase enzymes in their intestines that are produced by symbiotic bacteria. These help in digesting the insect prey (Whitaker et al. 2004). However, microbats also employ a variety of other feeding behaviors. Some of the larger species hunt vertebrates, including birds, rodents, lizards, frogs, or even fish (Myers 2001).

Bats play a key role in maintaining biodiversity levels (Kunz and Pierson 1994; Simmons

2005). Their unique characteristics as echolocation and hibernation make them excellent subjects for research on evolution (Teeling et al. 2000; Li et al. 2007; Zhao et al. 2009), use of sound for perception (Griffin 1958) and a broad range of ecological topics (Kunz 1988). Their role in temperate and tropical climates is also of great importance. In temperate regions, most of the bats live as insectivores, consuming huge amounts of prey (up to half of their own weight every feeding night (Federico et al. 2008; Kalka et al. 2008; Williams-Guillen et al. 2008). Similarly in tropical climates, bats are playing important role in recovery of tropical forests by pollination and dispersing seeds of many plant species (Whittaker and Jones 1994; Kelm et al. 2008).

Parsons et al. (2006) conducted a survey to determine the distribution of microbats in temperate zones and concluded that bats are much active between the beginning of August and the end of October with a peak in September. Activity varied markedly from night to night and was affected by rainfall and residual maximum ambient temperature. Moon phase had no detectable influence on swarming activity. Activity was low in the first few hours after sunset of each night during the swarming period indicating that few bats emerged and that there was low daytime occupancy of the site. Activity increased to a peak between 6 and 7 hours after sunset

…………………………………………………………………………………………Review of Literature with a large number of bats arriving during early evening, activity then decreased gradually up to dawn as these bats departed again.

Francesco et al. (2000) studied ecology in relation to variation in forest landscapes in four localities of the eastern Niger Delta. The study areas were inhabited by thirteen species, seven megachiropterans and six microchiropterans. The majority of captures occurred in secondary forest habitat followed by primary forest and by the bush. A multivariate set of analyses arranged various species into six ecological groups. The various groups are interpreted in the light of the available information on the ecology and distribution of Nigerian bats.

Joshi and Vanlalnghaka (2005) conducted a survey to examine the distribution of microchiropteran bats, in constant darkness in a natural cave. The bats were exposed to repeated dawn or dusk twilight pulses at eight circadian phases. All bats exposed to dawn twilight pulses were entrained by advancing transients, and the stable entrainment was reached when the onset of activity occurred about 12 hour before the lights-on of the pulses, irrespective of the initial phase at which the bats were exposed to twilight. Delaying transients, however, entrained all bats exposed to dusk twilight pulses and the stable entrainment was reached when the onset of activity occurred about 1.6 hour after the lights-on of the pulses. The entrainment caused by dawn and dusk twilight pulses of the postulated photoreceptors. The short wavelength sensitive

(S) photoreceptors mediating entrainment via dusk twilight and the medium wavelength sensitive

(M) photoreceptors mediating entrainment via dawn twilight.

Hourigan et al. (2006) investigated the patterns of community structure of bats in relation to gradients of environmental variation in a tropical urban area. A total of 32 sites spread equally across eight habitat types were sampled in the city of Townsville, North Queensland, Australia.

Eleven species were confidently identified while a possible four more were identified only to the

…………………………………………………………………………………………Review of Literature genus level. Ordination of environmental variables measured at these sites identified two distinct environmental gradients reflecting the degree of urbanisation and foliage density. With increasing urbanisation there was a decline in species richness and total foraging activity. They used regression trees to characterise foraging preferences of each species. This analysis suggested that only one species of Mormopterus was able to exploit the resources provided by urbanisation. This species foraged in areas with higher numbers of white streetlights. The remaining species of bats preferred to forage within close proximity to natural vegetation and with low numbers of streetlights. The density of vegetation in long-established suburbs did not substantially reverse the trend for urban areas to have fewer bat species than original habitats.

The pteropodids (fruit bats) are most ancient group of bats with more than 170 species distributed in Africa, Asia and Indo-Australia (Hill and Smith, 1985). The diet is composed of fruits, flowers and nectar. Most of the pteropodids do not echolocate however Rousettus can echolocate by the clicking of its tongue. Pereswiet-Soltan (2007) differentiated European bat fauna into three categories i.e. thermophilic species, species adapted to milder climatic conditions and species of cold climate on the basis of Mediterranean, temperate, continental, hemiboreal and milder climatic zones. From the three groups, those of milder climate have a larger distribution latitudinally in Palaearctic Region.

Morphometric studies of bats allow inferences of ecological and behavioral aspects

(Mauricio et al., 2001). Characters like body mass, wing morphology and forearm length may be designated important parameters for autecological considerations (Aeshita et al., 2006).

Although extensive research on bats has been carried out in some parts of Southeast Asia

(Francis et al., 1996; 1997ab; 1999, Francis and Vonghamheng, 1998; Robinson, 1997;

Robinson and Webber, 1998) but in others there is extreme shortage of even basic information.

…………………………………………………………………………………………Review of Literature

Therefore it is very difficult to describe the status of the species either the species is abundant or

rare (Roberts, 1997; Mahmood-ul-Hassan et al., 2009).

The tropical landscapes are currently fragmented to varying degrees and have gaps or

have had their natural vegetation replaced. Thus, in these landscapes there are different sizes of

habitat fragments of natural or anthropogenically modified vegetation (i.e., crops, pastures,

human settlements, and secondary vegetation) to which the movement of many species of both

plants and animals is restricted. These changes do not affect all species equally since some are

favored by these modifications (Moreno and Halffter, 2001). Purohit and Senacha (2004)

explored the bat fauna of Jaisalmer and nearby areas of Great Indian Desert (The Thar), India

and found that number of chiropteran species had been changed that reported four decades back.

Out of three microchiropteran species (Rhinopoma microphyllum, Rhinopoma hardwickii and

Taphozous perforatus) reported from the region during the early sixties of twentieth century,

Taphozous perforatus had been vanished while one new species (Taphozous nudiventris) has

occupied the various sites of the region in due course of time.

Pottie et al. (2005) documented 24 microchiropteran species on the basis of the historical

mammalian literature and surveys for the small equatorial island nation of Singapore. The

records indicated that, of these 24 taxa, 15 are still present, another eight species, including all

three hipposiderids, have become locally extinct and one other is indeterminate. Almost half of the surviving species have very low abundances. Three new records of bat species in Singapore, namely Nycteris tragata, Rhinolophus lepidus and Murina suilla are assumed to have been present in the past but not detected in earlier surveys. Nycteris tragata and M. suilla are categorized as locally endangered. The vespertilionid, Myotis oreias, recorded previously only in

Singapore, was not found in the survey and may be globally extinct. Purohit and Vyas (2006)

…………………………………………………………………………………………Review of Literature randomly sampled bats from various roosting sites in and around Jodhpur, the Great Indian

Desert, to explore the sex ratio of different species of bats. Females were dominated in the population of Rhinopoma microphyllum, R. hardwickii, Taphozous nudiventris and Rhinolophus

Lepidus while in Pteropus giganteus, Taphozous perforatus and Scotophilus heathii males were dominated. Male and females shared equal percentage in population of Pipistrellus tenuis of this study area.

The geographic position of Pakistan is unique. It is situated at the western end of the

South Asian subcontinent which is a stitching precinct between the Palaearctic and the

Indomalayan region, two of the world’s six major zoogeographic regions. The country is also linked to the Ethiopian region through land stacks. In the eastern part of the country Indo-

Malayan forms are predominant, while the mountains of the north and west hold the Palaearctic forms. The Palaearctic species include a mixture of those common to a large part of Eurasia, along with resemblances to the Middle East, West Asia (Afghanistan and Iran), Central Asia and

Tibet. The unification elements from different origins ensure a unique and diverse mixture of fauna and flora (Roberts 1997; Mahmood-ul-Hassan et al. 2009). Majority of the insectivorous bats that occur in Pakistan roost tree hollows. Cavities in buildings are equally acceptable roost sites for a number of these species. In some instances, there are few trees remaining that contain suitable hollows in the lower altitude of a bat-tenanted building, and elimination of access to that roost site may remove a remnant bat population from an area (Roberts 1997).

The chiropteran biodiversity of Pakistan is comparable to any other region of the world with similar climatic conditions and topography. The bat fauna of the country is very diverse and is represented by 50 species, 26 genera and eight families (Roberts 1997; Mahmood-ul-Hassan and Nameer 2006) however it is the least studied taxon in Pakistan (Mahmood-ul-Hassan et al.

…………………………………………………………………………………………Review of Literature

2009). The taxonomy of many chiropteran species is unclear and based on museum surveys,

most of which were conducted before partition (Roberts 1997; Mahmood-ul-Hassan and Nameer

2006). The bats are given no legislative protection in south Asian countries. Only Sri Lankan

legislations fully protect to one sub species Rousettus leschenaulti seminudus. Other countries like Pakistan go to the other extreme of exempting bats from wildlife legislation. Bats are exempted from the regulation of international trade (Mickleburgh et al. 1992; Sheikh and Molur

2004). This bat species can be used as a useful non-primate laboratory model to study menstruation and menstrual dysfunctions in human beings as these bats exhibit a human like menstrual cycle both morphologically and physiologically (Zhang et al. 2007).

Mahmood-ul-Hassan et al. (2010) studied the diet of Indian flying fox (Pteropus giganteus) in

Pakistan from March 2008 to February 2009 and found that the bats fed on 20 species belonging to 11 plant families. Of these, four families (Anacardiaceae, Bignonaceae, Malvaceae, and

Sapotaceae) were identified from remnants of flower petals in food boluses while the remaining families (Annonaceae, Arecaceae, Ebenaceae, Meliaceae, Moraceae, Myrtaceae, and

Sapindaceae) were identified from the seeds in the boluses and from guano samples. The findings confirmed that the ecological services rendered by P. giganteus, such as pollination and seed dispersal, outweigh its losses, such as damage to the ripe fruit. Hence, the species should not be regarded as a pest; rather efforts should be made to ensure its conservation.

Mahmood-ul-Hassan et al. (2012) recorded Egyptian tomb bat, Taphozous perforatus from

Pakistan. Javid et al. (2012a) recorded the lesser mouse-tailed bat, Rhinopoma hardwickii from for the first time from Southern Punjab, Pakistan. Javid et al. (2012b) reported least pipistrelle

(Pipistrellus tenuis) from Islamabad after 1961. Mean body mass of the captured specimens was

…………………………………………………………………………………………Review of Literature

4.25 ± 1.061 g, the head and body length was 35.00 ± 2.828 mm, the forearm was 28.00 ± 0.707 mm long. The greatest length of the skull was 10.19 mm and baculum was 3.46 mm long.

Javid et al. (2014) captured Asiatic lesser yellow house bat (Scotophilus kuhlii ) from Punjab after 1920. The external body, cranial and bacular measurements of the captured specimens were compared with the available literature. The forearm length (n = 5) was 49.40 ± 3.03 mm,the greatest length of the skull (n = 4) was 18.98 ± 0.61 mm and C-M3 (n = 4) was 6.27 ± 0.49 mm.

The echolocation call parameters of 25 pulses from five calls of the species were also analyzed.

The mean frequency of maximum energy was 56.9 ± 3.6 kHz, the mean start and end call frequencies were 103.5 ± 12.3 kHz and 50.6 ± 1.0 kHz, respectively.

2.1. Species Account

2.1.1. Rousettus leschenaulti, genus Rousettus Gray, 1821 includes 10 species distributed from

Sri Lanka and Pakistan to Myanmar, Vietnam, southern China, Java and Bali (Simmons 2005;

Bates and Harrison 1997). Localized and broad distributions of certain taxa are found in this vast geographical area (Emerick and Duncan 1982; Nougier et al. 1986). Incidental descriptions of new species and accidental extensions of their recorded ranges demonstrate research on Asian species of Rousettus. Gray 1870 catalogued the fruit bat in British museum and on the basis of color; he separated three new ones from South Asia (Rookmaakek and Bergmans 1981).

Rousettus leschenaultii is rare and unevenly distributed species in Pakistan. It is migratory species, visit plains of Punjab and KPK during summer and migrates up to 1200 m (4000 ft). It has been recorded in Azad Kashmir, Malakand, Peshawer, Sialkot, Lahore and Karachi. But

Lahore and Karachi populations are persistent and do not migrate (Roberts 1977). Thumb in R. leschenaulti is well developed and the tail is small vestigial. The averages head and body length is 131 mm, average forearm length is 79 mm and ear length is 21 mm (Roberts 1977).

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Average greatest skull length in R. leschenaulti is 37.3 mm, average condylobasal length 35.8

mm, zygomatic breadth 22.5 mm, breadth of braincase 15.3, interobital constriction 7.6 mm and

mandibular length is 29.4 mm (Bates and Harrison 1997).

2.1.2. Rhinolophus lepidus was first captured by Mrs. Nora Pendleton from Abbottabad,

Pakistan. This was first country record. The species is data deficient and its status in Pakistan is

not clear (Roberts 1997); however, it is near threatened in South Asia (Walker and Molur 2003).

Average head and body length if R. lepidus is 42.9 mm, forearm length 39.8 mm, length of 5th metacarpal 31.1 mm, length of 4th metacarpal 31.4 mm, length of 3rd metacarpal 30.4 mm, length

of first phalanx of 3rd metacarpal 11.8 mm , length of 2nd phalanx of 3rd metacarpal 17.3 mm,

length of first phalanx of 4th metacarpal 8.7 mm, length of 2nd phalanx of 4th metacarpal 10.8

mm, ear length 16.9 mm, tail length 20.4 mm and hind foot length is 7.6 mm. Average greatest

skull length is 17.2 mm, condylocanine length 14.6 mm, breadth of the braincase 7.1 mm,

zygomatic breadth 8.2 mm, postorbital constriction 2.2 mm and mandibular length 11.0 mm

(Bates and Harrison 1997).

2.1.3. Rhinolophus blasii is considered to be a marginal species in Pakistan and perhaps

represented in the country by its subspecies R. b. meyeroemi (Corbet and Hill 1992). The

population status of the species in the Indian subcontinent is unknown (Bates and Harrison

1997). Z. B. Mirza and T. J. Roberts collected a single specimen of the species in 1968 from

Lahore (Roberts 1997) which is preserved in the museum of the Department of Zoology at the

University of the Punjab, Lahore. Average head and body length of single R. blasii specimen captured from Pakistan is 33 mm, forearm length 41 mm, tail length 21 mm and ear length 15 mm (Roberts 1977). The specimens from Iran are larger in size with forearm length 47. 8 mm, tail length 26.6 mm, hind foot length 13.3 mm and ear length 20.0 mm (DeBlase 1980). Average

…………………………………………………………………………………………Review of Literature greatest skull length of Iranian specimens is 19.7 mm, condylocanine length 16.5 mm, zygomatic breadth 9.2 mm, breadth of the braincase 8.6 mm, post orbital constriction 2.3 mm, mandibular length 12.2 mm (Deblase 1980).

2.1.4. Scotophilus heathii has wide geographically distribution range from Afghanistan to South

China, including Hainan Isl, south to Sri Lanka, Vietnam, Cambodia, Thailand and Burma. In

Pakistan this species seems very common and widely distributed in the Indus plains. It has been recorded from Kohat (KPK), Islamabad city, Multan, Lahore and Sialkot districts of Punjab and

Kashmoor, Sakkur, Jacobabad, Mirpur Sakro, Dadu, Landi, Malir, Karachi districts of Sindh

(Wroughton 1916a; Lindsay 1926; Siddiqui 1960; Taber et al. 1967; Walton 1974; Roberts

1997). IUCN has placed this species “Least Concern” category (IUCN 2008).The morphometric measurements of specimens captured by Walton (1974) from Malir,

Karachi and Mirpur Sakro. are as, average head and body length is 60 mm, tail length is 13 mm and forearm length is 58 mm. Roberts (1997). Walton captured six specimens from south-west

Punjab and Karachi and described various measurements of these specimens as follows, average head and body length is 55 mm, tail length is 12 mm and ear length is 16 mm. Bates and

Harrison (1997) captured sixty three bat specimens from Pakistan, India and Sri Lanka their measurements are as, average head and body length of these specimens is 82.5 mm, tail length

59.1 mm, and hind foot length of fifty eight S. heathii specimens is 12.0 mm and forearm length of sixty four specimens is 60.7 mm. Greatest skull length of sixty three specimens is 23.4 mm, condylocanine length 20.2 mm and brain case breadth of sixty two specimens is 10.2 mm and post-orbital constriction of sixty six bat specimens is 5.5 mm

2.1.5. Pipistrellus paterculus, individuals colony of hundred individuals in Kululai, Swat was explored by Walton in 1974, othr than this colony of P. paterculus no speciemen has been

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recorded from elsewhere in Pakistan (Roberts 1997). According to the IUCN 2008 report P.

paterculus is placed in LC category. Very little literature is available about the presence of P.

paterculus in Pakistan (Roberts 1997) and in the Indian subcontinent (Bates and Harrison 1997).

Measurements of specimens collected from India and Mynamar are as follows. Average head and body length is 44.8 mm, tail length is 33.7 mm, hind foot length is 6.5 mm, forearm length is

30.9 and ear length is 10.9 mm. Greatest skull length is 12.1 mm, Condylocanine length is 11.2 mm, Breadth of the braincase is 6.2 mm, postorbital constriction is 3.5 mm, mandible length is

8.8 mm (Bates and Harrison 1997).

2.1.6. Pipistrellus javanicus has a wide range of distributed in South and Southeast Asia, East

Afghanistan, Northern region of Pakistan,North and Central Indian region, South and East Tibet

(China), Burma, Thailand, Vietnam and Philippines; perhaps in Australia. No record is available on the distribution of this species in Pakistan, however record of a single specimen is available collected from Gharial, Murree Hills (Mahmood-ul-Hassan et al. 2009). P. javanicus is

included in ‘Least Concern’ category (IUCN 2008). Average head and body length of specimens

recorded from Pakistan, India, Nepal and Bangladesh is 47.1 mm, tail length is 33.9 mm, hind

foot length is 6.0 mm, average forearm length is 33.2 mm and the ear length is 11.8 mm (Bates

and Harrison 1997). Average greatest skull length is 13.6 mm, condylocanine length is 12.4 mm,

zygomatic breadth is 8.5 mm, breadth of braincase is 6.6 mm, postorbital constriction is 3.7 mm

and mandibular length is 9.9 mm. (Bates and Harrison 1997).

2.1.7. Pipistrellus tenuis is the smallest bat within the Indian subcontinent having an average,

forearm length of 27.7 mm. It is very difficult to discriminate it from individuals of

P.coromandra on the basis of forearm length. P.tenuis averages body mass is about 2 grams

(Gopalakrishna and Karim 1972). P.tenuis is distributed in Afghanistan to the Moluccas; S

…………………………………………………………………………………………Review of Literature

China, Laos, Vietnam, Cocos eeling Isles and Christmas Isle (Indian Ocean). P.tenuis has been documented from Malakand (Roberts 1997), Chitral (Sinha 1980), Multan and Chaklala (Hinton and Thomas 1926), Chakri, Gambat, Sukkur (Siddiqui 1961), Karachi, Malir (Walton 1974). The species is categorized as ‘Least Concern’. The measurements of the specimen captured from

India, Pakistan and Sri Lanka are as, average head and body length is 39.1 mm, tail length is 28.9 mm, hind foot length is 5.3 mm, forearm length is 27.7 mm (Bates and Harrison 1997). Greatest skull length is 11.5 mm, Condylocanine length is 10.2 mm, Zygomatic breadth is 7.4 mm,

Breadth of the braincase is 6.0 mm, postorbital constriction is 3.3 mm (Bates and Harrison

1997).

2.1.8. Pipistrellus ceylonicus seems to be common in Pakistan. The species is particularly abundant around Karachi and Thatta districts in Sindh. It is likely to be present in warmer southern latitudes in the Indus plains (Mahmood-ul-Hassan et al. 2009). Taber et al. (1967) collected it from Lyallpur (Faisalabad) and Khanewal. It is relatively large sized pipistrelle. Its ears, naked areas of face, wings and inter femoral membranes are uniform dark brown. The adult body mass ranges between seven to eight grams (Madhavan 1971). The muzzle in this species often has glandular swellings between the eyes (Roberts 1977). This species is distributed in

Pakistan, India, Sri Lanka, Bangla Desh, Burma, Kwangsi and Hainan (China), Vietnam, Borneo

(Mahmood-ul-Hassan et al. 2009).

Average head and body length of P. ceylonicus is 51 mm and average tail length 38 mm (range

36-44 mm) while the forearm was 35 mm long (Roberts 1997). Average greatest skull length of

P. ceylonicus is 15.0 mm, condylocanine length 13.7 mm, zygomatic breadth 9.8 mm, breadth of the braincase 7.3 mm, postorbital constriction 4.0 mm and mandibular length is 11.2 mm (Bates and Harrison 1997).

…………………………………………………………………………………………Review of Literature

2.1.9. Scotozous dormeri has distribution only in Pakistan and India. In Pakistan it has been recorded from Sialkot (Punjab) and Shikarpur (Sindh) (Sinha 1980); information on this species is based on a single specimen collected from Sialkot near Indian border. It has restricted distribution only in Indian subcontinent and the species is rare Pakistan (Mahmood-ul-Hassan et al. 2009) but abundant in Indian regions like Rajisthan (Advani 1983).

Average head and body length of P. dormeri is 52 mm, tail length 38 mm, hind foot length 9 mm, ear length 13 mm (Roberts, 1997). Average greatest skull length is 14.3 mm, condylocanine length 13.3 mm, zygomatic breadth 10.0 mm, breadth of braincase 7.1 mm, postorbital constriction 3.9 mm and length of mandible 10.8 mm (Bates and Harrison 1997).

Morphologically this species differs slightly from other pipistrelles in terms of its pelage color and the size and number of its incisors. Its fur is almost white on the ventral surface which in other pipistrelles is brownish grey. Secondly, it has a single pair of incisors in the upper jaw. If any second pair is present they are much reduced in size and are almost vestigial (Roberts 1997).

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

(Kashmore and Mirpur in Jacobabbad, Larkana, Sukkerand Dadu Districts) and Punjab

(Muzaffargarh and Sialkot). Its population status is uncertain and deserves further study

(Mahmood-ul-Hassan et al. 2009). Average head and body length of S. pallidus was recorded 54 mm, tail length 37 mm, hind foot length 8 mm, ear length 13 mm (Roberts, 1997). Average greatest skull length of S. pallidus is 15.1 mm, condylocanine length 14.1 mm, zygomatic breadth 10.5 mm, breadth of the braincase 7.7 mm, post-orbital constriction 4.3 mm and mandibular length 11.4 mm (Bates and Harrison, 1997).

…………………………………………………………………………………………Review of Literature

2.2. Statement of Problem

The study was designed to achieve following objectives;

1. To conduct an extensive survey of the study area for exploring bat diversity of that area. 2. To describe morphology, external body, cranial and bacular measurements of various bats inhabiting the study area. 3. To re-define geospatial and geographic distribution of bat fauna of the study area. 4. To record and analyze echolocation calls of these bat species.

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CHAPTER 3

EXPERIMENT NO. 1

Title: The bats of wheat-rice based agroecosystem of Punjab, Pakistan

Publications

3.1 Morphometrics of fulvous fruit bat (Rousettus leschenaulti) from Lahore,

Pakistan

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

3.2 Morphometrics of Blyth’s horseshoe bat, Rhinolopus lepidus Blyth, 1844 from

Gujranwala, Pakistan

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

3.3 The Blasius’ horseshoe bat Rhinolophus blasii (Chiroptera, Rhinolophidae) still

extend to Pakistan

(This manuscript has been published in Mammalia)

3.4 Recent Record of Scotophilus heathii from wheat-rice based agroecosystem of

Punjab

(This manuscript has been published in Pakistan Journal of Zoology)

3.5 Bat fauna of genus Pipistrellus from wheat-rice based agroecosystem of Punjab,

Pakistan

(This manuscript has been submitted for publication in Mammalia)

………………………………………………………………………………………………………Chapter 3

3.6 Recent Record of Desert Yellow House Bat, Scotoecus pallidus (Order

Chiroptera) from Punjab, Pakistan

(This manuscript has been accepted for publication in the Journal of Animal and Plant

Sciences)

………………………………………………………………………………………………………Chapter 3

MORPHOMETRICS OF FULVOUS FRUIT BAT (ROUSETTUS LESCHENAULTI) FROM

LAHORE, PAKISTAN

M. Shahbaz, A. Javid, T. Javed, M. Mahmood-ul-Hassan* and S.M. Hussain**

Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore

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

**Department of Zoology, Wildlife and Fisheries, Government College University, Faisalabad

Corresponding author’s email: [email protected]

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

Citation: Shahbaz, M., A. Javid, T. Javed, M. Mahmood-ul-Hassan and S.M. Hussain. 2014.

Morphometrics of fulvous fruit bat (Rousettus leschenaulti) from Lahore, Pakistan. The

Journal of Animal and Plant Sciences, 24 (3): 955-960.

………………………………………………………………………………………………………Chapter 3

Abstract

Present study on Fulvous fruit bat (Rousettus leschenaulti) from October 2011 to March 2012 in the vicinity of Lahore, Pakistan took morphometric measurements of 15 (9♂ and 6♀) bat specimens.

The average head and body length of all 15 specimens was 99.55 ± 15.035mm, forearm was 77.64 ±

6.373mm long, lengths of 3rd, 4th and 5th metacarpals were 52.73 ± 4.832 mm, 51.56 ± 4.996mm and

49.86 ± 3.998, respectively and the tail length was 11.1 ± 3.072mm. The greatest skull length (n= 9) was 35.89 ± 2.848mm, breadth of braincase was 15.44 ± 1.509mm while bacular length of a male specimen was 3.075mm.

Key words: Fulvous fruit bat, Greatest skull length, Baculum, Badian.

Introduction

The chiropteran diversity of Pakistan is comparable to any other region of the world with similar climatic conditions and topography. The bat fauna of the country is very diverse and is represented by 50 species, 26 genera and eight families (Roberts, 1997; Mahmood-ul-Hassan and Nameer, 2006) however it is amongst the least studied taxon in Pakistan (Mahmood-ul-Hassan et al., 2009). The taxonomy of many chiropteran species is unclear and based on museum surveys, most of which were conducted before partition (Roberts, 1997; Mahmood-ul-Hassan and Nameer, 2006). The bats are given no legislative protection in south Asian countries. Only Sri Lanka legislations fully protect to one sub species Rousettus leschenaulti seminudus. Other countries like Pakistan go to the other extreme of exempting bats from wildlife legislation. Bats are exempted from the regulation of international trade (Mickleburgh et al., 1992; Sheikh and Molur, 2004).

The Old World fruit bats play important role in pollination, seed dispersal and are important agents for maintaining plant community (Pijl, 1982; Marshall, 1985; Cox et al., 1991; Fujita and

Tuttle, 1991; Mickleburgh et al., 1992; Rainey et al., 1995; Eby, 1996; Banack, 1998). More than

………………………………………………………………………………………………………Chapter 3

114 plant species of world totally depend on Old World fruit bats (Chiroptera: Pteropodidae) for

their survival (Mickleburgh et al., 1992). Three genera and four species of pteropodids are found in

Pakistan (Roberts, 1997; Mahmood-ul-Hassan et al., 2009) including short nosed fruit bat

(Cynopterus sphinx), the Indian flying fox (Pteropus giganteus), the Egyptian fruit bat (Rousettus aegyptiacus) and the fulvous fruit bat (Rousettus leschenaulti). Rousettus leschenaulti can be used as a useful non-primate laboratory model to study menstruation and menstrual dysfunctions in human beings as these bats exhibit a human like menstrual cycle both morphologically and physiologically

(Zhang et al., 2007).

Genus Rousettus Gray, 1921 includes 10 species distributed in Sri Lanka, Pakistan,

Myanmar, Vietnam, southern China, Java and Bali (Simmons, 2005; Bates and Harrison, 1997).

Localized and broad distributions of certain taxa of bats are found in this vast geographical area

(Emerick and Duncan, 1982; Nougier et al., 1986).

Geoffroy (1810) described the first species presently included in the genus Rousettus Gray,

I82I, Pteropus amplexicaudatus from Timor and the closely related Pteropus leschenaulti from

South-East India was named by Desmarest (1820). Rousettus leschenaulti is distributed in Sri

Lanka, Pakistan, Vietnam, S. China, Peninsular Malaysia, Sumatra, Java, Bali, and Mentawai Isles

(Indonesia) (Simmons, 2005). This species is rare with erratic occurrence in Pakistan. It migrates to

Pakistan during summer season with migration pattern up to 1200 m elevation. It has been reported in Azad Kashmir, Malakand, Peshawer, Sialkot, Lahore and Karachi (Roberts, 1997; Bates and

Harrison, 1997). However, its populations at Lahore and Karachi show persistency and do not

migrate (Roberts, 1997; Mahmood-ul-Hassan et al., 2009).

Geographic variations in organisms have long been a matter of debate. These variations may

be due to the geographic factors which play important role in evolution. The variations are

………………………………………………………………………………………………………Chapter 3

associated with genetic variability among populations from different geographical areas which

provide basis for speciation, a fundamental prerequisite for evolution. Researchers

interested in geographic variations often search for repeated clines because repeated patterns provide

evidence of adaptation, and can be used to deduce possible causes of geographic variation (Endler,

1977). Morphometric studies of bats allow inferences of ecological and behavioral aspects (Mauricio et al., 2001). Characters like body mass, wing morphology and forearm length may be designated important parameters for autecological considerations (Aeshita et al., 2006).

Although extensive research on bats has been carried out in some parts of Southeast Asia

(Francis et al., 1996; 1997ab; 1999, Francis and Vonghamheng, 1998; Robinson, 1997; Robinson and Webber, 1998) but in other parts of this region there is shortage of even basic information about bats. Therefore, it is very difficult to describe the status of a species whether abundant or rare

(Roberts, 1997; Mahmood-ul-Hassan et al., 2009). In Pakistan, the taxonomy, distribution, ecology and biology of most of the chiropteran species is little known. Most of the information is based on the original description of the species since it has not been collected subsequently. Similarly, there are no environmental policies or educational projects for bats. Keeping in mind the scarcity of knowledge about bats in Pakistan present study was conducted to find out bat roosts and elaborate morphological characters of fulvous fruit bat (Rousettus leschenaulti) in urban area of Lahore city.

Materials and Methods

The study was conducted from October 2011 to March 2012 in Lahore District to find out roosts of

Rousettus leschenaulti and to note its morphological characteristics.

Sampling strategy and species identification: Exploratory visits were made to the study area to search for potential bat roosts such as old and undisturbed buildings, ruins, abandoned wells, farm houses, tree groves and forest plantations. Local people were also interviewed for gleaning

………………………………………………………………………………………………………Chapter 3

maximum information about the exact location of bat roosts. Mist nets and hand net were used to

capture the specimens from the roosts. A day bat roost of Rousettus leschenaulti was observed at

Badian, Lahore. Mist nets were erected at the point of emergence firstly on January 18, 2012 in

evening hours (5:00 PM). This netting effort resulted in capture of 7 (4♂ and 3♀) Rousettus

leschenaulti specimen and 8 (5♂ and 3♀) specimens were captured in subsequent visit on March 14,

2012.

The species was identified in the field on the basis of external morphology following Bates and

Harrison (1997) and brought to laboratory for external body measurements, cranial and bacular

analysis.

External morphology: Each captured bat was placed in a separate cotton bat bag during mist

netting and at the completion of a netting session, each bat was weighed up to 0.1 g (Pesola balance

10050, Swiss made) euthanized and preserved in a plastic jar in absolute alcohol. Field number, sex,

age and exact locality of each bat were noted on the plastic jar. The external body measurements

were taken using a digital vernier caliper (0-150 mm). These measurements included head and body

length, ear length, forearm length, claw length, 2nd claw length, thumb length, length of each

metacarpal including its phalanges, wing span, penis length, tibia length, calcar length, hind foot, tail

length, and free tail length following Dietz (2005).

Cranial measurements: Skulls were prepared for recording cranial measurements of bat specimens

(n= 9) by removing eye balls, tongue and excessive flesh. The brain tissue was macerated and removed using forceps and cotton and cranial cavity was washed with a jet of water. Skulls thus cleaned were kept overnight in a dilute solution (0.2 % of Potassium Hydroxide (KOH)). After being thoroughly washed in tap water again, the skulls were kept in absolute alcohol for a night before being transferred to acetone for another night. Each of the dry skulls was stored in a properly labeled

………………………………………………………………………………………………………Chapter 3 vial padded with cotton. The greatest skull length, condylo-basal length, condylo-canine length, zygomatic breadth, interorbial constriction, postorbital constriction, maxillary toothrow length, mandibular toothrow length, posterior palatal width and anterior palatal width were measured following Bates et al. (2005).

Bacular measurements: Penis of a male bat 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 transferred to a plastic tube containing

5% KOH and a pinch of alizarin red powder. After 24 hours, the stained baculum was dissected out of the tissue and stored in glycerin in a labeled test tube following Bates et al. (2005). Total length of baculum, shaft length, width of proximal branch and width of distal branch were taken using vernier caliper.

Results and Discussion

Bat biologists in most parts of the world, especially in the underdeveloped countries, are using characters such as forehead slope, dorsal pelage sheen, and behavior of the bats to discriminate species (Harris, 1974; Nagorsen and Brigham, 1993; Verts and Carraway, 1998). Bat identification on the basis of external morphology and measurements of different skull parameters (Hill and Smith,

1985; Vaughan et al., 2000; Jacobs et al., 2006) is still a highly reliable technique in most instances.

Use of character matrices and identification keys are authentic tools to identify different chiropteran species (Daniel, 2009; Srinivasulu et al., 2010).

The average head and body length of 15 specimens was 99.55 ± 15.035 mm, the ears were

18.27 ± 3.494 mm long, average thumb and claw lengths were 12.43 ± 1.687 mm and 3.47 ± 0.640 mm, respectively (Table 1). Second claw length was recorded 2.73 ± 0.704 mm, the forearm was

77.64 ± 6.373 mm long, length of 3rd metacarpal, 1st phalanx on 3rd metacarpal and 2nd phalanx on

………………………………………………………………………………………………………Chapter 3

3rd metacarpal were 52.73 ± 4.832 mm, 34.00 ± 3.742 mm and 40.63 ± 4.908 mm, respectively.

Length of 4th metacarpal, 1st phalanx on 4th metacarpal and 2nd phalanx on 4th metacarpal were 51.56

± 4.996 mm, 34.00 ± 3.742 mm and 40.63 ± 4.908 mm, respectively. Length of 5th metacarpal was

49.86 ± 3.998 mm and its 1st phalanx was 49.86 ± 3.998 mm long. Wing span was 398.79 ± 56.771 mm, tibia length 37.24 ± 4.773 mm, calcar length 5.76 ± 1.321 mm, hind foot length 18.07 ± 2.554 mm and tail length was 11.1 ± 3.072 mm. Average penes length of 9 male specimens was 8.22 ±

3.022 mm (Table 1). The data obtained during the present study was compared with earlier studies on this species from India (Bates and Harrison, 1997) and Pakistan (Roberts, 1977) (Table 2). The mean values for head and body length, ear length, forearm length, hind foot length and tail lengths of all 15 Rousettus leschenaulti were smaller than recorded by Roberts (1977) and Bates and Harrison

(1997) while the upper limits of all these parameters fall within the ranges given by Roberts (1977) and Bates and Harrison (1997).

Combined mean greatest skull length was 35.89 ± 2.848 mm. The Codylo-basal and condylocanine lengths were 34.67 ± 2.958 mm and 33.50 ± 2.761 mm, respectively. The zygomatic and braincase breadths were 19.78 ± 3.866 mm and 15.44 ± 1.509 mm, respectively. Interorbital and postorbital constrictions were 7.67 ± 0.500 mm and 3.00 ± 0.000 mm, respectively. Maxillary and mandibular toothrow lengths were 13.44 ± 1.667 mm and 14.67 ± 1.785 mm, respectively. The posterior palatal width was 9.33 ± 0.866 mm while anterior palatal width was 6.94 ± 0.635 mm

(Table 1, Figure 1).

The data regarding cranial measurements of the species was not previously reported from

Pakistan, therefore the cranial parameters were compared only with that of Bates and Harrison

(1997). The mean breadth of braincase of nine R. leschenaulti captured during the present study was larger while zygomatic breadth and greatest length of skull were smaller than recorded by Bates and

………………………………………………………………………………………………………Chapter 3

Harrison (1997). However, all the other cranial measurements of currently studied specimens were within the ranges given by Bates and Harrison (1997).

Total length of baculum of a single specimen was 3.075 mm. The shaft was 1.275 mm long.

The proximal and distal branch widths were 0.925 mm and 0.800 mm, respectively (Table 1, Figure

2). The baculum of a single specimen captured from Sri Lanka was peg-shaped and its length was

3.6 mm (Bates and Harrison, 1997).

Table 1. Mean external body, cranial and bacular measurements (mm) of Rousettus leschenaulti captured from Badian, Lahore. (n is the number of specimens).

Body Parameters Males (n=9) Females (n=6) Combined Mean ±SD(Range) Head and body length 104.68±16.120 91.83±9.908 99.55±15.035(80-125) Ear length 19.77±2.991 16.00±3.098 18.27±3.494(12-24) Thumb length 13.04±1.649 11.50±1.378 12.43±1.687(9-16) Claw length 3.44±0.527 3.50±0.837 3.47±0.640(3-5) 2nd claw length 2.77±0.833 2.66±0.516 2.73±0.704(2-4) Forearm length 79.14±5.767 75.33±7.062 77.64±6.373(67-85) Length of 3rd metacarpal 54.22±4.658 50.50±4.550 52.73±4.832(44-60) 1st phalanx on 3rd metacarpal 34.77±3.114 32.22±4.579 34±3.742(27-38) 2nd phalanx on 3rd metacarpal 41.88±4.807 38.75±4.835 40.63±4.908(33-48) Length of 4th metacarpal 53.22±4.604 49.08±4.862 51.56±4.996(43-60) 1st phalanx on 4th metacarpal 27.50±3.122 25.00±2.683 26.5±3.122(22-33) 2nd phalanx on 4th metacarpal 28.72±4.324 25.00±3.464 27.23±4.305(20-34) Length of 5th metacarpal 52.00±3.808 48.16±3.971 49.86±3.998(43-56) 1st phalanx on 5th metacarpal 25.88±2.784 23.50±2.665 25±3.998(20-30) Wing span 421.16 ±54.434 365.23±45.074 398.79 ± 56.771(30-51) Tibia length 38.90±4.448 35.08±4.779 37.24±4.773(30-43) Calcar length 5.94±1.333 5.50±1.378 5.76±1.321(4-8) Hind foot length 19.45±2.126 16.67±1.941 18.07±2.554(13-22) Tail length 12.16±2.667 10.33±3.724 11.1±3.072(5-16) Penis length 8.22±3.022 0.00±0.000 8.22±3.022 (4-12) Cranial Parameters Males (n=5 ) Females (n=4 ) Combined Mean ± SD(Range) Greatest skull length 36.80±2.950 34.75±2.630 35.89±2.848(32-39) Condylo-basal length 35.80±2.950 33.25±2.630 34.67±2.958(31-38) Condylo-canine length 34.40±2.702 32.375±2.750 33.50±2.761(30-37) Zygomatic breadth 21.80±3.834 17.25±2.217 19.78±3.866(15-24) Breadth of braincase 15.20±0.837 15.75±2.217 15.44±1.509(14-19) Interorbial constriction 7.80±0.447 7.50±0.577 7.67±0.500(7-8) Postorbital constriction 3.00±0.000 3.00±0.000 3.00±0.000(3-3) Maxillary toothrow length 13.80±1.643 13.00±1.826 13.44±1.667(11-15) Mandibular toothrow length 15.10±1.746 14.12±1.931 14.67±1.785(12-16) Posterior palatal width 9.60±0.894 9.00±0.816 9.33±0.866(8-10) Anterior palatal width 7.00±0.707 6.87±0.629 6.94±0.635(6-8) Bacular Parameters n = 1 Total length of baculum 3.075 mm Length of shaft 1.275 mm Width of proximal branch 0.925 mm Width of distal branch 0.800 mm

………………………………………………………………………………………………………Chapter 3

Figure 2. Baculum of Rousettus leschenaulti captured Figure 1. Cranial features of Rousettus leschenaulti from Lahore captured from Lahore

Table 2. Comparison of mean external body and cranial measurements of Rousettus leschenaulti (I = Roberts (1977; II = Bates and Harrison (1997); III = Present study).

II III I Parameters n=37 n=15 (mm) Head and Body Length 131 (120-145) 125.9 (111-147) 99.54 (80-125) Ear length 21 (19-23) 20.8 (17.5-24) 18.26 (12-24) Forearm 79 80.6 (75-86) 77.64 (67-85) Hind foot 18.7 (15-22) 18.07 (13-22) Tail 14 (10-18) 15.6 (8-21) 11.1 (5-16) Breadth of braincase - 15.3 (14.4-16) 15.44 (14-19) Zygomatic breadth - 22.5 (20.2-24) 19.77 (15-24) Greatest length of skull - 37.3 (34.9-39.4) 35.88 (32-39) *Range is mentioned in parenthesis.

………………………………………………………………………………………………………Chapter 3

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MORPHOMETRICS OF BLYTH’S HORSESHOE BAT RHINOLOPUS LEPIDUS

BLYTH, 1844 FROM GUJRANWALA, PAKISTAN

Muhammad Shahbaz1, Arshad Javid1, Muhammad Ashraf3 and Syed Makhdoom Hussain4

1Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore

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

3Department of Fisheries and Aquaculture, University of Veterinary and Animal Sciences,

Lahore

4Department of Zoology, Wildlife and Fisheries, Government College University, Faisalabad

Corresponding author’s email: [email protected]

(This paper has been accepted for publication in Pakistan Journal of Zoology)

………………………………………………………………………………………………………Chapter 3

Abstract

Rhinolophus lepidus is an endemic bat of southeast Asian region but the status of the species from its native territory is still unknown. From territorial limits of Pakistan, the species was reported in 1985 from Abbotabad, Khyber Pakhtunkhwa province. During present study a bat roost containing 70 R. lepidus was found at Rasul Nagar (32º 19.687 N, 073º 46.922 E), district

Gujranwala from an underground cellar of an old temple and out of these, 10 (4♂, 6♀) were captured with the help of a hand net. The average head and body length of all the captured specimens was 42.36±1.1 mm, forearm length was 40.34±0.75 mm, greatest skull length (n= 2) was 17.5± 0.49 mm while baculum (n= 2) was 4.35 ± 0.38 mm long. The present record is first from the study area and the Punjab province.

Key words: Abbottabad, forearm length, bacular length, range extension, Gujranwala

Introduction

Chiropterans are second largest and most diverse group of small mammals after Rodentia but least studied in Pakistan (Javid et al., 2012a,b). The members of this group are unique in their vagrancy (Turmelle and Olival, 2009) and many species have changed their distribution range during past century (Taber et al., 1967; Javid et al., 2013). Horseshoe bats are characterized by their muzzle having complex folds of skin, a noseleaf (Bates and Harrison, 1997), resembling horseshoe. The breadth of the noseleaf is 6.0-8.0 mm and covers the whole muzzle (Csorba et al., 2003). The exact function of these facial folded structures has yet to be determined, but bat biologists believe they may have help in echolocation calls.

Family Rhinolophidae is represented by a single genus Rhinolophus. The genus is comprised of more than 77 species (Simmons, 2005) which are distributed throughout the

Afrotropical, Australian, Indomalayan, Oceanian and Palaearctic regions (Csorba et al., 2003;

………………………………………………………………………………………………………Chapter 3

Stoffberg et al., 2010). The genus is represented by five species in Pakistan (Roberts, 1997).

Blyth’s bat is easy to identify, because it is small in size. Rhinolophus lepidus is usually larger in

size than R. pusillus with a notched connecting process but in general morphology of the

noseleaf the species is comparable to R. pusillus. R. Lepidus however can be differentiated from

R. pusiluss with longer forearm and tibia (Bates and Harrison, 1997). R. lepidus is a very small

horseshoe bat with forearm length of 31 to 42 mm (Roberts, 1997).

This species inhabits forested landscapes (Brosset 1962), but Prakash (1963) reported it

from desert of Bikaner. Sinha (1973) suggested that R. lepidus has restricted distribution in hilly

areas of Bihar. It is found at different altitudes ranging from 246-2338 meters in Utter Pradesh

(Wroughton, 1914; Hinton and Lindsay, 1926). The species has diurnal shelter roosts in caves,

subterranean soils, tunnels (Brosset, 1962), old houses (Sinha, 1986) and ruined temples (Lal and

Biswas, 1985). They live solitary or in groups, sometimes in compact clusters of dozen to several

hundred individuals (Bates and Harrison, 1997). R. lepidus is an insectivorous bat, preys on

small insects of order Diptera and Coleoptera (Brosset, 1962) and Hymenopteran (Sinha, 1986).

It flies slowly at lower elevations and frequently visits trees branches for capturing tree insects

(Bates and Harrison, 1997). There is not any eminent threat to this species in Indian region as a

whole, however threats are emerging due to roost disturbance and tourism related activities at old

forts and havelis (Molur et al., 2002).

Rhinolophus lepidus has wide range of distribution from Afghanistan to Pakistan, north

India, Nepal, Burma, Thailand, southern China, Peninsular Malaysia and Sumatra (Simmon,

2005). In India the species has been reported from Rajesthan (Prakash, 1963; Sinha 1979;

Senacha, 2003) and Madhia Pradesh (Wroughton, 1913; Brosset, 1962; Khajuria, 1980). From

Pakistan the species was firstly recorded from Abbottabad in 1985 (Roberts, 1997; Bates and

………………………………………………………………………………………………………Chapter 3

Harrison, 1997; Mahmood-ul-Hassan, et al., 2009). Focus of the present study was to check the presence or absence of R. lepidus bat from central Punjab from where the species has never been documented prior to this survey.

Materials and Methods

Three main rice producing districts of the Punjab province namely Gujranwala,

Hafizabad and Mandi Bhauddin were surveyed from January 2011 to December 2012 to find out the bat fauna of the agroecosystem of the country. Three netting nights in each month and one night in each district were spent throughout the study period for collection of bats. Bats were captured with the help of mist and hand nets. In search of potential bat roosts in the area, old and undisturbed temples, buildings, ruins, abandoned wells, farm houses, tree groves and forest plantations were explored. Local people were also interviewed for getting maximum information about the bat roosts in the areas. A bat roost of 70 Rhinolophus lepidus was explored on August

3, 2012 from an under ground room (Figure 1) of a temple at Rasul Nagar (32º19.687 N,

073º46.922 E) and out of the total 70, ten (4♂, 6♀) R. lepidus were captured with the help of a hand net.

The captured specimens were euthanized, placed in cotton bat bags and each specimen was weighed up to 0.1 g (Pesola balance 10050, Swiss made). These specimens were preserved in a marked plastic jar in absolute alcohol and bat number, sex, age, exact locality and district of capture was noted on the jar. The preserved specimens were brought to the laboratory for further study and analysis. The morphometric measurements were taken with the help of 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) and Javid

………………………………………………………………………………………………………Chapter 3

(2011). Identification was made on the basis of morphological observations and comparisons of

morphometric measurements given by the Bates and Harrison (1997).

Results and Discussion

Rhinolophus lepidus has geographically widespread distribution but least studied in the

Indian subcontinent (Bates and Harrison, 1997). The species is a new record for Pakistan and the first specimens were captured by Mrs Nora Pendleton in 1985 from inside the down-sloping mine shaft near Abbotabad located at about 1280m elevation the species also have been reported from Afghanistan (Corbet and Hill, 1992; Sinha, 1980). Therefore, its occurrence in Pakistan is non unexpected (Roberts, 1997). Sinha (1980) encountered the species hanging from ceilings of dark temples. During present survey a bat roost of 70 R. lepidus was explored in an under ground room of a temple at Rasul Nagar (32º19.687 N, 073º46.922 E) located at an elevation of 197m.

Taxonomists seek help from basic characters such as dorsal hair color, behavior and forehead slope for discriminating the species (Nagorsen and Brigham, 1993; Verts and

Carraway, 1998). The members of the genus Rhinolophus are distinguished by body size, position of the upper premolar and the differences in the shape and size of nose leaves (Maree and Grant, 1997). Andersen (1905) found in his taxonomic and phylogenetic arrangement that all

Rhinolophus groups with Palaeotropical distribution i.e. R. simplex, R. lepidus, R. philippinensis and R. macrotis had the most ancestral species in Asia (Dejtaradol, 2009). The dorsal hair color of the captured specimens is grey-brown, belly is paler and the ears are pointed without tragus but have antitragal lobe. The horseshoe structure is relatively narrow and does not cover all the muzzle of mouth, lancet of horseshoe has pointed tip and has concave sides. Noseleaf has a smaller sella on it. Our findings are inline with the observation of Roberts (1997) and Bates and

………………………………………………………………………………………………………Chapter 3

Harrison (1997). Rhinolophus lepidus is a small sized bat with an average forearm length of

40.34±0.75mm. 3rd metacarpal of the forearm is shorter than the 4th metacarpal.

Bats identification on the basis of external body measurements and skull parameters is still a highly reliable method in many ways (Hill and Smith, 1984; Vaughan et al., 2000; Jacobs et al., 2006) and application of character matrices and identification keys are authentic tools to identify different chiropteran species (Srinivasulu et al., 2010a,b). Roberts (1997) and Bates and

Harrison (1997) are the only sources of literature in Indian region. During present study, 10

Rhinolophus lepidus were captured from the study area. The external body, cranial and bacular measurements of captured specimens were compared with Bates and Harrison (1997). The average head and body length of these 10 specimens was 42.36mm and the forearm was 40.3mm long. The blyth’s horseshoe bat has longer 4th metacarpal than 3rd and 5th metacarpals in length

(Bates and Harrison, 1997). Average length of 3rd, 4th and 5th metacarpals of the specimens

captured during present study was 31.28 mm, 32 mm and 31.48 mm, respectively. The average

wingspan of the captured specimens was 240.10mm and tail was 22.79mm long. The average

greatest skull length of R. lepidus (n = 2) was 17.5mm. Generally the baculum is short and lies in

the glans but in some species like R. lepidus it is very long, above 75% of the penis length

(Sinha, 1976). Average total length of baculum of four specimens captured during present study

was 4.35mm (Figure 2) while the average of penis was 6.57mm.

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………………………………………………………………………………………………………Chapter 3

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………………………………………………………………………………………………………Chapter 3

Table 1. Body weight (g), external body, cranial and bacular measurements (mm) of Rhinolophus lepidus (mean and range when at least two specimens were recorded) captured from Rasul Nagar, Gujranwala.

External body Present study Bates and Cranial Measurement n = 2 Bates and measurements (n = 10) Harrison Harrison (1997) (1997) Body mass 6.42(5.0-8.20) - Breadth of braincase 7.5(7.3-7.7) 7.1(6.5-7.8) Head and body length 42.36(41-44.6) 42.9(35-54) Zygomatic breadth 8.5(83-8.7) 8.2(7.6-8.8) Ear length 13.49(11-16) 16.9(14.5-20.6) Postorbital constriction 2.3(2.2-2.4) 2.2(1.8-2.6) Forearm length 40.34(39-42) 39.8(37-41.8) Condylo-canine length 14.2(14-14.4) 14.6(13.8-15.5) 3rd metacarpal length 31.28(30-32.4) 30.4(28.2-33.3) Condylo-basal length 14.8(14.6-15) - 3rdmetacarpal: 1st phalanx 12.35(11.7-13) 11.8(10.0-13.3) Greatest length of skull 17.5(16.8-17.5) 17.2(16.2-18.4) 3rd metacarpal: 2nd phalanx 19(17-23) 17.3(16-18.9) Maxillary toothrow 6.75(6.5-7) 6.1(5.6-6.8) 4th metacarpal length 32.0(30.8-33) 31.4(29.6-33.8) Anterior palatal width 4.3(4.2-4.4) 4.0(3.7-4.2) 4th metacarpal: 1st phalanx 9.68(9-11) 8.7(7.6-10.5) Posterior palatal width 6.3(6.2-6.4) 5.9(5.7-6.3) 4th metacarpal: 2nd phalanx 11.55(9-13) 10.8(9.6-12.3) Mandibular toothrow 5.6(5.5-5.8) 6.6(6-7.4) 5th metacarpal length 31.48(30.4-32.7) 31.1(29.4-33.4) Mandible length 11.2(11-11.4) 11(10.0-12.1) 5th metacarpal: 1st phalanx 10.61(9.8-11.5) - Bacular measurements n = 2 Wingspan 240.10(220.9-250.2) 244(232-256) Total length of baculum 4.35(4.06-4.61) - Tibia length 17.19(16.5-18.1) 16.7(14.9-18.4) Length of shaft 3.85(3.69-4.02) - Hind foot length 8.78(8-10.5) 7.6(5.5-10) Length of proximal 0.53(0.46-0.61) - branch Tail length 22.79(21-26) 20.4(14-28) Height of baculum 1.30(1.23-1.38) - Penis length 6.57(6-7) - - - -

(a) (b) (c)

Figure 1. Photographs showing (a) external view of the temple where the Rhinolophus lepidus are roosting, (b) inner view, (c) facial features of R. lepidus

Figure 2. Photograph of the baculum of Rhinolophus lepidus showing its shape

………………………………………………………………………………………………………Chapter 3

The Blasius’ horseshoe bat Rhinolophus blasii (Chiroptera, Rhinolophidae) still extends to Pakistan

Arshad Javid1, Muhammad Shahbaz1, Muhammad Mahmood-ul-Hassan2 and Syed Makhdoom

Hussain3

1Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore 2Department of Zoology and Fisheries, University of Agriculture, Faisalabad 3Department of Zoology, Wildlife and Fisheries, Government College University, Faisalabad

Corresponding Author’s Email: [email protected]

(This paper has been published in Mammalia)

Citation: Javid, A., M. Shahbaz, M. Mahmood-ul-Hassan and S.M. Hussain. 2014. The Blasius’

horseshoe bat Rhinolophus blasii (Chiroptera, Rhinolophidae) still extends to Pakistan.

Mammalia, DOI 10.1515/mammalia-2013-0161.

………………………………………………………………………………………………………Chapter 3

Abstract

Specimens of Rhinolophus blasii were captured in Manawa, district Lahore 43 years after the first

and single ascertained record in Pakistan. External, cranial and bacular measurements of R. blasii are

given for the first time in the country.

Key words: morphometrics; distribution; Punjab

Rhinolophus, the only genus of family Rhinolophidae is the second most diversified bat

genus, with 71 and 77 species recognized by Csorba et al. (2003) and Simmons (2005) respectively.

From a centre of evolution in South-East Asia (Bogdanowicz and Owen 1992) rhinolophids

extended across the Old World from rainforest to dry savanna and predertic areas through southern

temperate habitats.

Rhinolophus blasii Peters, 1866 has one of the largest range both in the Palaearctic and the

Afrotropics, where it is patchily distributed, extending marginally into the Indomalayan region

(Simmons 2005) including only one confirmed specimen in Pakistan, which was collected on 28

December 1968 in Lahore (Roberts 1977); a kin labeled ‘Mekran coast’ in the British Museum

(Natural History) may have been collected in either Iran or Pakistan (DeBlase 1980).

Then Rhinolophus blasii, possibly R. blasii meyeroemi Felten, 1977 according to Corbet and

Hill (1992) is considered to be a marginal species in Pakistan and the population status of the species in the Indian subcontinent is unknown (Bates and Harrison 1997). The finding of five horseshoe bats hanging in an underground cellar is the first record of R. blasii after 43 years.

These horseshoe bats were identified in the field by a short third metacarpal and second phalanx of the fourth finger, and additionally by the connective process of sella which was very

………………………………………………………………………………………………………Chapter 3 much pointed and rose to quite a prominent slender point (figure 1a). The body fur was very long and dense, dorsal hairs being whitish brown at base and dark grey brown at tips.

This small group was recorded on 21 January 2011 from Manawa (31º35.647, 074º27.660,

217 m a.s.l.) in Lahore district. Located on the left bank of river Ravi this city is the second most populated in Pakistan. Hot and moist climate prevails during summer (mean July temperature: 32 ºC) and colder during winter season (mean January temperature: 13 ºC). The city receives an average annual rainfall of 650 mm but the rainfall is more frequent during monsoon (Qadir et al. 2008, Ullah et al. 2009). Undulating and low alluvial plains are the characteristics of the area (Naeem et al.

2007). Irrigation system supply extensive agricultural areas and gardens detrimental to and caused expansion of the city at the expense of Sub Tropical Thorn Forest ecozone (Champion et al. 1965,

Chaudhry 1990).

These specimens of R. blasii (1♂, 2♀) were captured with an hand net, placed in cotton bags and weighed up to 0.1 g (Pesola balance 10050, Swiss made) before being euthanized and preserved in absolute alcohol. The bottles were assigned field number (MMH210111.1, MMH210111.2 and

MMH210111.3). In the laboratory external body measurements (table 1) were recorded using a digital vernier caliper (0-150 mm). These measurements were used to ascertain the identification of the captured bat and to compare them with published data (DeBlase 1980, Roberts 1997, Csorba et al. 2003). Skulls were prepared for recording cranial measurements following Bates et al. (2005).

Penis of the male specimen was cut down and the baculum prepared and measured following Bates et al. (2005). Its shape (figure 1b) with cylindrical shaft, quite deep basal cone and without dorsal emargination is in accordance with Csorba et al. (2003).

………………………………………………………………………………………………………Chapter 3

External and cranial measurements of the three collected specimens (table 1), and the former specimen reported by Roberts (1997) are smaller than those of a large set of specimens from Iran

(DeBlase 1980). On the other hand, all the measurements except length of 5th metacarpal and maxillary toothrow length fall within the ranges given by Csorba et al. (2003). According to Felten et al. (1977) the samples collected from Iran and Afghanistan represent a large subspecies, R. b. meyeroehmi Felten, 1977. This was anticipated by Aellen (1959) who reported that specimens from the eastern part of the range were larger and supported by Corbet and Hill (1992). However, Kock and Howell (1988) pointed out that Pakistanese population could not belong to R. b. meyeroehmi.

R. blasii is one of the five species of Rhinolophus in Pakistan. Two are part of the Palaearctic fauna (R. ferrumequinum and R. hipposideros) and two range in the Indo-Malayan region (R. lepidus and R. macrotis). In the area R. blasii prefer to live in arid to semi-arid conditions and lives in temples, ruins and abandoned cellars and buildings (Bates and Harrison 1997). In the Mediterranean region they mainly roost in caves and other underground sites (Aulagnier et al. 2009) and typically forage in shrubland and woodland, although it may penetrate to desert habitat in Jordan (Amr 2000).

In Punjab the areas in close vicinity of Lahore should be further explored to find out the species and it necessitate further analysis whether the subspecies recorded from Pakistan is R. blasii meyeroemi.

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quality of Lahore area, Punjab, Pakistan. J. appl. Sci. 7: 41-46.

Qadir, A., R.N. Malik and S.Z. Hussain. 2008. Spatio-temporal variations in water quality of Nullah

Aik-tributary of the river Chenab, Pakistan. Environ. Monit. Assess. 140: 43-59.

Roberts, T.J. 1977. The Mammals of Pakistan. Ernest Benn Ltd., London, UK. 361 pp.

Roberts, T.J. 1997. The Mammals of Pakistan. Oxford University 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 ed. The Johns Hopkins University Press,

Baltimore, MD. pp. 312-529.

Ullah, R., R.N. Malik and A. Qadir. 2009. Assessment of groundwater contamination in an industrial city, Sialkot, Pakistan. Afr. J. Environ. Sci. Technol. 3: 429-446.

………………………………………………………………………………………………………Chapter 3

(a) (b)

Figure 1. Noseleaf (a) and baculum (b) of R. blasii from Manawa (Lahore, Pakistan)

………………………………………………………………………………………………………Chapter 3

Table 1. External, cranial and bacular measurements (in mm, except weight in g) of Rhinolophus blasii (mean and range when at least two specimens were recorded).

DeBlase 1980 Csorba et al. 2003 Roberts This note Measurements 1977 (mm) Body mass - - - 8.56±0.58 Head and body length 55.8(47-64) - 33 39.33±0.58 Tail length 26.6(21-35) (15.4-35.0) 21 19.23±1.94 Ear length 20.0(15.8-22.0) (15.0-22.0) 15 15.67±1.26 Forearm length 47. 8(43-50) (40.0-51.0) 41 40.17±1.16 Hind foot length 10.3(8.0-11.0) - - 7.90±0.36 Third metacarpal (3mt) - (28.5-33.5) - 30.67±0.76 First phalanx of 3mt - - - 12.13±0.90 Second phalanx of 3mt - - - 19.10±1.02 Fourth metacarpal (4mt) - (30.9-36.5) - 31.43±0.51 First phalanx of 4mt - - - 9.43±0.60 Second phalanx of 4mt - - - 12.27±1.12 Fifth metacarpal - (32.6-38.5) - 30.90±0.96 First phalanx of 5mt - - - 10.20±0.17 Wing span - - - 212.33±2.52 Tibia length - - - 17.00±0.50 Calcar length - - - 5.00±0.00 Penis length - - - 7.00 Greatest length of skull 19.7(19.1-20.1) 19.20(18.17-19.98) - 17.22 Condylo-canine length 16.5(16.0-17.0) - - 16.01 Condylo-basal length - - 16.50 Zygomatic breadth 9.2(8.8-9.5) 9.21(8.09-9.88) - 8.32 Breadth of braincase 8.6(8.2-9.1) - - 7.50 Postorbital constriction 2.3(2.2-2.8) - - 1.51 Maxillary toothrow length (C-M3) 6.4(6.0-7.6) 6.70(5.65-7.10) - 4.93 Anterior palatal width - - - 4.54 Posterior palatal width - - - 6.24 Mandible length 12.2(11.9-12.7) 12.05(10.99-12.80) - 11.80

Mandibular toothrow length (C-M3) 7.00(6.9-7.2) 7.00(6.01-7.62) - 7.00 Total bacular length - - - 3.5 Shaft length - - - 2.5 Proximal branch length - - - 1.0 Proximal branch width - - - 1.0 Distal branch length - - - 0.0 Distal branch width - - - 0.5 Baculum height - - - 1.1

………………………………………………………………………………………………………Chapter 3

Recent Record of Scotophilus heathii From Wheat-Rice Based Agroecosystem of Punjab

Muhammad Shahbaz,1 Arshad Javid,1 Muhammad Mahmood-ul-Hassan,2 Syed Makhdoom

Hussain,3 Sana Ashraf1 and Muhammad Idnan1

1Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore

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

3Department of Zoology, Wildlife and Fisheries, Government College University, Faisalabad

(This paper has been published in Pakistan Journal of Zoology)

Citation: Shahbaz, M., A. Javid, M. Mahmood-ul-Hassan, S.M. Hussain, S. Ashraf and M.

Idnan. 2014. Recent record of Scotophilus heathii from wheat-rice based

agroecosystem of Punjab. Pakistan Journal of Zoology, 46(4): 1175-1179.

………………………………………………………………………………………………………Chapter 3

Abstract

December 2012 and a total of 33 S. heathii were captured. The external body, cranial and bacular measurements of the captured specimens were compared with available literature. The average head and body length of all 33 captured specimens was 73.7±4.4 mm, forearm length was 60.6±4.1 mm, greatest skull length (n = 6) was 18.7±1.7 mm while baculum (n = 1) was

3.075 mm long. The cranial and bacular features of the species which are important traits for mammalian identification are reported for the first time in country and this is also the first record of the species from study area.

Key words: cranial measurements, baculum size, agro-ecosystem, Gujranwala

Introduction

Worldwide, genus Scotophilus is represented by 12 species with distribution ranges from South

Africa to Senegal, Sudan, Somalia and Madagascar, Arabia, Afghanistan to Indonesia, Philippines and Taiwan (Koopman, 1993). In Indian subcontinent this genus is represented by two species namely greater Asiatic yellow house bat territorial limits of Pakistan (Bates and Harrison, 1997;

Srinvasulu et al., 2010; Javid et al., 2014). In Pakistan, S. heathii is common and wide spread throughout the Indus plains and has been reported from Kohat (Khyber Pakhtunkhwa), Islamabad,

Sanghoi, Bhattu Hisar, Multan Lahore and Sialkot (Punjab), and Kashmoor, Sakkur, Jacobabad

(Wroughton, 1916), Mirpur Sakro (Lindsay, 1927), Dadu, Landi, Malir, Karachi (Sindh) (Siddiqui,

1960; Taber et al., 1967; Walton, 1974).

………………………………………………………………………………………………………Chapter 3

Scotophilus heathii roosts in variety of habitats, in crevices and hollows of old buildings, tree hollows, banyan and peepal trees, abandoned wells, ruins (Sinha, 1986), leaves and crowns of coconut and palm (Phillips, 1980). The species lives singly or in colonies that vary up to 50 individuals (Sinha, 1986). The species is often mixed with its congener in the Indian region the larger species were initially recognized as S. kuhlii and smaller as temmnickii and wroughtoni.

However, larger specimens of this genus were later referred to as S. heathii and both the species were correctly recognized (i) larger ones as S. heathii and (ii) smaller ones as S. kuhlii (Hill and

Thonglongya, 1972; Corbet and Hill, 1992; Koopman, 1993; Bates and Harrison, 1997; Simmons,

2005).

Apparently S. heathii is a common and widespread species worldwide however during surveys in Sri Lanka only one specimen was collected during 1990s (Bates and Harrison, 1997). The present study is unique as S. heathii has never been reported from the study area prior to this survey.

Materials and Methods

This two year study extending from January 2011 to December 2012 was conducted in areas of wheat-rice based agro-ecosystem of Punjab province. These areas are comprised of three districts namely Gujranwala, Hafizabad and Mandi-Bhaudin in central Punjab, which is most populated province of Pakistan. 19 sampling stations (Table I) were fixed in these three districts and netting efforts were made to ascertain the presence or absence of Scotophilus heathii. Three nights in each month, one night in each district was spent throughout the study period and bats were captured with the help of mist and hand nets. For locating potential bat roosts in the study area old and undisturbed buildings, ruins, abandoned wells, farm houses, tree groves and forest plantations were searched.

People of the study area were also interviewed for getting maximum information about the exact

………………………………………………………………………………………………………Chapter 3

Table I.- Sampling sites in three districts of wheat-rice based agroecosystem of Punjab.

Sampling sites District Longitude Latitude

Civil hospital, Gujranwala Gujranwala 74°11.583 E 32°10.203 9 N Qadirabad colony Gujranwala 73°41.563 E 32°17.490 N Kelaske village Gujranwala 73 º58.668 E 32 º10.803 N Gakhar mandi town Gujranwala 74°08.791 E 32°18.340 N Rasul nagar village Gujranwala 73º46.720 E 32º19.68 N Ali pur chattha town Gujranwala 74º09.361 E 32º11.272 N Verpal chattha village Gujranwala 73º58.803 E 32º 10.803 N District katchery, Hafizabad Hafizabad 73°34.918 E 31 º58.018 N Kot sarwar, village Hafizabad 73 º30.189 E 31 º55.148 N Nothain village Hafizabad 73 º32.770 E 31 º56.241 N Kaleki mandi village Hafizabad 73°42.697 E 32°04.150 N Sukheki mandi village Hafizabad 73º34.108 E 31º61.116 N Pindi bhattian town Hafizabad 73 º16.895 E 31 º55.148 N Jalal pur bhatian village Hafizabad 73º22.51 E 32º02.39 N Farid town Mandi Bhaudin 73º30.46 E 32º35.123 N Phalia town Mandi Bhaudin 73º58.13 E 32º43.601 N Malikwal town Mandi Bhaudin 73º45.08 E 32º35.102 N Head rasul Rest House Mandi Bhaudin 73º31.148 32º40.096 Mano chak Mandi Bhaudin 73º45.29 32º25.308

location of bat roosts.

Once the bat specimens were captured, they were euthanized, placed in cotton bat bags and each

specimen was weighed up to 0.1 g (Pesola balance 10050, Swiss made). Each bat was preserved in a

plastic jar in absolute alcohol and brought to laboratory for further observations and analysis. The external body 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).

Results and Discussion

There is dire need to identify bats for better ecological research and conservation of taxa. The

insectivorous bats are pest control agents and there is a strong relationship between bat morphology

………………………………………………………………………………………………………Chapter 3

and prey selection (Nadeem et al., 2013; Weterings and Umponstira, 2014). Bats identification on the basis of external body measurements and skull parameters is still a highly reliable method (Hill

and Smith, 1984; Vaughan et al., 2000; Jacobs et al., 2006) and application of character matrices and

identification keys are authentic tools to identify different chiropteran species (Daniel, 2009;

Srinivasulu et al., 2010). Roberts (1997) and Bates and Harrison (1997) are the only sources of

literature in Indian region. Scotophilus heathii has been reported from sea level to an elevation of

1,500 m (Molur et al., 2002). During present survey, a total of 33 S. heathii specimens were captured

from an elevation of 1700 m. The external body, cranial and bacular measurements of captured

specimens were compared with Walton (1974), Roberts (1997) and Bates and Harrison (1997)

(Table II). The average head and body length of all 33 S. heathii was 73.7±4.4 mm while the forearm

was 60.6 ± 3.4 mm long. The lengths of 3rd, 4th and 5th metacarpals were 59.7±2.5 mm, 58.7±2.4 mm

and 54.5±1.7 mm, respectively. The average wingspan of the captured specimens was 355±30.1 mm

and tail was 53.3±4.3 mm long. The average greatest skull length of six S. heathii was 18.7±1.7 mm.

Average total length of baculum of five specimens was 1.6±0.11 mm (Table II). The baculum of

Scotophilus lies in the glans penis and it is duckbilled shaped (Harrison and Brownlow, 1978). The

bacular shape of one of the specimens is represented in Figure 1.

Average values for head and body length and tail length of all the 33 specimens captured

during the present survey are within the ranges given by Roberts (1997) and Bates and Harrison

(1997) while the same measurements are smaller than the specimens’ recorded by Walton (1974).

The mean values of forearm length and hind foot length of the currently captured specimens are

within the ranges given by Walton (1974), Roberts (1997) and Bates and Harrison (1997). Similarly,

the mean values of the 3rd, 4th and 5th metacarpals fall within the ranges mentioned by Roberts (1997)

………………………………………………………………………………………………………Chapter 3

and Bates and Harrison (1997). Mean breadth of braincase, mandibular tooth row and mandible

length of six S. heathii captured during present study are within the ranges recorded by Bates and

Harrison (1997) (Table II).

Fig. 1. Baculum of Scotophilus heathii showing its shape

References

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

Museum, Sevenoaks, UK, pp. 258.

Bates, P., Thong, D. and Bumrungsri, S., 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), pp. 12.

Corbet, G.B. and Hill, J. E., 1992. A World List of Mammalian Species, Third edition. Natural

History Museum Publications & Oxford University Press, London and Oxford.: v-viii, 1-243.

Daniel, B.A., 2009. Bat taxonomy and echolocation workshop for researchers at M.K.U. Small

………………………………………………………………………………………………………Chapter 3

Mammal Mail: Bi-annual Newsletter of CCINSA and RISCINSA 1(2).

Harrison, D.L. and Brownlow, I. P., 1978. Mammalia, 42: 123-130.

Hill, J. and Smith, J., 1984. Bats: A natural history. Austin: University of Texas Press.

Hill, J.E. and Thonglongya, K., 1972. Bull. Brit. Mus. (Nat. Hist.), 22: 171 – 196.

Jacobs, D.S., Eick, G. N., Schoeman, M.C. and Matthee, C. A., 2006. J. Mammal, 87:161–170.

Javid, A., Mahmood-Ul-Hassan, M., Hussain, S.M. and Iqbal, K.J., 2014. Mammalia, 78: 133-137.

Koopman, K. F., 1993. Order Chiroptera (137 -241). In: Mammal species of the world: a taxonomic

and geographic reference eds. (D.E. Wilson and D.M. Reeder). 2nd ed. Smithsonian Institution

Press, Washington, D.C. 137-241.

Lindsay, H.M., 1927. [i] Report No 43: Nelliampathy plateau and Palni Hills [591-597]; [ii] Report

No 44: Kangra and Chamba [597-606]; [iii] Report No 45: The Punjab Salt Range and Murree

[606-614]; Bombay Natural History Society’s Mammal Survey of India. J. Bombay nat. Hist.

Soc., 31: 591-614.

Molur, S., Marimuthu, G., Srinivasulu, C., Mistry, S., Hutson, A. M., Bates, P. J. J., Walker, S.,

Priya, K. P. and Priya, A.R.B., 2002. Status of South Asian Chiroptera: Conservation,

Assessment and Management Plan (CAMP) Workshop report, 2002. Zoo Outreach

Organization CBSG South Asia and WILD, Coimbatore, India, viii+141pp+CD-ROM.

Nadeem, M.S., Sara, Z., Kayani, A.R., Muhammad M.; Beg, M.A. and Nasir, M.F., 2013.

Distribution and roosting habitats of some microchiropteran bats in Rawalpindi district,

Pakistan. Pak. J. Zool., 45 (2): 565-569.

Phillips, W.W.A., 1980. Mammal of the mammals of Sri Lanka. Part-I. Wildlife and Nature

Protection Society of Sri Lanka.1-116.

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Roberts, T.J., 1997. The mammals of Pakistan. Oxford University Press, Karachi, Pakistan. pp 525.

Siddiqi, M. S., 1961. Biologia, 7: 93-225.

Simmons, N. B., 2005. Order Chiroptera. In: Mammal species of the world: a taxonomic and

geographic reference (eds. D.E. Wilson and D.M. Reeder). 3rd ed. The Johns Hopkin

University Press, Baltimore, MD. pp. 312-529.

Sinha, Y.P., 1986. The bats of Bihar: taxonomy and field ecology. Rec. Zool. Survey India, Misc.

Publ., Occasional Pap.77: 1-60.

Srinivasulu, C., Racey, P.A. and Mistry, S., 2010. J. Threat. Taxa, 2: 1001-1076.

Taber, R.D., Sheri, A.N. and Ahmad, M.S., 1967. J. Mammal, 48: 392-407.

Vaughan, T., Ryan, J. and Czaplewski, N., 2000. Mammalogy, 4th Edition. Toronto: Brooks Cole.

Walton, D.W., 1974. J. Mammal. Soc. Jpn. 6: 43-50.

Weterings. R. and Umponstira, C., 2014. eJ Biol., 10: 21-27.

Wroughton, R.C., 1916. J. Bombay nat. Hist. Soc., 24:291–316.

………………………………………………………………………………………………………Chapter 3

Table II.- Body mass (g), external, cranial and bacular measurements (mm) of Scotophilus heathii captured from wheat-rice based agro ecosystem of Punjab, Pakistan (mean ± standard deviation (minimum - maximum) (n is the number of specimens).

External body Present Walton Roberts Bates and Cranial Present study Bates and measurements study (1974) (1997) Harrison measurements (n = 6) Harrison (n = 33) (1997) (1997)

Body mass 30.9±5.4 - (36-39) - Breadth of braincase 9.3±0.9 10.2 (9.7-10.8) Head and body length 73.7±4.4 142 83 82.5 Zygomatic breadth 13.7±1.0 15.6 (14.5-16.9 (72-92) (67-93) Ear length 14.6±1.8 - 16 16.9 Postorbital 5.1±0.8 5.5 (5.2-5.9) (14-7) (13.0- constriction 20.2) Tragus length 8.16±0.73 - - - Condylo-canine 17.8±1.8 20.2 (19.0-21.3) length Thumb length 9.1±0.93 - - - Condylo-basal length 18.3±1.8 - Claw length 2.5±.39 - - - Greatest length of 18.7±1.7 23.4 (21.7-25.2) skull Forearm length 60.6±3.4 58 - 60.7 Maxillary too throw 6.8±1.0 7.7 (7.1-8.4) (55.4- 65.8) 3rd metacarpal length 59.7±2.5 - - 59.4 Anterior palatal width 6.1±1.0 - (53.7- 64.8) 3rd metacarpal: 1st 19.9±1.5 - - - Posterior palatal 8.4±1.3 10.0 phalanx width 3rd metacarpal: 2nd 15.7±1.6 - - - Mandibular too throw 7.9±1.0 8.8 (8.1-9.6) phalanx 4th metacarpal length 58.7±2.4 - - 58.2 Mandible length 14.1±1.9 16.3 (14.8-18) (54.0- 63.9) 4th metacarpal: 1st 15.9±.96 - - - Bacular n = 5 - phalanx measurements 4th metacarpal: 11.6±1.4 - - - Total length of 1.6±0.11 - 2ndphalanx vacuum 5th metacarpal length 54.5±1.7 - - 54.6 Length of shaft 1.4±0.23 - (50.3- 59.2) 5th metacarpal: 1st 11.1±2.1 - - - Length of proximal 0.20±0.02 5-3 phalanx branch Wingspan 355±30.1 - - - Length of distal 0.04±0.01 - branch Tibia length 23.9±1.2 - - - Width of proximal 0.87±0.07 - branch Calcar length 6.3±0.93 - - - Width of distal 0.43±0.01 - branch Hind foot length 12.7±1.5 13 12 12.0 Height of baculum 0.37±0.05 - (11-13) (9.0-15.0) Tail length 53.3±4.3 60 55 59.1 - - - (51-60) (43.0- 71.0) Penis length 7.7±0.90 ------

………………………………………………………………………………………………………Chapter 3

Bat fauna of genus Pipistrellus from wheat-rice based agroecosystem of Punjab, Pakistan

Arshad Javid1, Muhammad Shahbaz1, Muhammad Mahmood-ul-Hassan2, Muhammad Ashraf3

and Syed Makhdoom Hussain4

1Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore

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

3Department of Fisheries and Aquaculture, University of Veterinary and Animal Sciences,

Lahore

4Department of Zoology, Wildlife and Fisheries, Government College University, Faisalabad

(This paper has been submitted for publication in Mammalia)

………………………………………………………………………………………………………Chapter 3

Abstract

Three rice producing districts viz. Gujranwala, Hafizabad and Mandi Bhauddin in Pakistan were

surveyed to explore bat fauna of genus Pipistrellus in central Punjab from January 2011 to

December 2012. A total of 172 specimens of genus Pipistrellus belonging to six species i.e. P.

pipistrellus (n = 43), P. paterculus (n = 12), P. javanicus (n = 39), P. tenuis (n = 18), P. cylonicus (n = 40) and P. dormeri (n = 20) were captured. All these species are reported for the first time from study area while P. pipistrellus and P. paterculus from Punjab province. The shape and length of baculum were the characters that help in clear cut identification of various

Pipistrellus species. The external body, cranial and bacular features of the species were compared with available literature.

Key words: Chiroptera; Baculum; District Gujranwala

Introduction

Genus Pipistrellus is represented by 51 species (Koopman 1993) with distribution ranges

extending from central southern Africa, throughout Eurasia to Japan, Indonesia, New Guinea,

Solomon Islands and northern Australia with occurrence in Canada, USA and Mexico. In Indian

Subcontinent the genus is represented by 12 species (Bates and Harrison 1997) while eight species have been reported from territorial limits of Pakistan (Roberts 1997). Members of genus

Pipistrellus are small and their external features resemble Eptesicus. The nostrils in these bats are directed antero-laterally with a distinct internarial groove. The ears are small and roundly pointed with short and bluntly shaped tragus (Roberts 1997). It is difficult to identify the species

from one another on the basis of external morphology however the cranial and bacular features

aid significantly to discriminate various species (Hill and Harrison 1987).

………………………………………………………………………………………………………Chapter 3

Pipistrellus pipistrellus ranges from Britain and southern Scandinavia through Europe,

China and India to Japan and Taiwan it also present in Morocco. In Pakistan, P. pipistrellus has

been recoded from Gilgit (Blanford, 1888-91) in Northern areas; Kulali and Dir, Chitral in KPK

(Walton 1974).

Pipistrellus javanicus ranges from Afghanistan, Pakistan and India to Myanmar,

Indonesia, Philippines, Korea, Japan, New Guinea and perhaps Australia. In Asia, P. javanicus has wide spread distribution ranging from Afghanistan, Pakistan, and India to Mayanmar,

Indonesia, Philippines, Korea, Japan, New Guinea and perhaps in Australia. In Pakistan the species has been reported from Karakar pass (KPK) and pine forest of Gharial Muree Hills

(Punjab) (Roberts 1977).

Pipistrellus tenuis ranges from Afghanistan, Pakistan, India and Sri Lanka to Vietnam and Thailand. In Pakistan, the species has been reported from Malakand (Roberts 1977) and

Chitral (Sinha 1980) in KPK; Multan, Bhatu Hisar, Chaklala (Hinton and Thomas 1926), Chakri

(Siddiqi 1961), Khanewal, Sheikhpura (Districts) in Punjab (BMNH) and Gambat; Sukur

(Siddiqi 1961), Karachi and Malir (Walton 1974) in Sindh and Islamabad (Javid et al. 2012a).

Pipistrellus paterculus is geographically distributed in northern India, Burma, Thailand,

Vietnam and south-west China. In Pakistan the species has been reported from Kululai (KPK) and very little is known about this bat in the country (Roberts, 1997).

Pipistrellus ceylonicus ranges from Pakistan, India and Sri Lanka to Myanmar, China,

Vietnam and northern Borneo. The species in Pakistan has been reported from Landhi

(Wroughton 1916), Malir (Walton 1974), Karachi and Thatta in Sindh and Lyallpur and

Khanewal (Roberts 1977) in Punjab.

………………………………………………………………………………………………………Chapter 3

Pipistrellus dormerii is confined to India and Pakistan only (Roberts 1997, Bates and

Harrison 1997). In Pakistan, the species has been reported from Sialkot in Punjab and Shikarpur

(Sinha, 1980) in Sindh (Roberts 1997).

Literature regarding bat fauna of Pakistan is scarce and there is dire need to explore these environment friendly creatures in various parts of country (Javid et al. 2014a,b). During present survey, the agro-ecosystems of Punjab province were searched to find out the chiropteran diversity belonging to the genus Pipistrellus.

Materials and Methods

Three districts of the Punjab province Gujranwala, Hafizabad and Mandi-Bhaudin were explored to find out species of bats belonging to the genus Pipistrellus. Punjab is the most populated province of the country and the districts comprising study area constitute the core rice producing belt, hence the natural ecosystems have been replaced by the agro-ecosystems to fulfill the food and shelter requirements of increasing human population. These districts lie about

200 m above sea, average annual rainfall is about 950 mm but the rains are more frequent during monsoon. The temperature varies from 4°C during winter to above 40°C during summer (Qadir et al., 2008; Ullah et al., 2009).

This two year study extending from January 2011 to December 2012 was conducted in areas of wheat-rice based agro-ecosystem of Punjab province. These areas are comprised of three districts namely Gujranwala, Hafizabad and Mandi Bhaudin. All these three districts were explored for collection of bats and location of their roosts. Three nights in each month, one night in each district was spent throughout the study period at different sampling station (Table 1) and bats were captured with the help of mist and hand nets. For locating potential bat roosts in the study area, old and undisturbed buildings, ruins, abandoned wells, farm houses, tree groves and

………………………………………………………………………………………………………Chapter 3 forest plantations were searched. People of the study area were also interviewed for getting maximum information about exact location of bat roosts.

Once the bat specimens were captured, they were euthanized, placed in cotton bat bags and each specimen was weighed up to 0.1 g (Pesola balance 10050, Swiss made). Each bat was preserved in a plastic jar in absolute alcohol, its number, sex, age, exact locality and district of capture was noted on the jar. These specimens were brought to the laboratory for further observations and analysis. The external body 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) and Javid (2011).

Results and Discussion

During present survey, a total of 172 specimens belonging to six species of genus Pipistrellus were captured. These include Pipistrellus pipistrellus (n = 43), P. paterculus (n = 12), P. javanicus (n = 39), P. tenuis (n = 18), P. cylonicus (n = 40) and P. dormeri (n = 20). All these six species are the first reports from the study area as the bat fauna of the study area was never documented prior to present investigation. However, P. pipistrellus and P. paterculus are the new provincial records and never recorded from Punjab province before present survey. The external body, cranial and bacular measurements of captured specimens of belonging to genus

Pipistrellus were compared with available literature (Table 2 & 3).

Pipistrellus pipistrellus is a small sized narrow winged bat with forearm length 27-31 mm. The ears are broad but short in length, tragus is 4.2 mm long about half of the ear’s length.

The hairs are reddish brown on dorsal and slightly paler on ventral side. Average condyle-canine length is 10.9 mm. Baculum is very small, with narrow extended shaft and distal end is bifid but proximal basal lobes are well developed (Bates and Harrison 1997). A total of 43 P. pipistrellus

………………………………………………………………………………………………………Chapter 3

specimens were captured from study area during present survey. Average body mass of all these

captured specimens was 3.3 g and the average forearm length was 28.9 cm. Average condyle-

canine length (n = 3) was 10.3 mm while the average bacular length (n = 2) was 1.6 mm.

Pipistrellus javanicus is a medium size bat with forearm length 33-35 mm. Ears are short

and rounded with long tragus, pelage color of dorsal side is brown, wing membranes and ears are

blackish-brown (Chan et al. 2009). Average condyle-canine length is 12.4 mm. Baculum has

long narrow shaft with distal bifid tips with well- developed proximal lobes. The average body

mass of all the twelve P. javanicus captured during present study was 7.6 g and the average

forearm length was 34.2 mm. Average condyle-canine length (n = 3) was 11.3 mm while the

average bacular length was 6.0 mm.

Pipistrellus tenuis is a very small sized bat having average body weight of 3-4 g (Ingle and Heaney 1992, Javid et al. 2012) and forearm length 27-29 mm. This is the smallest bat of the

Indian subcontinent and is known as least pipistrelle or Indian pygmy bat. Morphologically P.

tenuis and P. coromandra are very similar but can be differentiated on the basis of cranial

characters (Bates and Harrison 1997, Javid et al. 2012). The baculum of P. tenuis has thin long

shaft with distinct distal bifid tip and well developed proximal lobes (Hill and Harrison 1987,

Javid et al. 2012). Average body mass of all the 18 P. tenuis specimens captured during present

survey was 3.6 g. Average forearm length 29.2 mm, the condyle-canine length (n = 3) was 8.7

mm and average bacuar length (n = 2) was 3.8 mm.

Pipistrellus paterculus is a small sized bat with average forearm length 30 mm. The hairs

are long and pelage color is dark brown on the head and back while ventral surface, belly hair

tips are pale ginger brown. Average condyle-canine length is 11.2 mm. P. paterculus has large

baculum with long narrow shaft and distal end has bifid tip (Bates and Harrison 1997).Total of

………………………………………………………………………………………………………Chapter 3 twelve specimens of P. paterculus was captured during present study have an average body mass

3 g, average forearm length was 30.5 mm, the condyle-canine length was 11.0 mm and average baculum length (n = 2) was 9.4 mm.

Pipistrellus ceylonicus are relatively large sized pipistrellus species with an average forearm length of 37.2 mm (Bates and Harrison, 1997) and weight 8 g (Roberts, 1997).Ears, face and interfemoral membranes are dark brown in color. Some part of interfemoral membrane near main body, tail and femora is hairy (Bates and Harrison, 1997). Dorsal pelage color of the species is greyish, red or golden brown while the ventral hairs are pale grey. The baculum has short upwardly curved shaft, bifid tip and well developed proximal lobes (Bates and Harrison,

1997).Average body mass of 40 P. ceylonicus specimens captured during present survey was 3.7 g. Average forearm length was 35.3 mm, the condyle-canine length (n = 3) was 12.7 mm while average length of baculum (n = 2) was 9.4 mm long.

Pipistrellus dormeri is a medium sized pipistrelle with an average forearm length of 34.4 mm and body mass 6.0-7.0 g (Madhavan 1978), tail is short than head and body length. Hairs are dark brown on dorsal surface with grey brown tips, and paler with whitish tips on ventral surface.

Average condyle-canine length 13.3 mm. Baculum has long narrow, slightly sinuous shaft and broadened, weakly bifid tip, the base is slightly broadened and bifid (Bates and Harrison 1997).

Average body mass of 12 P. dormeir specimens captured during present study was 5 g, average forearm length was 34.5 mm, condyle-canine length (n = 2) 13.5 mm and total bacular length (n

= 2) was 3.2 mm.

References

Bates, P.J.J. and D.L. Harrison. 1997. Bats of the Indian subcontinent. Harrison Zoological

Museum, Sevenoaks, UK. pp. 258.

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Bates, P.J.J., D. Thong and S. Bumrungsri. 2005. Voucher specimen preparation: bats. In (P.J.J.

Bates, ed.) Taxonomic initiative for Southeast Asian bat studies (Vietnam, Thailand, Cambodia and Lao PDR). Harrison Institute, Sevenoaks. pp. 1 – 12.

Blanford, W.T. 1888-91. The Fauna of British India, Mammalia. Taylor and Francis, London.

617 pp.

Chan, K.W., K.K.P. Lim and T.M. Leong. 2009. The java pipistrelle, Pipistrellus javanicus

(Mammalia: Chiroptera: Vespertilionidae) in Singapore. Nature in Singapore. 2: 323-327.

Hill, J.E. and D.L. Harrison. 1987. The baculum in the Vespertilioninae (Chiroptera:

Vespertilionidae) with a systematic review, a synopsis of Pipistrellus and Eptesicus, and the description of a new genus and subgenus. Bulletin Brit. Mus. nat. Hist. (Zool.) 52: 225-305.

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. J. Bombay Nat. Hist. Soc. 31:606

– 614.

Ingle, N.R. and L.R. Heaney. 1992. A key to the bats of the Philippine Islands. Field Museum of

Natural History. Fieldiana: Zoology, 69: 1-44.

Javid, A. 2011. Bat biodiversity (Vespertilioniformes: Order Chiroptera) in some tropical and arid-subtropical regions of Pakistan. PhD Thesis. Department of Wildlife and Ecology,

University of Veterinary and Animal Sciences, Lahore-Pakistan. pp. 196.

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. 2014a. Recent record of the lesser yellow house bat (Scotophilus kuhlii) from Punjab, Pakistan. Mammalia 78: 133–137.

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Javid, A., M. Shahbaz, M. Mahmood-ul-Hassan and S.M. Hussain. 2014b. The Blasius’ horseshoe bat Rhinolophus blasii (Chiroptera, Rhinolophidae) still extends to Pakistan.

Mammalia, DOI 10.1515/mammalia-2013-0161.

Koopman, K.F. 1993. Order Chiroptera. In: (D.E. Wilson and D.M. Reeder, eds.) Mammal species of the world: a taxonomic and geographic reference. 2nd ed. Smithsonian Institution

Press, Washington, D.C. pp. 137 -241.

Madhavan, A. 1978. Breeding habits and associated phenomena in some Indian bats. Part 5-

Pipistrellus dormeri (Dobson) – Vespertilionidae. Journal Bombay nat. Hist. Soc. 75(2): 426-

433.

Roberts, T.J. 1977. The Mammals of Pakistan. Oxford University Press, Karachi, Pakistan. pp.

361.

Roberts, T.J. 1997. The Mammals of Pakistan. Oxford University Press, Karachi, Pakistan. pp.

525.

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(1-2): 93-

225.

Sinha, Y.P. 1980. The bats of Rajasthan: taxonomy and zoogeography. Record zool. Surv. India.

76(1-4): 7-63.

Walton, D.W. 1974. New records of bats (Chiroptera) from Pakistan. J. Mammal. Soc. Japan. 6:

43 – 50.

Wroughton, R.C. 1916. [i] Report No. 24: Sind [749-758]; [ii] Report No. 25: China Hills [758-

773]; [iii] Report No. 26: Darjiling District [773-781]. Bombay Natural History Society’s

Mammal Survey of India, Burma and Ceylon. Journal Bombay nat. Hist. Soc. 24(1): 749-781.

………………………………………………………………………………………………………Chapter 3

Table 1. Netting stations in three districts of wheat-rice based agro-ecosystem of Punjab. Sr. # Sampling sites District Longitude Latitude Date of capture 1. Civil hospital Gujranwala 74°11.583 E 32°10.203 9 N 08/02/2011 2. Qadirabad colony Gujranwala 73°41.563 E 32°17.490 N 07/03/2011 3. Kelaske village Gujranwala 73 º58.668 E 32 º10.803 N 08/06/2011 4. Gakhar mandi town Gujranwala 74°08.791 E 32°18.340 N 11/09/2011 5. Rasul nagar village Gujranwala 73º46.720 E 32º19.68 N 01/04/2012 6. Ali pur chattha town Gujranwala 74º09.361 E 32º11.272 N 018/05/2012 7. Verpal chattha village Gujranwala 73º58.803 E 32º 10.803 N 011/06/2012 8. District katchery Hafizabad 73°34.918 E 31 º58.018 N 013/05/2011 9. Kot sarwar village Hafizabad 73 º30.189 E 31 º55.148 N 02/06/2011 10. Nothain village Hafizabad 73 º32.770 E 31 º56.241 N 04/07/2011 11. Kaleki mandi village Hafizabad 73°42.697 E 32°04.150 N 03/08/2011 12. Sukheki mandi village Hafizabad 73º34.108 E 31º61.116 N 02/06/2012 13. Pindi bhattian town Hafizabad 73 º16.895 E 31 º55.148 N 08/07/2012 14. Jalal pur bhatian village Hafizabad 73º22.51 E 32º02.39 N 03/09/2012 15. Farid town Mandi Bhaudin 73º30.46 E 32º35.123 N 08/05/2011 16. Phalia town Mandi Bhaudin 73º58.13 E 32º43.601 N 05/06/2011 17. Malikwal town Mandi Bhaudin 73º45.08 E 32º35.102 N 08/02/2012 18. Head rasul rest house Mandi Bhaudin 73º31.148 E 32º40.096 N 05/06/2012 19. Mano chak Mandi Bhaudin 73º45.29 E 32º25.308 N 022/07/2012

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Table 2. Mean body mass (g) and external body measurements (mm) of six species of genus Pipistrellus captured from wheat rice based agroecosystems of Punjab, Pakistan (1 = Present study; 2 = Bates and Harrison 1997). P. pipistrellus P. paterculus P. javanicus P. tenuis P. ceylonicus P. dormeri External measurements 1 2 1 2 1 2 1 2 1 2 1 2 (n = 43) (n = 12) (n = 39) (n = 18) (n = 40) (n = 20) Body mass 3.3(2.5-4.3) - 3.5(2.9-4.7) - 7.6(4.5-10.7) - 3.6(1.8-5.4) - 3.7(2.9-4.3) - 5(3.7-6.8) - 41.4(38.8- Head and body length 38.2(34.9-43.2) 40-48 42-48 48.2(39.5-52) 40-55 36.8(30-40) 33-45 53.5(48-61.2) 45-64 46.7(41.3-52.3) 39-55 44.2) Ear length 9.0(6.8-12.7) 10.5-12 9.8(8.7-11) 10-13 9.8(7-12.2) 5-15 9.1(7-11) 5-11 10.2(8.3-11.3) 9.5-14 10.19(8.7-12.4) 10-18 Tragus length 4.1(3.2-5.1) - 4.2(3.4-4.8) - 5.1(4-7.5) - 4.4(3.4-6) - 4.9(4.1-6.1) - 5.5(4.7-6.2) - Thumb length 4.3(3.1-5.6) - 4.04(3.1-5.2) - 5.9(4.6-7) - 4.7(4-6) - 3.4(2.5- 4.7) - 5.3(4.3-7.2) - Claw length 1.6(1.2-2.1) - 1.63(1.1-2.5) - 2.0(12.5) - 1.4(0.7-2) - 1.98(1-3) - 1.5(4.3-7.2) - Forearm length 28.9(26.5-3.14) 30.-31.6 30.5(29-32.3) 29.2-34 34.2(30.5-37.5 30-36 29.2(27-31) 25-30 35.3(31.3-38) 33-42 34.5(31.5-36.8) 32.7-36.3 30.03(28- 3rd Metacarpal length 27.9(24.3-31.9) 29.5-31 27.6-32.4 33.7(29-36.5) 25.9-34.8 28.4(26-30) 23.9-29.7 34.0(30.2-36.8) 33-39.5 33.6(31-36) 31.7-36.5 31.8) 3rd Metacarpal: 1st phalanx 10(9.2-11.2) - 11.3(9.5-12) - 11.6(9-13) - 11.3(10-12) - 11.6(9.8-13.2) - 10.4(8.3-12.5) - 3rd Metacarpal: 2nd phalanx 8.3(7.2-9.6) - 8.8(7.3-10.5) - 9.6(8-11) - 9.02(7-10.4) - 9.6(8.5-11) - 9.0(7.2-11) - 4th Metacarpal length 27.0(24.3-31.5) 28.7-30.8 29.6(28-31) 27.4-32.4 32.9(28-35) 29.9-34.7 27.8(25.5-30) 23.7-29.2 33.1(28.5-36) 32.6-38.5 33.3(31-35.2) 31.6-36.4 4th Mtacarpal: 1st phalanx 9.9(8.7-10.7) - 10.7(8.5-12) - 10.4(8.5-12) - 10.8(10-12) - 101.(8.3-12) - 9.4(8-11.3) - 4th Metacarpal: 2nd phalanx 6.4(5.3-8.1) - 7.8(6.5-10) - 9.2(7.3-11) - 8.02(6.7-10) - 8.5(7.2-10.5) - 8.5(7.2-9.8) - 5th Metacarpal length 26.5(23.5-29.3) 28.4-29.8 28.4(27.2-30) 27.1-31.2 31.5(27.5-34.7) 29-33.4 27.2(25-29) 23.5-28.5 31.9(27-35.7) 30.7-36.7 33.0(31-35) 31.2-35 5th Metacarpal:1st phalanx 10.8(5.3-76.4) - 7.7(6.5-8) - 9.8(7.1-10) - 7.9(7-10.4) - 9.8(8.9-11.6) - 8.3(7-9.5) - Wingspan 187(175-207) - 182(142-213) - 194(167-221) - 175(137-203) - 183(148-198) 227-262 234(218-225) 238-257 11.7(11.2- Tibia length 11.1(9.7-12.8) - - 12.4(10-14.5) - 12.0(11-13) - 12.6(10.7-14.5) - 11.6(10.2-13.7) - 12.3) Calcar length 4.9(4.5-5.7) - 4.8(4-6) - 4.2(3-5) - 4.5(3-6.4) - 4.7(3.3-6) - 4.6(3.7-5.6) - Hind foot length 6.2(5.2-7.4) 6.0-7.0 6.6()5.2-7.5 6-7 8.1(6-10) 3.0-8.0 6.3(6-8) 3-7 9.3(7.8-10.7) 6-11 6.9(6.2-8.1) 5-8 32.0(28.5- Tail length 27(24.6-28.8)- - 31-38 28.6(24-33) 26-40 28.0(22-33) 20-35 3.0(26.3-34.6) 30-45 30.5(27.5-34.5) 27-41 35.2) Penis length 6.3(6.1-7); n=17 - 6.8(6-8); n=5 - 8(7-9); n=5 - 6.2(4.2-8); n=6 - 8.3(8-9); n=14 - 6.3(6.1-7); =12 -

………………………………………………………………………………………………………Chapter 3

Table 3. Mean cranial measurements (mm) of six species of genus Pipistrellus captured from wheat rice based agroecosystems of Punjab, Pakistan (1 = Present study; 2 = Bates and Harrison 1997). P. Pipistrellus P. Paterculus P. Javanicus P. Tenuis P. Ceylonicus P. Dormeri Cranial measurements 1 1 1 1 1 1 2 2 2 2 2 2 (n = 43) (n = 12) (n = 39) (n = 18) (n = 40) (n = 20) Breadth of braincase 6.3(5.96-6.64) 6.3-7.1 6.0 6.0-6.4 6.4(4.3-8.5) 6.3-7.1 6.5(4.6-8.4) 3-7 7.12(5.15-9.09) 6.8-7.8 7.6(7.7-7.5) 6.8-7.5

Zygomatic breadth 8.8(7-10.6) 8.2-9 7.1 - 9.8(7.2-12.4) 8.2-9 8.3(6-10.6) 20-35 11.46(7.23-15.69) 9.2 -11 11.2(11.1-11.3) -

Postorbital construction 3.51(3.25-3.77) 3.3-4.3 3.3 3.2-3.9 3.9(3.12-4.68) 3.3-4.3 4.1(2.4-5.8) - 4.26(3.26-5.26) 3.7-4.3 4.2(4.6-3.8) 3.6-4.2

Condylo-carine length 10.3(9.9-10.67) 11.9 11.0 10.6-11.6 11.3(7.5-15.1) 11.9-13.1 8.7(6.6-10.8) 9.3-10.7 12.7(7.7-17.7) 13.1-14.3 13.5(13-14) 12.8-13.6

Condylo basal length 11.1(10.6-11.5) 11 .5 - 12.1(8.4-15.8) - 9.8(6.7-12.9) - 10.76(7.7-13.76) 14.3(14-14.7) -

Greatest length of skull 11.5(11.13-11.87) 13-14.6 11.6 11.7-12.6 13.1(9.5-16.7) 13-14.6 10.4(7.7-13.1) 10.7-12.1 13.6(8.07-19.2) 14.4-15.8 14.4(14.2-14.6) 13.7-15

Maxillary toothrow (C-M3) 3.51(3.28-3.74) 4.6-5.2 4.1 4.1-4.8 3.8(2.8-4.7) 4.6-5.2 4.2(1.5-6.9) 3.5-4.1 6.01(3.08-8.9) 5.2-5.9 5.3(5.1-5.5) 5.2-5.6

Anterior palatal width 3.61(3.1-4.1) - 3.7 - 3.9(2.8-5) - 3.6(1.9-5.3) - 4.79(2.7-6.7) 4.8(4.7-5) -

Posterior palatal width 5.3(4.99-5.61) - 5 .0 - 3.8(2.9-4.7) - 4.8(2.5-7.1) - 6.6(4.29-9.09) 6.2-7.2 6.9(6.8-7) 6.3-7

Mandibular toothrow (C-M3) 3.58(3.1-3.9) 4.8-5.5 4.5 4.4-5.0 3.9(3.1-4.6) 4.8-5.5 4.7(3.5-5.9) 3.8-4.4 5.3(2.7-7.9) 5.7-6.5 6.1(6-6.3) 5.5-6.1

Mandible length 7.8(7.03-8.5) 9.3-10.7 8 .0 8.4-9.1 9.2(9-9.4) 9.3-10.7 8.1(7.3-8.8) 7.2-8.3 5.3(4.88-15.4) 10.6-12 10.2 (10-10.5) 10.4-11.2

………………………………………………………………………………………………………Chapter 3

Figure 1. Bacula of P. pipistrellus (a), P. dormeri (b), P. tenuis (c), P. ceylonicus (d), P. javanicus (e), P. paterculus (f)

………………………………………………………………………………………………………Chapter 3

Recent Record of Desert Yellow House Bat, Scotoecus pallidus (Order: Chiroptera) from

Punjab, Pakistan

Muhammad Shahbaz, Arshad Javid, Syed Makhdoom Hussain1, Muhammad Ashraf2 and

Hamda Azmat2

Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore

1Department of Zoology, Wildlife and Fisheries, Government College University, Faisalabad

2Department of Fisheries and Aquaculture, University of Veterinary and Animal Sciences,

Lahore

Corresponding Author’s email: [email protected]

(This paper has been submitted for publication in the Journal of Animal and Plant

Sciences)

………………………………………………………………………………………………………Chapter 3

Abstract

The desert yellow house bat, Scotoecus pallidus is an endemic species of Indian sub-continent with type locality, Mian Mir, Lahore, however, very little is known about the species in the

Indian region. During present study, specimens of S. pallidus (n = 36) were captured after 136 years from Punjab province and 51 years from Pakistan. The external body, cranial and bacular measurements of specimens captured from Gujranwala, Mandi Bhauddin and Hafizabad districts were compared with available literature. The average head and body length of all the captured specimens of S. pallidus (n = 36) was 55.9 mm, average forearm length was 37.0 mm, greatest

skull length (n = 5) was 14.8 mm while average baculum length (n = 3) was 5.0 mm. The cranial

and bacular features of the species are reported for the first time in country.

Key words: Cranial measurements; baculum size; agro-ecosystem, Gujranwala

Introduction

The chiropteran diversity of Pakistan is comparable to any other region with similar

physiographic features. The bats constitute 28% of mammalian fauna of the country but are

amongst the least studied taxa (Roberts, 1997; Mahmood-ul-Hassan et al., 2009). There is

extreme shortage of knowledge regarding occurrence and distribution of bat species within

territorial limits of Pakistan (Roberts, 1997; Bates and Harrison, 1997). Information for many of

the bat species is based on its original description as the species has not been collected

subsequently (Mahmood-ul-Hassan et al., 2009). Up till now 54 chiropteran species have been

documented from Pakistan but the number is expected much more if the cryptic bat species are

accurately identified (Walker and Moller, 2004; Mahmood-ul-Hassan et al., 2009). Bats are the

only mammals capable of true flight and can cross the barriers other mammals cannot (Wilson

and Reeder, 1993; Hutson et al., 2001). Feeding habits of bats range from primary consumers

………………………………………………………………………………………………………Chapter 3

(seed, pollen, leaf or fruit eaters) to top order predators (insects, fish and small mammal eaters)

(Beolens et al., 2009).

In Pakistan, the research on bats started quite recently and very few biologists are trying to explore bat fauna of the country (Mahmood-ul-Hassan et al., 2009). However, there is serious lack of taxonomic knowledge to identify the bats on the basis of their morphological characters.

Although, molecular techniques are available and being used in many parts of the world (Russo et al., 2006) but these techniques are costly and the results are not immediately available (Waller et al., 2007). Therefore, many scientists, especially in developing states use identification keys to correctly identify the species (Jacobs et al., 2006). The ecological services provided by the bats are acknowledged almost all over the world but the scenario is totally different in Pakistan where bats are considered loathsome and fearsome creatures.

Scotoecus is largely an African genus with distribution range from Senegal to Ethiopia south to Angola and Mozambique (Hill, 1974). Single Asian species Scotoecus pallidus is endemic to Indian subcontinent (Sinha, 1986a) and has been reported from India and Pakistan

(Koopman, 1993; Roberts, 1997). The species has not been recorded from any part of

Afghanistan and Iran and it may have distribution in northern India through Uttar Pradesh and

Bihar (Corbet and Hill, 1992). In Pakistan, S. pallidus was first collected by Dobson from Mian

Mir near Lahore in 1876. The species has wide spread distribution in Indus plains of Pakistan and has been reported from Kashmore, Mirpur, Naundero (Wroughton, 1916), Sukker and Dadu in Sindh province (Siddiqi, 1961), Muzaffargarh and Sialkot in Punjab province. S. pallidus seems to be an uncommon bat and no specimen has been collected from Lahore District after

1876 (Roberts, 1997).

………………………………………………………………………………………………………Chapter 3

Scotoecus pallidus Dobson, 1876 is a relatively small vespertilionid bat with an average forearm length 36.2 mm (Bates and Harrison, 1997). The species prefers to live in tropical thorn forests (Siddiqi, 1961). However, nothing is known about species’ habitat and population status in the Indian subcontinent (Molur et al., 2002). The survival of S. pallidus is at risk and the major threats include urbanization, loss of habitat and competition from invasive alien species

(Molur et al., 2002). This grieved situation demands long term monitoring and research on these environment friendly creatures (Meyer et al., 2010). The present work was therefore planned to explore three main rice producing districts of Punjab, Pakistan to ascertain the presence or absence of S. pallidus.

Materials and Methods

This two years study extending from January 2011 through December 2012 was carried out in three districts namely Gujranwala, Hafizabad and Mandi Bhaudin of the central Punjab. These districts comprise core rice producing belt of the country, are densely populated and the entire natural ecosystem has been changed in to agroecosystems and human habilitations. These districts experience cold winters and warm summers. Temperature fluctuates between minimum up to freezing point during winters to 50 ºC during summer season. Annual rainfall is 650 mm but rains are more frequent in monsoon (Qadir et al., 2008; Ullah et al., 2009).

Each district was surveyed on monthly basis and mist nets and hand nets were used to collect the bat specimens. Old buildings, abandoned wells, ruins, houses, tree groves and plantations were explored in search of bat roosts. People of the study area were also interviewed to get information about exact locality of bats.

Once the specimens were captured, they were euthanized, placed in cotton bat bags and each specimen was weighed up to 0.1 g (Pesola balance 10050, Swiss made). The captured

………………………………………………………………………………………………………Chapter 3

specimens were brought to the laboratory for further analysis. The external body 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) and Javid (2011).

Results and Discussion

Character matrices and identification keys are authentic tools for accurate identification of

different bat species (Daniel, 2009; Srinivasulu et al., 2010). Taxonomic status of many of the

bat species is unclear in Pakistan and there is dire need to identify bats on the basis of physical

features. Roberts (1997) and Bates and Harrison (1997) only source of literature on bats of the

region. During present study, a total of 36 Scotoecus pallidus were captured and external body,

cranial and bacular features of these specimens were compared with Roberts (1997) and Bates

and Harrison (1997).

The average head and body length of all 36 specimens captured during present study was

55.9 mm (47-59 mm) while the forearm was 37 mm (34-39.5 mm). The lengths of 3rd, 4th and 5th metacarpals were 35.2 mm (34-39 mm), mm 34.7 (31-38.5 mm) and 34.3 mm (33.2-35.4 mm), respectively. The average wingspan of the captured specimens was 25 mm (21.6-32.8 mm) and tail was 33.2 mm (27.2-38 mm) long. The average greatest skull length of S. pallidus (n = 5) was

14.8 mm (14.3-15.2 mm). Average total length of baculum (n = 3) was 4.9 mm (4.7-5.2 mm)

(Table 1).

The average head and body length, tail length, length of 3rd, 4th and 5th metacarpals of all

36 S. pallidus specimens captured during present study fall within the ranges given by Bates and

Harrison (1997). Similarly, average breadth of braincase, mandibular toothrow length and

………………………………………………………………………………………………………Chapter 3

mandible length of five S. pallidus captured during present study were within the ranges

mentioned by Bates and Harrison (1997).

References

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Museum, Sevenoaks, UK. pp 187-188.

Bates, P. J. J., D. Vu Thong and S. Bumrungrsi (2005). Voucher specimen preparation: bats.

Harrison Institute, Bowerwood House, St Botolph’s Road, Sevenoaks, Kent, England.

Beolens, M. Watkins and M. Grayson (2009). "Vives". The Eponym Dictionary of Mammals.

Johns Hopkins University Press. pp. 432–433.

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Table 1. Comparison of external body, cranial and bacular measurements of Scotoecus pallidus captured during present study with Roberts (1997) and Bates and Harrison (1997).

External body measurements Present study Roberts Bates and Harrison Cranial measurement Present study Bates and Harrison (1997) (n = 36) (1997) (1997) (n = 5) Body mass 11.5 (9-14.3) - - Breadth of braincase 7.2(6.4-8.0) 7.7(7.5-8.2) Head and body length 55.9 (47-59) 54(50-59) 58(50-58) Zygomatic breadth 10.14(9.8-10.4) 10.5(10.5-10.5) Ear length 11.2(9-13.5) - 12.8(12-15) Postorbital construction 4.28 (3.9-4.8) 4.7(4.2-4.5) Tragus length 4.2(3.4-4.8) - - Condylo-canine length 14.3(13.7-15.2) 14.1 (13.8-14.8) Thumb length 6.3(5.2-7.5) - - Greatest length of skull 14.8(14.3-15.2) 15.1 (14.5-16.1) Claw length 2.2(2-4.5) - - Maxillary tooth row 4.9(4.2-5.5) 5.6 (5.5-5.9) Forearm length 37(34-39.5) 36.2(34.1-37.3)36.2(34.1-37.3) Anterior palatal breadth 4.5(4.2-4.7) 3rd metacarpal length 35.2(34-39) - 34.6(33.5-36) Posterior palatal breadth 6(5.3-6.4) 6.9(6.6-7.2) 3rd metacarpal: 1st phalanx 12(7-13) - - Mandibular tooth row 5.4(4.8-5.7) 6.1(5.9- 6.4) 3rd metacarpal: 2nd phalanx 10.(6.1-11) - - Mandible length 10.8 (10.3-11.2) 11.4(10.9-12) 4th metacarpal length 34.7(31-38.5) - 34.2(32.8-35.4) Penis length - 9.7(6-12.7) 4th metacarpal: 1st phalanx 11.3(10.2-12.5) - - Bacular Measurements (n = 3) - 4th metacarpal: 2nd phalanx 8.98(7-10.7) - - Total length of baculum 4.9 (4.7-5.2) - 5th metacarpal length 34.3(33.2-35.4) - 33.7(32.6-34.9) Length of shaft 4.1(3.6-4.7) - 5th metacarpal: 1st phalanx 9.3(5.8-11.5) - - Length of proximal Branch 0.5(0.46-0.7) - Wing span 25(21.6-32.8) - - Length of distal branch 0.36(0.34-0.4) - Tibia length 13.3(8.5-15) - - Width of Proximal branch 1.2(0.8-1.7) - Calcar length 5.7 (3.5-8) - - Width of distal branch 0.5(0.47-0.53) - Hind foot length 9.5(7.5-11) 8.0 8.3(6-10) Height of Baculum 0.5(0.4-0.6) - Tail length 33.2(27.2-38) 37(31-34) 36.9(34-41) - - -

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CHAPTER 4

SUMMARY

Bats in Pakistan are considered fearsome and loathsome that’s why remained unexplored in the country. Present study on bats of wheat-rice based agro-ecosystem of Punjab province was carried out at three rice producing districts in central Punjab namely Gujranwala, Hafizabad,

Mandi Bhaudinn and at some part of Lahore city. Study area constitutes one of the most populated part of the country. Bats belonging to three families, five genera and eleven species were captured during a two-year survey extending from January 2011 through December 2012.

The external body, cranial and bacular features of all the eleven species were compared with the available literature.

Present study on Fulvous fruit bat (Rousettus leschenaulti) from October 2011 to March

2012 in the vicinity of Lahore, Pakistan took morphometric measurements of 15 (9♂ and 6♀) bat specimens. The average head and body length of all 15 specimens was 99.55 ± 15.035mm, forearm was 77.64 ± 6.373mm long, lengths of 3rd, 4th and 5th metacarpals were 52.73 ± 4.832 mm, 51.56 ± 4.996mm and 49.86 ± 3.998, respectively and the tail length was 11.1 ± 3.072mm.

The greatest skull length (n= 9) was 35.89 ± 2.848mm, breadth of braincase was 15.44 ±

1.509mm while bacular length of a male specimen was 3.075mm.

99 ………………………………………………………………………………………………………Summary were captured with the help of a hand net. The average head and body length of all the captured specimens was 42.36±1.1 mm, forearm length was 40.34±0.75 mm, greatest skull length (n= 2) was 17.5± 0.49 mm while baculum (n= 2) was 4.35 ± 0.38 mm long. The present record is first from the study area and the Punjab province.

Specimens of Rhinolophus blasii were captured in Manawa, district Lahore 43 years after the first and single ascertained record in Pakistan. External, cranial and bacular measurements of

R. blasii are given for the first time in the country.

Present study was focused to explore core rice producing belt of central Punjab to ascertain the presence or absence of Asiatic Greater Yellow House bat Scotophilus heathii. Three districts namely Gujranwala, Hafizabad and Mandi Bhaudin were surveyed from January 2011 through December 2012 and a total of 33 S. heathii were captured. The external body, cranial and bacular measurements of the captured specimens were compared with available literature.

The average head and body length of all 33 captured specimens was 73.7±4.4 mm, forearm length was 60.6±4.1 mm, greatest skull length (n = 6) was 18.7±1.7 mm while baculum (n = 1) was 3.075 mm long. The cranial and bacular features of the species which are important traits for mammalian identification are reported for the first time in country and this is also the first record of the species from study area.

Three rice producing districts viz. Gujranwala, Hafizabad and Mandi Bhauddin in

Pakistan were surveyed to explore bat fauna of genus Pipistrellus in central Punjab from January

2011 to December 2012. A total of 172 specimens of genus Pipistrellus belonging to six species i.e. P. pipistrellus (n = 43), P. paterculus (n = 12), P. javanicus (n = 39), P. tenuis (n = 18), P. cylonicus (n = 40) and P. dormeri (n = 20) were captured. All these species are reported for the first time from study area while P. pipistrellus and P. paterculus from Punjab province. The

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………………………………………………………………………………………………………Summary shape and length of baculum were the characters that help in clear cut identification of various

Pipistrellus species. The external body, cranial and bacular features of the species were compared with available literature.

The desert yellow house bat, Scotoecus pallidus is an endemic species of Indian subcontinent with type locality, Mian Mir, Lahore, however, very little is known about the species in the Indian region. During present study, specimens of S. pallidus (n = 36) were captured after

136 years from Punjab province and 51 years from Pakistan. The external body, cranial and bacular measurements of specimens captured from Gujranwala, Mandi Bhauddin and Hafizabad districts were compared with available literature. The average head and body length of all the captured specimens of S. pallidus (n = 36) was 55.9 mm, average forearm length was 37.0 mm, greatest skull length (n = 5) was 14.8 mm while average baculum length (n = 3) was 5.0 mm.

The cranial and bacular features of the species are reported for the first time in country.

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