Distribution and Current Population Status of Freshwater Turtles of Khyber Pakhtunkhwa

Home , Bara River, Hadero Lake, Kabul River, Korang River, Pristurus rupestris, Sinjoro

DISTRIBUTION AND CURRENT POPULATION STATUS OF FRESHWATER TURTLES OF KHYBER PAKHTUNKHWA

AMTYAZ M. Sc., M. Phil.

Thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Zoology (Wildlife and Fisheries).

DEPARTMENT OF ZOOLOGY UNIVERSITY OF KARACHI, KARACHI-75270 2016

BOARD OF ADVANCED STUDIES & RESEARCH UNIVERSITY OF KARACHI

CERTIFICATE

I have gone through the thesis and titled "DISTRIBUTION AND CURRENT POPULATION STATUS OF FRESHWATER TURTLES OF KHYBER PAKHTUNKHWA " submitted by Mr. AMTYAZ S/O AURANG ZEB for the award of Ph. D degree and certify that to the best of my knowledge it contains no plagiarized material.

Date: 15th March 2016

BOARD OF ADVANCED STUDIES & RESEARCH

University of Karachi

DECLARATION

I, AMTYAZ S/O AURANG ZEB hereby declare that on part of the work presented by me has been plagiarized from anywhere. Proper references are cited, wherever necessary. I understand that the university reserves the right to cancel the degree if any of the above declaration is proved false before or after the award of degree.

Signature of the candidate:

Name of the candidate: Amtyaz

Title : "Distribution and Current Population

Status of Freshwater Turtles of Khyber

Pakhtunkhwa".

Degree : Ph. D

Department/ Subject : Zoology

Date : 15-03-2016

DEDICATION

Dedicated to my beloved mother

TABLE OF CONTENTS

Sr. No Particulars Page No I Abstract i - iii II Abstract in Urdu iv - v III Acknowledgements vi - viii CHAPTER 1 1 Introduction 1 - 43 1.1 Order Chelonia/Testudines of Pakistan 5 1.2 Khyber Pakhtunkhwa 10 1.3 Charsadda 16 1.4 Peshawar 24 1.5 Nowshera 30 1.6 Mardan 34 1.7 Dera Ismail Khan 37 CHAPTER 2 2 Review of Literature 44-70 CHAPTER 3 3 Materials and Methods 71-78 3.1 Direct Counting Methods 72 3.2 Indirect Counting Methods 74 CHAPTER 4 4 Results 79-143 4.1 Charsadda District 80 4.2 Peshawar District 80 4.3 Nowshera District 81 4.4 Mardan District 82 4.5 Dera Ismail Khan District 82 4.6 Drains and Canals of Study areas 83 4.7 Rivers of Study areas 83 4.8 Peshawar Valley 84 4.9 Lissemys punctata andersonii 107 4.10 Nilssonia gangeticus 112 4.11 Nilssonia hurum 117 4.12 Chitra indica 121 4.13 Pangshura tectum 125 4.14 Pangshura smithii 129 4.15 Hardella thurjii 134 4.16 Geoclemys hamiltonii 139 CHAPTER 5 5.1 Discussion 144-175 5.2 Conclusion 176-177 5.3 References 178-195

LIST OF TABLES

Table No. Particulars Page No. CHAPTER 1 1.1 IUCN and CITES Status of freshwater turtles of Pakistan 8 1.2 Habitat, Feeding habits, Reproduction and Behavior of 9 Freshwater turtles of Pakistan 1.3 National parks of Khyber Pakhtunkhwa 13 1.4 Districts of Khyber Pakhtunkhwa Province of Pakistan 14

1.5 The use of turtles in some Traditional Chinese Medicine 42 preparations CHAPTER 4 4.1 Status of Population and Distribution of Freshwater Turtles of 85 Khyber Pakhtunkhwa 4.2 Status of Population and Distribution of Freshwater Turtles in 87 Charsadda District 4.3 Status of Population and Distribution of Freshwater Turtles in 89 Peshawar District 4.4 Status of Population and Distribution of Freshwater Turtles in 91 Nowshera District 4.5 Status of Population and Distribution of Freshwater Turtles in 93 Mardan District 4.6 Status of Population and Distribution of Freshwater Turtles in 95 Dera Ismail Khan District 4.7 Status of Population and Distribution of Freshwater Turtles in 97 Drains and Canals of Khyber Pakhtunkhwa 4.8 Status of Population and Distribution of Freshwater Turtles in 99 Rivers of Khyber Pakhtunkhwa 4.9 Status of Population of Freshwater Turtles of Peshawar Valley 101 4.10 Status of Population and Distribution of Freshwater Turtles in 103 selected districts of Khyber Pakhtunkhwa

LIST OF FIGURES

Figure No. Particulars Page No. CHAPTER 1 1.1 Maps of Pakistan and Khyber Pakhtunkhwa showing study 15 districts 1.2 Maps of Khyber Pakhtunkhwa and Charsadda District 17 1.3 Jindi River in Charsadda 18 1.4 Swat River in Charsadda 19 1.5 Kabul River in Charsadda 20 1.6 Hisara Drain in Charsadda 21 1.7 Kashmalo Drain in Charsadda 22 1.8 Dub Drain in Charsadda 23 1.9 Maps of Khyber Pakhtunkhwa and Peshawar District 25 1.10 Naguman (A distributary of Kabul River) in Peshawar 26 1.11 Shahalam (A distributary of Kabul River) in Peshawar 27 1.12 Budhni River in Peshawar 28 1.13 Bara River in Peshawar 29 1.14 Maps of Khyber Pakhtunkhwa and Nowshera District 31 1.15 Kabul River in Nowshera 32 1.16 The junction of Kabul River and Indus River in Nowshera 33 1.17 Maps of Khyber Pakhtunkhwa and Mardan District 35 1.18 Jalala Drain in Mardan. 36 1.19 Maps of Khyber Pakhtunkhwa and Dera Ismail Khan 38 1.20 Indus River in Dera Ismail Khan 39 CHAPTER 3 3.1 Map of Khyber Pakhtunkhwa showing study sites 76 3.2 Map of study sites in Peshawar Valley 77 3.3 Map of study sites in Dera Ismail Khan 78 CHAPTER 4 4.1 Status of Population and Distribution of Freshwater Turtles of 86 KPK 4.2 Status of Population and Distribution of Freshwater Turtles in 88 Charsadda District 4.3 Status of Population and Distribution of Freshwater Turtles in 90 Peshawar District 4.4 Status of Population and Distribution of Freshwater Turtles in 92 Nowshera District 4.5 Status of Population and Distribution of Freshwater Turtles in 94 Mardan District 4.6 Status of Population and Distribution of Freshwater Turtles in 96 D. I. Khan District 4.7 Population status of Freshwater turtle Species in Peshawar 98 Valley 4.8 Status of Population of Freshwater Turtles in Selected 100 Districts of KPK 4.9 Status of Total Population Density of Freshwater Turtles in 102 Selected Districts of KPK 4.10 Status of Population Density of different Species of 104 Freshwater Turtles in Selected Districts of KPK 4.11 Comparison of Turtle Population in Drains/Canals with Rivers 105 of KPK 4.12 Comparison of Turtle Population of Freshwater Turtles of 106 Peshawar Valley with Southern District (D. I. Khan) 4.13 Distribution of Lissemys punctata andersonii 110 4.14 Lissemys punctata andersonii (Indian flap-shell turtle) 111 4.15 Distribution of Nilssonia gangeticus 115 4.16 Nilssonia gangeticus (Ganges soft-shell turtle) 116 4.17 Distribution of Nilssonia hurum 119 4.18 Nilssonia hurum (Indian Peacock soft-Shell turtle) 120 4.19 Distribution of Chitra indica 123 4.20 Chitra indica (Indian Narrow headed soft-shell turtle) 124 4.21 Distribution of Pangshura tectum 127 4.22 Pangshura tectum (Indian Roofed turtle) 128 4.23 Distribution of Pangshura smithii 132 4.24 Pangshura smithii (Brown Roofed turtle) 133 4.25 Distribution of Hardella thurjii 137 4.26 Hardella thurjii (Crowned River turtle) 138 4.27 Distribution of Geoclemys hamiltonii 142 4.28 Geoclemys hamiltonii (Spotted pond turtle) 143 CHAPTER 5 5.1 Notification for addition of freshwater turtles in Wildlife Act, 163 1975 5.2 Some of the equipment’s for turtle poaching 164 5.3 Capturing techniques for Turtles 165 5.4 Captured turtles 166 5.5 Dead specimen of Freshwater turtles 167 5.6 Trading activity of body parts of turtles 168 5.7 Trading activity of turtles 169 5.8 Another trading activity 170 5.9 Canal closure during winter season 171 5.10 Eggs in a nest of Freshwater turtle 172 5.11 Turtle’s capturing 173 5.12 Making a net 174 5.13 Awareness is giving to local community about turtles 175

ABSTRACT

Freshwater turtles have served as an important food resource in many Asian countries. However, several countries of our region have made few attempts for conservation and management of this resource. The present study of distribution and current population status of freshwater turtles was conducted in Charsadda, Peshawar, Nowshera, Mardan and Dera Ismail Khan (D. I. Khan) Districts of Khyber Pakhtunkhwa (KPK) Province during the years 2013-2015. Eight species of freshwater turtles viz. Lissemys punctata andersonii (Webb, 1980a), Nilssonia gangeticus (Cuvier, 1825), Nilssonia hurum (Gray, 1831), Chitra indica (Gray, 1831), Pangshura tectum (Gray, 1863), Pangshura smithii (Gray, 1863), Hardella thurjii (Gray, 1831) and Geoclemys hamiltonii (Gray, 1831) were recorded.

In the present study, seven species of freshwater turtles were recorded from Charsadda district, Lissemys punctata and Nilssonia gangeticus were common. Chitra indica, Nilssonia hurum and Pangshura smithii were less common; Pangshura tectum and Hardella thurjii were rare. Geoclemys hamiltonii was not recorded from district Charsadda. According to the present data, (2013-2015) N. gangeticus was recorded as 29.76 %, L. punctata as 29.25%, N. hurum as 11.31%, C. indica as 10.01%, P. smithii as 9.87%, P. tectum 6.70% and H. thurjii as 3.10%.

In the district of Peshawar, seven species were recorded, Lissemys punctata and Nilssonia gangeticus were common, Nilssonia hurum,

Pangshura smithii and Chitra indica were less common, while Pangshura tectum and Hardella thurjii were recorded as rare. Geoclemys hamiltonii was not recorded from this district. According to the present data (2013-2015), L. punctata was recorded as 35.03%, N. gangeticus as 24.07%, N. hurum as 14.87%, P. smithii as 12.52%, C. indica as 09.00%, P. tectum 2.35% and H. thurjii as 2.15%.

Seven species were recorded in the Nowshera District. Nilssonia gangeticus and Nilssonia hurum were common; While Lissemys punctata, Pangshura tectum and Pangshura smithii were recorded as less common. Hardella thurjii and Chitra indica were rare. Geoclemys hamiltonii was not recorded in Nowshera district. According to the present data (2013-2015), N. hurum was recorded as 25.39%, N. gangeticus as 22.70%, L. punctata as 17.02%, P. tectum as 13.62%, P. smithii as 12.48%, H. thurjii as 6.10% and C. indica as 02.70%.

Only four species were recorded from Mardan Distrct. Lissemys punctata and Nilssonia gangeticus were common, Pangshura smithii was less common, while Pangshura tectum was recorded as rare. Geoclemys hamiltonii, Chitra indica, Nilssonia hurum and Hardella thurjii were not recorded from Mardan District during present study (2013-2015). L. punctata was found abundant among the recorded species and that was 48.66% followed by N. gangeticus (36.90%). P. smithii and P. tectum were recorded as 10.16% and 4.28%, respectively.

In the district of Dera Ismail Khan (D. I. Khan), all the eight species of freshwater turtles were recorded, Nilssonia gangeticus was common. The status of Nilssonia hurum, Chitra indica and Lissemys punctata were recorded as less common, while Pangshura smithii, Geoclemys hamiltonii and Hardella thurjii were in intermediate levels. Pangshura tectum was recorded as rare. According to the present data (2013-2015), all the eight species of freshwater turtles of Pakistan were present in Dera Ismail Khan, district of Khyber Pakhtunkhwa. And Geoclemys hamiltonii was only recorded from this district of Khyber Pakhtunkhwa province. Nilssonia gangeticus was found as 35.31%, Nilssonia hurum, 15.34%; Chitra indica, 14.18%; and Lissemys punctata as 12.01%. While Pangshura smithii, Geoclemys hamiltonii, Hardella thurjii and Pangshura tectum were recorded as 8.25%, 7.38%, 5.64% and 1.88%, respectively.

iii

ABSTRACT (IN URDU) iv

ACKNOWLEDGEMENTS

First of all, I bow down my head to the Omnipotent, Omnipresent and Omniscient Allah. As a result of His clemency my success was finally consummated.

It is a matter of great pleasure for me to express my gratitude and cordially thanks to my Research Supervisor, Dr. Muhammad Zaheer Khan, Professor, Department of Zoology, University of Karachi for his intellectual qualities and sincere guidance helped me a lot in the smooth progress of the present research work.

I would like to express my gratitude to Prof. Dr. Rehana Yasmeen Farooque, Chairperson, Department of Zoology, University of Karachi, for providing the research facilities in the department.

The author thanks to Dr. Michael R. J. Forstner, Regent’s Professor, Alexander Stone Chair in Genetics, Biology Department, Texas State University, San Marcos, Texas for his valuable guidance, advice and full support during my visit to Texas State University of USA.

I would like to express my gratitude to Prof. Dr. Dittmar Hahn, Chair Department of Biology of Texas State University, USA for providing Laboratory facility and accommodation during my stay in Texas State University.

The author wish to thanks the entire team of Laboratory of Herpeto- Genetics of Texas State University, USA for cooperation.

The author wish to thanks HEC (Higher Education Commission of Pakistan) for providing grant from IRSIP (International Research Support Initiative Program).

I would like to thanks Dr. Peter Praschag of “Conservation breeding and research center for turtles” Austria for his technical cooperation and guidance.

I would like to express my sincere appreciation to Dr. Syed Ali Ghalib Consulting Wildlife Ecologist, for his encouragement and valuable suggestions during the research work.

Thanks to Prof. Wisal Khan of Charsadda Post Graduate Government College, Prof. Sultan-U-Din Yousufzai of Govternment Degree college, Gul Abad, Lower Dir, Muazzam Ali Khan of Charsadda, Dr. Javed Khan of Charsadda, Tehsinullah, Ali Raza and Ejaz Khan of Charsadda, Dr. Islam Shah of Nowshera, Kiramat Shah of Mardan, Salman Khan of Gomal University Dera Ismail Khan, Usman Khan of Islamabad and Musavir Shah of Peshawar for cooperation during field works of different districts of Khyber Pakhtunkhwa.

I wish to offer my heartily and grateful thanks to my friend Usman Ali Hashmi of Department of Zoology, University of Karachi and Head of Department of Zoology of Dehli Science College Karachi, for his cooperation during the preparation of this thesis.

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I wish to offer my heartily thanks to my colleagues in Department of Zoology, Sir Syed Government Girls College, Nazimabad, Karachi for their cooperation during preparation of this thesis.

I would like to thanks the whole team of Wildlife and Fisheries Section, Department of Zoology, University of Karachi for their encouragement and cooperation during preparation of this thesis.

I express my indebtedness to my mother, Brothers, Sisters, Wife and my Sons (Ahmed Zeb Safi and Anwar Zeb Safi) for immense understanding and meticulous care.

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Chapter 1

INTRODUCTION

Freshwater ecosystems are rich in biodiversity, but unfortunately facing severe threats. Freshwater animals are more at risk among all organisms. Riverine ecosystems are important for mankind in socioeconomic, ecological and bio-esthetic levels. Understanding the mechanisms driving losses in aquatic ecosystem is important to the protection and back to restoration of natural ecosystems worldwide (Strayer and Dudgeon, 2010).

There are thirteen recognized families and about three hundred species, in which two hundreds of living species of terrapins and tortoises are listed as globally threatened. The highest numbers of threatened species are native to Asia, in which approximately 75% are Critically Endangered (CR) and Vulnerable (VU). Approximately 90% of living species of terrapins are included in the IUCN Red List 40% of Global and 75% of Asian species of terrapins and tortoises are now considered threatened with extinction. The major threat is the poaching of adult turtles. Turtle’s meat, carapace and plastron are mostly demand in Asian markets, and has increased turtle poaching in every region of the World. Asian turtle’s species are in critical condition. Every year a large number of terrapins exported from different countries to markets in Asia. A large number of Asian turtles are exported as pet to western markets as well. Mostly these exported specimens for trade are taken from South Asian and East Asian countries. Control of trade in these species is overdue. Many of

1 the Asian terrapins still remain unlisted in CITES Appendices (IUCN, 2015).

Turtles are reptiles characterized by shell developed from ribs that acts as a shield. These are the oldest reptilian group, first evolved in Triassic period. They don’t lay eggs underwater and breathe air through lungs like other amniotes. Turtles are ectotherms (Poikilothermic), however, leather back sea turtles (Dermochelys coriacea) are endotherms because of their high metabolic rate (Wikipedia, 2016).

Testudines are more endangered group of Chordates, surpassing Aves, Mammals, Pisces and Amphibians. According to the “IUCN Red list threatened species” 135 of terrapins species are threatened [(Critically Endangered (CR), Endangered (EN), or Vulnerable (VU)]. 175 (52.2%) are Threatened or Extinct, 167 (49.9%) are Threatened (CR, EN, or VU) and 107 (31.9%) are CR or EN out of 335 total species of turtles and tortoises (Van Dijk et al., 2014; Khan et al., 2015; 2016).

Many species of terrapins face imminent extinction threats without bold and effective conservatory action globally. Generally, turtle shell is an important morphological innovation in vertebrate history. All Species of terrapins alone occupy the inland waters throughout the world, from the tropical areas to just outside the Arctic Circle (Gaffney, 1990).

Internationally terrapins are favored for consumption, medicinal value and use as pets globally and especially in Asia. Native terrapin of China have already been drastically declined due to these reasons. Turtle species found in Chinese markets are collected in Asian countries. Besides Pakistan, Bangladesh, India, Nepal, New Guinea and even the species from the USA are affected. Trade and food markets in China are the major threat for Asian turtles. Turtles and Tortoises have been used as human’s food for centuries, but recent changes in Asian economies especially, when the Chinese currency became convertible, have opened direct access to international markets (Behler, 1997).

Survivors of million years, turtles in our millennium are in jeopardy due to many problems such as collected for pet trade, butchered for bones, flesh eaten, professed medical use and traded in devastating numbers. Similarly, agricultural and developmental activities destructed or altered turtle’s habitat affecting turtle populations. Many species of the terrapins and tortoises of the World will become extinct within the coming few decades due to lack of proper conservational action and plans (Sarwar et al., 2015).

Wetlands are also called as supermarkets, due to their vast and rich food webs and enrich ecological biodiversity. Freshwater wetlands are home for many species, including fishes, amphibians, reptiles, invertebrates, herbs and microorganisms. Currently wetlands are one of the most vanishing ecosystems in biosphere after tropical rain forests and coral reefs of warm Seas (Khan et al., 2006).

Commercial pressure on turtles is currently greatest in the Asian countries especially, south Asia and for east. Commercial excessive exploitation of terrapins in Asia over the last few decades, mainly for consumption, traditional medicines, pets and other uses, has been increasing sorrow decline of these valuable members of wetlands. It is estimated that at least thirteen thousand metric tons of wild turtles has been transporting (Moll and Moll, 2004).

The Wildlife of Pakistan has interesting and diverse segments because of its Geographical location between two bio-geographical regions: the Oriental and Palearctic regions. Some members are also resemble with Ethiopian fauna. Baluchistan and Himalayan area has fauna of Palearctic type, while the Indus plains have Oriental fauna. Indus plains extend from the coastal zone and Rann-Kutch of the Tharparker to the Himalaya in the north. The Makran coastal belt and some of the Indus flood plains have some mammalian species of Afro-Tropical origin. Pakistan has some of the hottest areas and some of the coldest and highest areas and that’s the reason that the country possesses some of the world's major climatic and floral biomes within a small land (Khan and Hussain, 1985).

The total estimated wetlands area is 78,000,00 ha in Pakistan, in which 3,100,000 ha of rivers, 56,000 ha of canals and irrigation steams, 110,000 ha of natural lakes and ponds, 92,000 ha of reservoirs of water storage, 108,000 ha of temporary pools and fish farms, 300,000 ha of Indus delta, and over 4,000,000 ha of water- logged and 250,000 ha to 283,000 ha area of coastal mangroves swamps (Ansari, 1987).

The Indus River, which is the major river of Pakistan, rises from Mansrowar lake on the Tibet plateau at a height of 3500 meters; it travels 1280 km before entering Pakistan and meanders another 1600 km before reaching the Arabian Sea. The Northern and Western mountains provide the drainage basin for the tributaries from the north and west. The freshwater ecosystems of Pakistan face stresses due to increase in human’s population and some natural actions. Most of the wetlands of Pakistan are in need of some urgent and major restoration plans. Most of freshwater wetlands provide sites for migratory birds, fishes, invertebrates and aquatic flora. Since several years, many wetlands of the globe have been degraded and have lost their significance due to human’s activities like, unsustainable exploitation, increased levels of urban and domestic wastes discharge in to the wetlands (Amjad and Kidwai, 2003).

ORDER CHELONIA/TESTUDINES OF PAKISTAN: Order Chelonia is represented in Pakistan by following 5 families, 13 genera and 15 species (Khan, 2006).

FAMILY CHELONIIDAE: (Hard-shell sea turtles):

Chelone mydas (Green Sea Turtle)

Caretta caretta (Logger-head Sea Turtle)

Eretmochelys imbricata (Hawks-bill Turtle)

Lepidochelys olivacea (Olive Ridley Turtle)

FAMILY DERMOCHELYIDAE (Soft-shell sea turtles):

Dermochelys coriacea (Leatherback Sea Turtle)

FAMILY GEOEMYDIDAE (Hard-shell terrapins):

Geoclemys hamiltonii (Spotted Pond Turtle)

Hardella thurjii (Brahminy or Crowned River Turtle)

Pangshura smithii (Brown-roofed Turtle)

Pangshura tectum (Indian Roofed Turtle)

FAMILY TESTUDINIDAE (Tortoises):

Geochelone elegans (Indian Star Tortoise)

Testudo horsfieldi (Afghan Tortoise)

FAMILY TRIONYCHIDAE (Soft-shell terrapins):

Nilssonia gangeticus (Ganges Soft-shelled Turtle)

Nilssonia hurum (Peacock Soft-shelled Turtle)

Chitra indica (Narrow-headed Soft-shelled Turtle)

Lissemys punctata andersonii (Indian flap-shelled Turtle).

The terrapins of Pakistan are entirely Oriental at both the species and generic levels and consist of two families, six genera and eight species [(Khan, 2006 and 2015; Azam and Saeed, 2011; Noureen et al., 2012; Safi and Khan, 2014; Khan et al., 2015; 2016) (Table 1.1 and 1.2)].

In Pakistan, two families of terrapins, family Geoemydidae (Hard- shell turtles) and Family Trionychidae (Soft-shell turtles) occur in the rivers and wetlands. The Nilssonia hurum, Nilssonia gangeticus, Geoclemys hamiltonii and Pangshura tectum are included in Appendix-I, whereas, Hardella thurjii, Chitra indica, Lissemys punctata and Pangshura smithii are listed in Appendix-II of the Convention on International Trade in Endangered Species of Flora and Fauna [(CITES, 2016) (Table 1.1)].

Terrapins of Pakistan are found in the entire Indus River system. Terrapins play important and key role in wetland’s ecosystems by scavenging upon diseased fishes and other aquatic animals. Turtle’s species of Pakistan are facing serious survival threats due to environmental changes, poaching, habitat alteration and unsustainable construction, shortage of water in wetlands, closure of canals, desilting and other anthropogenic changes (Khan, 2006; Safi and Khan, 2014).

Table 1.1. IUCN and CITES Status of terrapins of Pakistan.

Family Species Common Name CITES IUCN Status Status

Geoemydidae Geoclemys Spotted pond turtle Appendix I Vulnerable hamiltonii

Geoemydidae Hardella thurjii Crowned river turtle Appendix II Vulnerable

Geoemydidae Pangshura smithii Brown river turtle Appendix II Lower Risk

Geoemydidae Pangshura tectum Indian roofed turtle Appendix I Lower risk

Trionychidae Chitra indica Narrow headed turtle Appendix II Endangered

Trionychidae Nilssonia Ganges soft-shell Appendix I Vulnerable gangeticus turtle

Trionychidae Nilssonia hurum Peacock soft-shell Appendix I Vulnerable turtle

Trionychidae Lissemys punctata Indian Flap-shell Appendix II Lower Risk turtle

Table 1.2. Habit, Habitats, Reproduction and Behavior of Terrapins of Pakistan.

Species Habitat Feeding habit Clutch Incubation Behavior size period (Days)

Geoclemys Shallow ponds, Carnivore 5-15 169-213 Shy hamiltonii pools, lakes, rivers.

Hardella Pools, ponds, Herbivore 8-13 200-273 Shy thurjii lakes, canals, Saltwater.

Pangshura Lakes, pondes, Omnivore 7-8 75-112 Shy smithii puddles, canals.

Pangshura Standing and Omnivore 8-12 125-144 Non- tectum slow moving aggressive water. Chitra Sandy shallow Carnivore 60-120 22-40 Aggressive; indica river margins. Ambushes prey Nilssonia Rivers, lakes, Omnivore 25-40 25-35 Very gangeticus permanent ponds. aggressive

Nilssonia Rivers, lakes, Omnivore 20-30 25-35 Aggressive hurum permanent ponds.

Lissemys Lakes, rivers, Omnivore 6-14 30-40 Shy; punctata shallow pools. Aggressive

STUDY AREA

KHYBER PAKHTUNKHWA

Khyber Pakhtunkhwa was previously called as North West Frontier Province. This is the 3rd biggest province of Pakistan by population and by economy, located in the north-west of the country. It shares borders with FATA to the west; Gilgit–Baltistan (GB) to the northeast; Azad Kashmir and Islamabad to the east; Balochistan to the south and Punjab to the east and southeast (www.wikipedia.com, 2016).

The wildlife of KPK is unique due to its physiographic diversity in Pakistan. D. I. Khan abode xerophytic vegetation due to its lowest elevation in the province whereas the highest elevation near Tirichmir peak of Chitral supports charismatic species like snow leopard, Himalayan ibex, Snow cock and Snow partridge. Six National parks namely Ayoubia National Park, Chitral Gol National Park, Sheikh Buddin National Park, Saifulmalook, Lolusar-Dodipat and Broghil valley have been established, which are well known for the naturalists and biologists for their unique wildlife. The rare blind Indus dolphin is found in the Indus River. Three wildlife sanctuaries, thirty six game reserves and fifty two community game reserves have also been established in KPK, where hunting is regulated and the threatened and rare species are provided appropriate protection [(Shah, 2011) (Table 1.3)].

GEOGRAPHY

KPK is located on the Persian plateau on the junction of the slopes of the Hindu Kush of the Eurasian plate to the Indus-watered Mountains of south Asia, which is the main reason for more seismic activity in the area. The province could be divisible into the northern zone from Hindu Kush to the borders of Peshawar Valley and the lower zone from Peshawar to the D. I. Khan in south.

The major rivers in KPK province are the Indus, Kabul, Swat, Chitral, Kunar, Siran, Panjkora, Bara, Kurram, Dor, Haroo, Gomal, Jindi and Zhob Rivers.

CLIMATE

The northern zone of the province is generally snowy in winters with heavy rainfall and pleasant summers while in Peshawar Valley, the summer is hot and cold winter with less rainfall. The south zone of D. I. Khan is arid with low rainfall, hot summer and cold winter.

DEMOGRAPHICS

The total population is approximately 21 million in the province. Pashtun is the largest ethnic group, followed by Hazarewal. However, in D. I. Khan District most of its population speaks Saraiki.

LANGUAGES

PASHTO: Most of the peoples speak Pashto especially in the central districts.

HINDKO: Most of the peoples in Hazara speak Hindko.

SARAIKI: Most of the Peoples in Tank and D. I. Khan speak Saraiki.

KHOWAR: Most of the peoples in Chitral speak Khowar.

KOHISTANI: Most of the peoples in Kohistan and north half of Swat speak Kohistani.

GOJRI: minority in the northern hilly peoples speak Gojri.

ADMINISTRATIVE DIVISIONS

Khyber Pakhtunkhwa consists of 26 districts, comprising twenty one settled area districts and five provincially administrated area (PATA) districts (Table 1.4; Fig. 1.1).

Table 1.3. National parks of KPK Province.

Name Location Date Area Key Wildlife Established (Hec)

Ayoubia Abbottabad 1984 3,122 Koklass Pheasant, Kalij Pheasant, National Park Chakor Partridge, Yellow-Throated Marten, Common Leopard, Rhesus Macaque, Flying Squirrel. Chitral Gol Chitral 1984 7,750 Markhor, Urial, Snow Leopard, Wolf, National Park Himalayan Snow Cock, Chakor Partridge, Green Wood Pigeon Sheikh Dera Ismail 1999 15,540 Black Partridge, Grey Partridge, Chukar Buddin Khan Partridge, Rock Dove, Pied Bush Chat, National Park Red-Vented Bulbul, Fox, Hare, Jackal, Jungle Cat, Porcupine, Wild Boar, Wolf Saiful Malook Mansehra 2003 12,026 National Park Asian Black Bear, Marten, Ram Chakor, Snow Partridge, Himalayan Monal

Lulusar- Mansehra 2003 75,058 Common Leopard, Asian Black Bear, Ibex, Dudipatsar Marten, Himalayan Monal, Koklass National Park Pheasant, Ram Chakor Broghil Chitral 2010 Ibex, Blue Sheep, Snow Leopard, Brown Valley 134,744 Bear, Tibetan Wolf, Golden Marmot, Snow National Park Cock, Chakor Partridge

Table 1.4. Districts of KPK Province.

1. Peshawar 8. Malakand 15. Abbotabad 22. Karak

2. Charsadda 9. Buner 16. Haripur 23. Lakki Marwat

3. Nowshera 10. Swat 17. Mansehra 24. Bannu

4. Mardan 11. Shangla 18. Battagram 25. Tank

5. Swabi 12. Dir Lower 19. Tor Ghar 26. D. I. Khan

6. Kohat 13. Dir Upper 20. Upper Kohistan

7. Hangu 14. Chitral 21. Lower Kohistan

Fig. 1.1. Maps of Pakistan and KPK showing selected study districts.

CHARSADDA

Charsadda is a city and headquarter of Charsadda District. It is at an altitude of 906ft and lies 18miles from Peshawar. Charsadda spreads like a maple leaf and is bounded by Nowshera and Peshawar districts to the south, Mardan district to the east, Malakand District to the north and the Mohmand Agency (FATA) to the west. The area of the district is 996 sq.km. Total Population is 1,626,000 and population Density is 1,026/km2 (2,660/sq. mi).

Geographically, Charsadda could be divisible into Doaba and Hashtnagar. The district is at the extreme end of the monsoon winds. The inhabitant of the area enjoying four seasons in a year namely summer, autumn, winter and spring.

The district is administratively subdivided into three tehsils i.e. Shabqadar, Tangi and Charsadda Tehsils and 49 union councils (Fig. 1.2).

Charsadda can truly be called the land of rivers. River Swat, River Jindi, River Kabul are the main sources for irrigation [(Wikipedia, 2016) (Fig. 1.3 - 1.8)].

Fig. 1.2. Maps of KPK Province and Charsadda District.

Fig. 1.3. Jindi River in Charsadda.

Fig. 1.4. Swat River in Charsadda.

Fig. 1.5. Kabul River in Charsadda.

Fig. 1.6. Hisara Drain in Charsadda.

Fig. 1.7. Kashmalo Drain in Charsadda.

Fig. 1.8. Dub Drain in Charsadda.

PESHAWAR

Peshawar is the capital and biggest city of KPK province, located at the north-west end of the country about 160 km west of the Islamabad. The total population has estimated as 3.5 million. It is located at the eastern end of the Khyber Pass, close to the Afghan border (Fig. 1.9).

Peshawar has a geo-strategically important location. The district has one Tehsil (Peshawar tehsil) and there are 11 seats for provincial assembly (MPAs).

Peshawar is irrigated by various canals of the Kabul River and by its right tributary, the Bara River (Fig. 1.10-1.13).

Summer in Peshawar is start from mid-May to mid-September while winter starts from November and ends in March. Rainfall occurs in summer as well as in winter. The average summer rainfall levels are lower than those of winter (wikipedia, 2016).

Fig. 1.9. Maps of KPK Province and Peshawar District.

Fig. 1.10. Naguman (A distributary of River Kabul) in Peshawar.

Fig. 1.11. Shahalam (A distributary of River Kabul) in Peshawar.

Fig. 1.12. Budhni River in Peshawar.

Fig. 1.13. Bara River in Peshawar.

NOWSHERA

Nowshera (known locally as Nowkhaar) is an important city and a district in Peshawar valley. Nowshera city is located 27 miles east of Peshawar city at 34°0'55N 71°58'29E on the GT Road as well as on the Motor way between Islamabad and Peshawar. It is also one of the largest cities of the province. The district is administratively divided into two tehsils; Nowshera and Pabbi. Nowshera District is divided into 47 Union Councils and 5 provincial seats. Nowshera cantonment is located on the bank of Kabul River. The city still has post Anglo- Sikh wars barracks built in 1852-60. Total area is 1,748 km² (675 sq mi). It is bordered by Charsadda to the north-west, Mardan to the north, Peshawar to the west, Swabi to the north-east, Kohat District to the south, Orakzai Agency (FATA) to the south-west and Attock of Punjab province is to the east (Fig. 1.14).

The major source of income of the region is agriculture. Bara River, Kabul River and Indus River flow through Nowshera District (Fig. 1.15-1.16).

Fig. 1.14. Maps of KPK Province and Nowshera District.

Fig. 1.15. River Kabul in Nowshera.

Fig. 1.16. The junction of River Kabul and River Indus in Nowshera.

MARDAN

Mardan is a second biggest city and district in KPK Province. It is the center of the Yousafzai tribe, although a significant number of Mohmands have settled there over the past years. Mardan was once part of the ancient Gandhara civilization, the remains of which are still scattered throughout the area. It is the second largest city in the province located east to Charsadda, south to Malakand and Buner, west to Swabi and north to Nowshera. The district is located at 34°12'0N 72°1'60E and an altitude of 283 meters (928 ft) (Fig. 1.17).

Kalpani is an important stream of the district, other important streams join Kalpani are Baghiari Khawar, Muqam Khawar, Naranji Khawar, Lownd Khawar and Jalala khwar. Most of the streams drain into Kabul River in south (Fig. 1.18).

Most of the rainfall occurs in July and August. The relative humidity is quite high throughout the year while maximum humidity has been recorded in December i.e. 73.33 percent (wikipedia, 2016).

The district of Mardan is administratively subdivided into three tehsils i.e. Mardan, Takht Bhai and Katlang tehsils.

Fig. 1.17. Maps of KPK Province and Mardan District.

Fig. 1.18. Jalala Drain in Mardan.

D. I. KHAN

D. I. Khan is a southern city of KPK Province. It is located on the west bank of the River Indus. Chashma Right Bank Canal is the major canal for irrigation. D. I. Khan has hot summers and mild winters.

The city is connected to Peshawar via the Indus highway. Another road connects D. I. Khan to Mianwali of Punjab province through Chashma Barrage. The third major road connects it to Bhakkar District of Punjab. It is bordered by Lakki Marwat to the north, Tank to the north-west, South Waziristan to the south-west, Dera Ghazi Khan to the south-east, Bhakkar and Mianwali to the east.

The district is subdivided 47 union councils and 5 tehsils i.e D. I. Khan, Kulachi, Paharpur, Daraban and Paroa. The district is represented by 5 provincial assembly [(wikipedia, 2016) (Fig. 1.19- 1.20)].

Fig. 1.19. Maps of KPK Province and D. I. Khan District.

Fig. 1.20. River Indus in D. I. Khan.

The intensive exploitation of turtles in Asian market, has contributed to declines in turtle population across the continent. Turtles are also used for scientific studies, museum collections and laboratory dissections, neurological and circulatory demonstrations etc. There has been a long historical background of using Chelonians as food and medicine in China. The soft shell turtle are targeted mostly by local because these turtles have high demand in the international markets due to larger in size as compared to hard-shell turtles, low bone to bone ratio and gelatinous skin (Walters, 2000).

According to Chinese mythology, the terrapin, tiger, dragon and the Feng bird, are the four divine animals. Each animal is associated with a season and a compass point. The turtle represents winter and the north. This is why turtles are considered as “hot food”, to be eaten in winter. In China the use of terrapin’s shells in Traditional Chinese Medicine is an old tradition and can be found in at least 117 preparations. Some species are highly prized due to pharmaceutical values, like some parts of terrapins are used to heal cancer, while some parts are prescribed to treat male erectile dysfunction. The plastron is said to be “reinforcing the kidney and liver to strengthen the bones, nourishing the blood, reinforcing the heart, and normalizing menstruation to cure menorrhagia” (Table 1.5) (Altherr and Freyer, 2000).

Dried parts of terrapins and blood can be used as medicine. Turtle’ eggs and flesh are popular because of their aphrodisiac qualities. Turtle fat for making medicine for arthritis and the fresh blood of turtle for curing asthma is in practice. Soft-shell turtles are major

40 source of Traditional Chinese Medicine, and their shells are supposed to be highly effective for purifying blood and to cure many diseases. The persistence of turtles is valuable not just socially and environmentally but also for the services they provide to the wetlands by controlling other species, they may reduce algal bloom. Anthropogenic disturbance to wetlands can change ranging behavior with subsequent changing of key demographic processes. For example, stress in terrapins suppresses egg laying and production. Terrapins are of the important aquatic group of wetland. They play same role in the habitat which is played by vultures in the terrestrial ecosystems (Safi and Khan, 2014).

Table 1.5. The use of turtles in some Traditional Chinese Medicine preparations.

Name of Preparation Date of origin Application

th Guilinggao (Turtle’s 19 Century Skin, Heart diseases, Improving circulation, jelly) Assisting muscle growth, Relieving itching, Reducing acne, Kidney restoration. Qinghao biejiatang 18th Century Periodically recurring fever, Chronic low fever.

Sanjia fumotang 18th Century Fever, Blood stasis, Spasms.

Qinggusan 17th Century Periodic fever, Emaciation, Red tongue.

Zuoguiwan 17th Century Emaciation, Infertility, Night sweat, Confusion, poor eye sight, Dry mouth. Dabuyinwan 14th Century Irritability, Cough, Nocturnal emission, Buzzing in the ears.

Gujingwan 13th Century Normalizing menstruation.

th Sangpiaoxiaosan 12 Century Uncontrolled ejaculation and urinary excretion, Cloudy urine, Forgetfulness, Pale tongue.

An investigative researched survey report by WWF-P and the Sindh Wildlife Department for TRAFFIC reported the first trade of terrapins in 1990 in Sindh Province (Baig, 2006; Safi and Khan, 2014).

Commercial exploitation of body parts of terrapins in KPK province was introduced in the year 2006 for the first time. Poaching of soft- shell terrapins was first time reported in Pakistan by Baig (Shah, 1996; Noureen et al., 2012).

No prior scientific research has been reported on terrapins of KPK, so basic data on status of population and distribution of species is not available. The main objective of this study was to determine the status of population and distribution of terrapins in KPK province, particularly in the districts rich in wetlands and potentially provide better habitats for terrapins. And record the anthropogenic and natural threats faced by the freshwater turtle’s Species of the selected districts of KPK province.

Chapter 2

REVIEW OF LITERATURE REVIEW OF LITERATURE

Smith (1931) compiled a book “The Fauna of British India including Burma and Ceylon”. He has described the taxonomic characters, habit, habitat, and distribution of Amphibio-reptiles.

Minton (1966) published a book entitled “Herpetology of Pakistan” and discussed the distribution, biodiversity and abundance of the reptiles of Pakistan including Terrapins.

Martens (1969 and 1971) compiled the work of amphibian and reptilian on Pakistan. His work was directly concerned with Taxonomy and distribution of Amphibio-reptiles of Pakistan.

Choudhury and Bhupathy (1993) reported that Soft-shell turtles, namely Lissemys punctata, Nilssonia gangeticus, and Nilssonia hurum, are exploited in low level. Data of the captive stocks of terrapins of zoos in India was prepared through survey. Feedback was received from thirty five different zoos. Common species in these zoos were Lissemys punctata and Geochelon elegan. Sixty two geographic localities (45 Protected Areas), covering all but two biogeography zones, were visited during that study, and data of turtles was collected. Detailed analyses were done on the status of chelonians at both biogeographic and state levels, and action plans are proposed. Also, a new listing for population status was suggested for turtles and tortoises to incorporate in the Indian Wildlife Protection Act, 1972.

Javed and Hanfee (1995) reported Batagur dhongoka from conserved area of Dudhwa National Park, but they have remarked that these wetlands may represent marginal habitats for fauna. Hardella was reported by them as common in this area.

Klemens and Thorbjamarson (1995) reported that reptiles are an important source of protein for human’s consumption around the world especially in Asian countries. Exploitation of food is directly responsible for the decline of many turtles. It is imperative that more attention be focused on the improvement of sustainable use Programs for these turtles.

Aguirre et al. (1997) worked on the ecology of the Balson tortoise, Gopherus flavomarginatus. The studies got a result from bi-national effort with the collaboration of USA. The Balson tortoise was endemic to the Mapimian Sub province of the Chihuahuan Desert. Its decline in population was a result of many factors, including climatic changed and anthropogenic activities. The WWF-U.S. and the Turtle Recovery Program had supported research in the Sierra del Diablo District (Chihuahua State) where healthy populations, comparable to those of Mapiml, still remain. A joint U.S - Mexican plan to reintroduce the Bolson tortoise into the Big Bend region of southwest Texas had been explored.

Burke and Gibbons (1997) investigated a variety of freshwater organisms. They tested wetland boundaries by using a geographic information system model to define the land use activities of three

45 species of terrapins (Kinostemon subrubrum, Pseudemys floridana, and Trachemys scripts).

Canstano-mora (1997) studied the distribution, commercial exploitation as well as some of their conservation-related problems for 25 species of Colombian turtles. He updated information and raised some priority actions for legal conservation status of several species.

Choudhury et al. (1997) studied conservation and management of terrapins and tortoises in India, a study by the Wildlife Institute of India and the U.S Fish and Wildlife Service, a joint conservative and collaborative service and Management of terrapins and Tortoises in India was launched in May 1991. The main objective of that study was to estimate the population and determined the status of turtles and finding suitable habitats to establish protected areas for endangered chelonians, and to provide scientific training on turtle’s conservation and biological studies.

Herman and Tryon (1997) studied the distribution and ecology of the bog turtle, Clemmys muhlenbergii (Schoepff). They recommended some conservational measurements like: Management of sites, including restoration, selective cutting and pruning of forests, cattle grazing, and awareness of landowners was recommended.

Jacobson (1997) studied some diseases in wild populations of terrapins and tortoises. In the mid-1980s moribund flattened musk turtles with ulcerative lesions of the integuments and pneumonia were

46 identified in the Sipsey fork in north-central Alabama, and several species of emydine turtles with proliferative shell lesions were observed in Lake Black Shear in south-west Georgia. A major decline in populations of desert tortoises, Gopherus agassizh and Gopherus polyhemus were associated with respiratory tract disease. Declines of tortoise on the Chuckwalla Bench areas of critical concern, Riverside County, California, had been associated with an unusual shell disease. Chelonians may represent an excellent indicator species for fluxes in the quality of the environment in which they live.

Jennings (1997) studied the Gopherus agassizii, and its habitats in the western Mojave Desert. He observed that this species was badly affected by off-road vehicles. To determine habitat used and food selection, 18 large juveniles and adult tortoises were studied. The researched area contained four sub habitats or strata. They preferred native plants compared to non-native plants.

Luiijf (1997) investigated that the increased in wildlife trade had significantly decrease the tortoise and terrapins populations in the wild. Regulations of the “Convention on Trade in Endangered Species” (CITES) could be treated as a tool to help stop these declines, but serious problems in enforcement had prevented their successful application.

Mullen and Ross (1997) studied the habitat conservation plans for a desert tortoise. 72 specimens of desert tortoises, Gopherus agassizii, were removed from a selected area (one square mile 2.59 km2) of habitat in California. Tortoises were relocated to a section of fenced

47 habitat in a natural area. Results indicated that the native population of tortoises was not negatively affected by the addition of new tortoise on to their range.

Ramon (1997) worked with Land Tortoise in Spain, their status and conservation, two species of tortoises occurred in Spain, Testudo graeca and Testudo hennannlj. Although both these had received legal protection for over 20 years, their numbers continued to decline. The primary population of Testudo graeca in southeastern Spain was threatened by poaching and habitat destruction. A comparatively stable population occurred in Donana National Park and a reduced population was found in a small area in north-west Majorca. The endangered western race of Testudo hennanni occurs in southeastern Majorca, some parts of Minorca, and in only one remaining locality on mainland Spain, in the northeastern comer of the country. Populations that occurred along the Mediterranean coast until the tum of the century had been extirpated in the last 50 years. The last indigenous population of this tortoise in Spain was of ecological and biogeographically interests as it western most population of the species, isolated from other populations such as those in southern France. Two Testudo hermanni reintroduction projects were being conducted within protected areas from which tortoise disappeared some decades ago.

Sarkar and Hossain (1997) reported the population and habitat status of terrapins and Tortoises of Bangladesh. 28 species of turtles are found in Bangladesh; 21 are terrapins, 2 are tortoises and 5 are marine turtles. Bangladesh exported an average of 600,000 US$

48 turtles per annum and the exported turtles mostly consist of Nilssonia hurum, Nilssonia gangeticus, Chitra indica, Lissemys punctata, Morenia petersi, Hardella thurjii, and Pangshura tectum. Turtles are collected from their natural habitats during breeding seasons. Wild populations of these reptiles are decrease with increase in human’s population, urbanization, sand mining, use of agrochemicals, drainage of wetlands, and deforestation.

Meylam and Donnelly (1999) investigated that the Hawksbill turtle (Eremochelys imbricate). Most populations were depleted, Only 5 regional populations remained with more than 1000 females nesting per year (Seychelles, Mexico, Indonesia and Australia). Hawksbills were closely associated with coral reefs, one of the most endangered in marine ecosystem types, with good management and enforcement are effective tools to improve the conservation of hawksbill turtle.

Passmore and Brooks (1999) observed that snapping turtle eggs from four distinct populations from North American species. Embryo mortality was high in two southern populations, variation in embryo viability and hatchling survival between populations indicated that each population responds differently to same conditions in captivity.

Rashid and Swingland (1999) observed the habitat, distribution, status, reproductive biology, feeding habits, allometric relationships, and ecology of twelve species of terrapins from Bangladesh. They observed that natural habitats had destroyed and several species were now became extinct from their former wild habitats.

Shrestha (1999) investigated the tortoises and terrapins of Nepal had intrinsic biological, educational, religious and inspirational value. They were deeply rooted in the Hinduism and Buddhism and medicines. They were unique and were worthy of long-term conservation and management up to the end of the 19th century, turtles were widely distributed throughout the wetlands of the Terai and the Himalayan region of Nepal. However, populations in the floodplains of the Koshi, Gandaki, Karnali and Mahakali rivers were in decline as a result of habitat destruction, alteration (Dam construction, deforestation, and draining of swamps), over fishing pollution and poaching. The present stems and distribution of Nilssonia gangeticus, N. hurum, Chitra indica, Geoclemys hamiltonii, Hardella thurjii, Lissemys punctata, Malanochalys tricarinata, M. trijuga, Pangshura dhongoka, P. Kachuga, P. smithii and P. tectum.

Souza and Shinya Abe (1999) examined the biology of Phrynops geoffroanus inhabiting in south-eastern Brazil. They observed high population and they concluded that this species is feeding on organic waste. Other reasons are: absence of predators and increased availability of nesting grounds in the area.

Van Dijk (1999) reported that Asia was previously rich in habitats for turtles. More than one hundred species of terrapins and tortoises are native to Asia, and new discovered species continued to be described. Unfortunately, the survival of these turtle species was of real concern. The Red list of Threatened Species included 37 Asian species, Including 5 in the Critically Endangered category, 9 considered as Endangered, and 23 as Vulnerable, as well as 18 species which were

Data Deficient but perceived to be under some level of threat. At previous, a re-evaluation of it the threats to Asian tortoises and terrapins considered more species to fall in the threatened categories. Details of the status of and threats to individual turtle species in most countries of South, Southeast, and East Asia were given in the country papers in this volume.

Whitaker (1999) reported, the commercial trade of a large scale of turtle’s meat in West Bengal. Lissemys punctata was mostly observed in these markets. Batagur among hard shell was second to Lissemys.

Dudgeon (2000) studied the conservation of freshwater bio-diversity in Indian Realm. Wetlands in Asia are under the serious threat due to increase in human’s population and the rapid pace of development has led to the degradation of natural habitats throughout the region.

Joyal et al. (2001) studied the habitat and movements of two species, spotted turtles (Clemmys guttata) and Blanding's turtles (Emydoidea blandingii). Individuals of these species are found in permanent and seasonal wetlands and used uplands for nesting.

Rao (2001) studied fauna of the Ganga River, India which is very important because its water is used for human and cattle consumption, Electricity generation, fishing and irrigation and for pilgrimage. 40 species of zooplanktons, four crustaceans, 15 mollusks, 51 Insects, 83 fishes, 12 terrapins, 2 crocodiles, 48 aquatic birds and two mammalian species are found in the upper Ganga River. The river has been under continuous threat of pollution by

51 sewage and disposal of dead bodies, deforestation and use of chemicals as fertilizers and pesticides, bathing, pilgrimage and water development programs. The pollution of the river is a serious matter of concerned for all. Several agencies for example, the Central Ganga Authority, several research institutions, government and NGOs have done work for many projects. Local people’s participation in many programs has contributed much to the biological restoration in the Ganga River. This paper presents species lists and highlighted the major issues for resource management in Ganga River.

Pearse and Avise (2001) studied the reproductive biology, behavior and genetic Paternity of fishes, amphibians and reptiles. Turtle by contrast had received fewer attentions, yet they displayed a variety of main behaviors and life history characteristics that made them better understanding of animal’s reproductive strategies.

Engstrom et al. (2002) studied Phylo-Genetic relationship of Chitra Spp. The intensive human’s exploitation of turtles has contributed decrease in terrapin’s populations in Asia. 75% of Asia's turtles were endangered and half were threatened. A recent workshop on the crises of Asian turtle’s species might include unrecognized, narrowly distributed species of much higher concern. Individuals from Thailand have been described as a separate species, Chitra chitra, but this has not been accepted by most of the herpetologists and they considered Chitra as a monotypic Genus. Phylogenetic analyses of data from the mitochondrial ND4 gene revealed the monophyletic lineages within Chitra genus: C. indica, C. chitra, and a third

52 unnamed, probably Critically Endangered, which highlights the importance of systematic studied in determining conservation priorities.

Jackson (2002) studied the physiological adaptation of the painted turtle, in temperate climates. He studied the effect of climatic factors on this species. Two general physiological adaptive responses were studied viz., the coordinated depression of metabolic processes within the cells and the second was an exploitation of the extensive buffering capacity of the turtle exoskeleton and endoskeleton to neutralize the large amount of lactic acid that eventually accumulate.

McCoord and Thomson (2002) described a new terrapin’s species of long-necked turtle from northern Australia; the species Chelodina novaeguineae was restricted to southern New Guinea. The new species differed from its New Guinea counterpart in being a larger species with a border shell and wider plastron, the skull having paired premaxillae and a thin parietal ridge, having unifrontal bone, posteriorly partially dividing the parietals, in the form and connection to the pterygoids of the vomer, and narrower cristapar- occipitalis.

Saunders et al. (2002) observed that terrapin is most endangered group in the world. They presented three points for conservation strategies for wetlands: whole-catchments plan, natural flow maintenance and exclusion of non-native taxa.

Azam et al. (2003) surveyed the distribution and status of terrapins in the Indus River. Surveys were conducted in Indus River adjacent to Sukkur Barrage, Guddu Barrage and Jamaldin Wali Pond areas adjacent to Kandh Kot during March-April 2003. Six species of turtles i.e. Nilssonia gangeticus, Pangshura smithii, Pangshura tectum, Hardella thurjii, Chitra indica and Lissemys punctata were observed from the study area Pangshura smithii and Chitra indica were observed to be abundant in the study area.

Luiselli (2003) studied the seasonal activity and feeding habits of the three sympatric Afro-tropical tortoises, Hinge-back tortoise (Kinixys belliana nogueyi, Kinixys erosa and Kinixys homeana) were found in sympatry in the rain forests of the Niger Delta, southern Nigeria.

Platt et al. (2003) studied the population status and protection of the Critically Endangered Burmese star Tortoise Geochelone platynota in Myanmar. This species was endemic to the dry zone of central Myanmar. Populations were believed to be in decline throughout its limited range due to over exploitation for commercial trade.

Spencer and Thompson (2003) concluded that the nest site selection of turtles in micro and macro habitat had important consequences for terrapin’s health and population.

Wilson et al. (2003) studied the technique of counting growth rings to estimate the age of turtles in the scientific literature. They investigated 145 scientific research papers that have been used for age estimation with the help of counting rings on scales.

Khan (2004) presented a complete check list of Amphibio-reptiles of Pakistan. He described a recent herpetological collections and several new amphibian and reptilian taxa have been added to the herpeto- fauna of Pakistan. Thus increasing the number of species from Minton's 144 and Mertens 178 to 225.

Lowary et al. (2004) investigated the mortality of air-breathers as a significant risk. They correlate turtle catch rates in harvested lakes and with no harvested lakes. Harvest had minimal effect on the size of turtle captured. They suggested that painted turtle population likely had been impacted by harvested activities. Further work was needed to determine whether there were any long-term effects on painted turtle populations.

Reese et al. (2004) studied the submerged hatchling of Chrysemys picta, Chelydra serpentine and Graptemys geographica in normoxic and anoxic condition at 3°C. Periodically, terrapins were removed, Lactate and glycogen were measured from different organs along with relative shell minerals like: (Na), (K), (Ca), (Mg), (P) and (CO2).

Luiselli et al. (2005) studied the effect of oil industry on related to the habitat destruction and pollution on four species of terrapins (Pelusios castaneus, Petusios niger, Pelomedusa subrufa, Trionyx triunguis) in west Africa. The number of turtle specimens observed during their study declined drastically in polluted sites.

Akbar et al. (2006) observed all the eight species of terrapins from the rivers and canals in Punjab. The most abundant species was Pangshura smithii followed by Pangshura tectum. The status of Hardella thurjii and Chitra indica were rare, whereas the status of Geoclemys hamiltonii, Nilssonia hurum and Lissemys punctata were observed as frequent and that of Nilssonia gangeticus as common, while Geoclemys hamiltonii, Nilssonia hurum and Lissemys punctata were recorded as frequent. Hardella thurjii and Chitra indica were rare.

Bowne et al. (2006) under took a 4 years study to calculate connectivity based on observed movement rates and movement probabilities for painted turtles (Chrysemys picta) in USA. The influenced of habitat quality on connectivity had often been ignored, but their results showed its significance.

Cheung and Dudgeon (2006) investigated the Asian turtle’s crisis. They surveyed different markets in south China during 35 months. 950251 individuals of 157 terrapin species were recorded. All without two of the 157 species were encountered in Hong Kong; Guangzhou ranked second in diversity (113 species) and Shenzhen third (89 species). 72 globally threatened species were found during that survey. The majority of species traded had natural ranges that included China and neighboring countries. Those non-Chinese Asian turtles (Bataguridae) constituted around two-thirds of the 77 species were found in that survey.

Khan (2006) has compiled all up-to-date available information on the amphibio-reptiles of Pakistan. After reviewing of the available published literature on the herpeto-fauna of the country.

Narain et al. (2006) studied the ecology and population dynamics of terrapin Pangshura tentoria and its role as water purifier. The study site “Panchnada” is the area, where there is a junction of five important national rivers and is preserving an appreciable population of nine species of terrapins. Pangshura tentoria was located at all the sampling stations surveyed by the authors, and hence selected for that study.

Shiping el al. (2006) reported that China has most diverse freshwater turtle fauna but also a major consumer of terrapins. Over-collecting, poaching, habitat alteration and destruction increased drastically the terrapin’s population in China. The main factors that lead to illegal trade include the cultural belief that turtles were a viable food and medicine product, lack of conservation awareness, poaching of turtles as a supplement to income, and poor law enforcement. Possible conservation strategies were discussed.

Noureen (2007) mentioned in her research paper about Dr. Khalid Javed Baig’s report of Taunsa visit, she mentioned that a family of about 40 persons, camping at Taunsa Barrage for two months killed Chitra indica and Nilssonia gangeticus to obtain plastron and chest pellicles. They collected over 200 turtles per week. The Pakistan Wetlands Program team in its visit to D. I. Khan on April 17th-22nd 2007 found that the communities called Kails residing along the

River sides were involved in capturing Nilssonia gangeticus and Nilssonia hurum. She reported that kails community is expert in turtles hunting and these peoples use traditional equipment’s like spears and nets for capturing the turtles. She reported that according to kails community and other local peoples all the eight native species of terrapins of Pakistan are found in D. I. Khan but Nilssonia gangeticus, Pangshura smithii, Pangshura tectum and Lissemys punctata were in abundance status here.

Bour (2008) studied the Global diversity of terrapins. Today, about 250 of the total of 320 species of terrapins have recognized; mostly from tropical and subtropical zones. Diversity hotspots occurred in the Southeast North America, regarded Emydidae, and in the lndo- Malayan region, mostly Geoemydidae and Trionychidae. Chelidae were predominantly Neotropical and Australasian, While Pefo- medusidae were African.

Fatima (2008) researched on distribution and current status of terrapins of Thatta, Badin, Sanghar and Sukkur districts of Sindh province during the years 2004-2006. All the eight species of terrapins viz. Lissemys punctata, Pangshura smithii, Pangshura tectum, Chitra indica, Nilssonia gangeticus, Nilssonia hurum, Hardella thurjii, and Geoclemys hamiltonii were observed. Six species of terrapins were found in District Thatta. Lissemys punctata was found to be more common, while Chitra indica, Nilssonia gangeticus, Nilssonia hurum, and Pangshura smithii were common, while Hardella thurjii was less common. 4 species of terrapins were observed in Badin District. Lissemys punctata was more common,

Nilssonia hurum as common, while Geoclemys hamiltonii as rare. Six species found in the Sanghar District. Lissemys punctata was found to be common, Nilssonia gangeticus, Pangshura smithii and Hardella thurjii were less common. These species were commonly found in Chotiari Wetland Complex, while Geoclemys hamiltoniii as rare. In Sukkur district, surveys were made along the right and left bank of Sukkur Barrage. Along the right bank area of Sukkur Barrage, six species of terrapins were recorded, Chitra indica was found to be common, Pangshura tectum, Pangshura smithii and Nilssonia gangeticus were common, while Hardella thurjii was less common, the Population of Geoclemys hamiltonii was rare. Along the Left bank of Sukkur barrage, six species were observed, Chitra indica was common, while Nilssonia gangeticus, Pangshura tectum, Pangshura smithii and Hardella thurjii were less common. Geoclemys hamiltonii was rare in the study area.

Azam and Nazar (2009) studied the population status of terrapins at four selected riverine wetlands Viz., Chashma Barrage, Taunsa Barrage, Ghazi Ghat and Head Punjned. Six species of terrapins were recorded in that survey. These include Chitra indica, Nilssonia gangeticus, Nilssonia hurum, Pangshura smithii Geoclemys hamiltonii and Lissemys punctata. P. smithii, N. gangeticus and G. hamiltonii were found at all the four sites. Chitra indica was recorded at three sites including Taunsa Barrage, Ghazi Ghat and Head Punjnad while N. hurum was found only at Head Punjnad. Capturing of terrapins for trade is major threat to the terrapin’s species. Other threats include accidental killing in fishing nets and angles etc.

Das and Singh (2009) studied the Taxonomy of chitra indica, The Indian narrow headed soft-shell turtle. They described the Taxonomy of this terrapin as: This is an extremely large (Total carapace length at least 110 cm). Highly aquatic species. A large clutch consist of 65- 193 eggs. Each egg is about 26.8 mm in diameter and 10.4 g mass. The breeding season is the monsoon in central India and in northern India, Bangladesh.

Kumar et al. (2009) reported that Soft-shell terrapins are the endangered group of aquatic animals that need an urgent attention. In Kerala (India), 2 species of terrapins, Melanochelys trijuga coronata (Schweigger, 1812) and Lissemys punctata punctata (Lacépède, 1788) are exploited from Vembanad wetland and associated wetlands in Punnamada to meet the requirements from local motels and toddy shops.

Noureen (2009) reported preliminary finding of poaching of freshwater turtle’s parts in Sindh during November 2009.

Ahmad and Das (2010) surveyed about Assessment of Present Status and Conservation of Tortoises and Terrapins in Northeastern India. The study was conducted in the six northeastern states (Excluding Tripura) of India involving protected areas, wetland habitats (River, beels, and marshes), ex-situ conservation areas, and temple ponds. They used river transects to document the diversity. They documented 19 species out of 21 species so far reported from the region. Each species is backed up with color pictures. Habitat destruction due to illegal felling, cultivation, over-fishing, and

60 poaching are looming threats to the terrapin’s population in northeastern India.

Azam (2010) visited and reported studies on population status of terrapins at selected wetlands (Head Qadirabad, Head Marala, Head Rasool barrage) for study of population status of turtles during July, 2010. Three species of turtles were observed during the survey. These include Pangshura smithii, Lissemys punctata and Nilssonia hurum. The observed numbers of the turtles were not very high as there was high flood in the rivers and conditions were not much batter for observation of turtles.

Azam et al. (2010) surveyed the abundance and distribution of terrapins at Guddu and Sukkur barrage under the project “status and distribution of threatened species of terrapins in selected areas of Indus River system”. The study was conducted in the lower Indus basin i.e. Guddu and Sukkur Barrage to study the abundance, distribution and threats to the terrapin’s population. Six species of terrapin’s viz. Pangshura smithii, Lissemys punctata, Nilssonia gangeticus, Chitra indica, P. tectum and Geoclemys hamiltonii were observed at Guddu Barrage while four species of terrapin i.e. P. smithii, P. tectum, C. indica and N. gangeticus were recorded at Sukkur Barrage. Illegal and unsustainable capturing of turtles for trade and livelihood of the local community is major threat. Use of chemicals to capture the turtle is a serious problem faced by these animals as it is resulting in mass mortality of terrapins.

Azam and Saeed (2010) surveyed the status and distribution of species of terrapins in selected study areas of Indus River system. The survey was conducted at Head Trimmu and Head Sidhnai with the following objectives; 1. To study the population distribution and status of terrapins species at Head Trimmu and Head Sidhnai. 2. Record illegal hunting of terrapins. 3. Record natural and anthropogenic threats faced by the terrapin’s species. Two species of terrapins were recorded at head Trimmu, Pangshura smithii was most common species at the site. 207 turtles of P. smithii were found. The greatest number of individuals found was at the downstream of the headwork where river bank is sandy. Other species of terrapins recorded at head Trimmu was N. hurum. Only three individuals of N. hurum were observed at the upstream of the headwork where most of the fine textured sediment is deposited. None of the individuals of this species was observed basking and were only captured in drag nets. No individuals of N. hurum were observed in canals and downstream of the headwork as well. No other species of terrapins was recorded at Trimmu headwork. The only species of terrapins observed at Sidhnai was the P. smithii. More than two hundred individuals of P. smithii were observed. Most of the individuals were found basking at the downstream of the headwork.

Eskew et al. (2010) studied the Populations of semi-aquatic turtles that depend on high survivorship of reproductive adults, habitat alteration in suburban areas. They studied Chrysemys picta in five ponds in North Carolina. They designed a program MARK for

62 population model examining the effects of location and sex. Their results showed approximately 100 turtles/ha population densities for 4 years in all ponds occurring at a recently developed site.

Patrick and Gibbs (2010) studied interactions between highways, structure of population and movements of terrapins. They examined the effects of industrialization and urbanization on populations of terrapins. They sampled and marked terrapins in 15 ponds arranged along a steep, urban and rural gradient in New York. They captured 494 terrapins, the majority of which were Chelydra serpentina (n = 191) and Chrysemys picta picta (n = 122). Their study suggests that roads alter both local and landscape-level terrapin’s populations.

Azam and Saeed (2011) surveyed the distribution and status of terrapins at Taunsa and Guddu Barrages and Punjnad Headwork. Five species of terrapin’s viz., Pungshura smithii, Lissemys punctata, Nilssonia gangeticus, Chitra indica and Geoclemys hamiltonii were observed from the study sites. Pangshura smithii was recorded at all the study sites while Chitra Indica, Geoclemys hamiltonii and Nilssonia gangeticus were only recorded at Taunsa Barrage. Lissemys punctata was observed both at Punjnad Headwork and Taunsa Barrage.

Liebing et al. (2012) studied the phylogenetic relationships of different Nilssonia species. Mitochondrial DNA and nuclear DNA confirm the mono-Genic of the genus.

Mahmood et al. (2012) studied the distribution and abundance of terrapins of Korang River, Islamabad-Rawalpindi. Three species were recorded, Lissemys punctata was found to be the most common up to 56%, Nilssonia gangeticus 30% and Pangshura smithii was 8% of total number of terrapins observed while 6% turtles were unidentified.

Noureen et al. (2012) reported the poaching of turtle’s body parts in Pakistan. A well-organized terrapin trade was started in Pakistan in 2002. Turtle’s body parts are transported to wildlife contractors in Peshawar, Lahore and Karachi. These cities have International exits and therefore preferred by the wildlife traffickers for export of terrapin consignments. China, Hong Kong, Vietnam and Korea are the final destinations.

Begum et al. (2013) describe the current status of mammalians and reptilians fauna at hub dam area, Sindh and Baluchistan. Twenty five reptilian species belonging to 3 orders and 12 families were also recorded from the area.

Hossain et al. (2013) studied Morphometry of Indian Roofed turtle, Pangshura tectum (Gray, 1831) in Bangladesh in several district of Bangladesh. They concluded that the average weight of the female P. tectum was 4.8 times, which was more than that of the male.

Rehman et al. (2013) conducted a survey to evaluate the illegal trading terrapins and tortoises in different markets of Bangladesh. They collected data through questionnaire interviews. It was

64 estimated that 60-70% of terrapins and tortoises supplied in the markets were softshell turtles such as Lissemys punctata, Nilssonia hurum and the other remaining part was hard shell (30-40%). The price of Lissemys punctata varied from Tk. 400-450/kg, Nilssonia hurum Tk. 450-650/kg, N. gangeticus Tk. 400-450/kg, Morenia petersi Tk. 250-300/kg, Pangshura tectum Tk. 200-250/kg and Geoclemys hamiltonii Tk. 200-250/kg were found during the current survey period.

Bhupathy et al. (2014) studied the Taxonomy of the Lissemys punctata (Family Trionychidae), they described the Taxonomy as: This is a small soft-shell turtle with a carapace total length of up to 350 mm. Three subspecies are found in Indian sub-region. These subspecies are found in different wetlands and the populations are more stable and not yet seriously threatened.

Chng (2014) reported for TRAFFIC on escalating trade of Geoclemys hamiltonii of Asia. A research study of this species which was rescued from a seizure in Hong Kong. Of this, at least 1865 were seized between January 2013 and March 2014. Data indicated that most of the shipments were carried from Bangladesh, India and Pakistan. International smuggling occurs in popular demand from the pet trade and human’s consumption.

Ramakrishna et al. (2014) reviewed a collection of the research papers related to Testudines of India. Different aspects of diversity studies pertaining to terrapins in India was presented in this review along with threats and protective initiatives in different areas of India

65 in different timeline and Pattern of demand. Although most of the traffickers resulted in arrests.

Safi and Khan (2014) studied the distribution and current population status of terrapins of Charsadda, KPK. 365 specimens of terrapins were observed of 02 Families Viz., Geoemydidae; Hardella thurjii, Pangshura smithii and Pangshura tectum and Family Trionychidae; Chitra indica, Nilssonia gangeticus, Nilssonia hurum, and Lissemys punctata andersonii were investigated. Lissemys punctata and Nilssonia gangeticus were in better population status, whereas, Hardella thurjii and Pangshura tectum were observed as rare. Geoclemys hamiltonii was not sighted in Charsadda.

Cruez et al. (2015) reported the poaching of Geochelone elegans in India and Thailand. Within India, this tortoise has gained protection as a Schedule IV list species of the Wildlife (Protection) Act 1972 for over 40 years. This paper documented the poaching of 55,000 individuals tortoises poached from just one site in India. Although local demand continue, these individuals seem to have been major source for pets in other Asian countries (e.g. Thailand and China). Since 1975, this tortoise has been included in Appendix II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) that regulates all commercial trade. In consideration of conservation and animal welfare concerns, they also call for more field research to determine the impacts of poaching on wild populations of this species, an updated assessment of its conservation status, increased cooperation between national enforcement agencies, and the implementation of targeted human

66 behavior change initiatives to help reduce consumer demand for this species.

Kayani et al. (2015) studied the Morphometry of the terrapins from Rawalpindi and Islamabad Region of Pakistan. They studied, 20 specimens of three different species i.e., Lissemys punctata, Nilssonia gangeticus and Pangshura smithii were investigated from thirteen different study sites. Among these three species of terrapins Nilssonia gangeticus was biggest and heaviest species with 30.42 cm and 2276 g measurements. While Pangshura smithii was lowest with 18.08cm in length and 510g in weight.

Khan (2015) reported the terrapin’s fauna of the Indus valley. He described with notes on morphology, natural history and threats. According to him, the terrapins of Pakistan belong to two families: Family Emydidae includes the genera Geoclemys, Hardella and Pangshura; Family Trionychidae includes the genera Nilssonia, Chitra and Lissemys.

Khan et al. (2015) studied the distribution and population status of terrapins from four selected districts from Sindh province and four from KPK province of Pakistan. Charsadda, Peshawar, Nowshera and D. I. Khan of KPK, while Thatta, Badin, Sanghar and Sukkur districts from Sindh province. Eight species viz, Lissemys punctata, Pangshura smithii, Pangshura tectum, Chitra indica, Nilssonia gangeticus, Nilssonia hurum, Hardella thurjii, and Geoclemys hamiltonii were observed. Geoclemys hamiltonii was observed in Badin, Sanghar and Sukkur as rare, while other species were

67 common, less common or intermediate level. Pangshura tectum was observed from Sukkur only while Chitra indica in all the four studied districts of Sindh. Geoclemys hamiltonii was only observed in D. I. Khan of KPK province. Lissemys punctata was the most common species in KPK. Population of terrapins in Sindh is richer than KPK.

Rahman et al. (2015) investigated the conservation, occurrence and exploitation of terrapins in Sangu Matamuhuri Reserve area of Bangladesh, from 2011 to 2015. During their survey, they get eight species which were Heosemys depressa, Manouria emys, Cuora mouhotii, Indotestudo elongata, Pangshura sylhetensis, Cyclemys spp., Amyda ornata and Lissemys punctata. The critically endangered H. depressa and the endangered C. mouhotii are recorded from Bangladesh for the first time, and the endangered P. sylhetensis is recorded from this area for the first time. They documented 2 isolated populations of M. emys in the Sangu Matamuhuri Reserve Forest. Subsistence hunting is probably the most immediate threat to chelonians in this region. With no intervention, subsistence hunting will likely cause large-scale local extirpation of extant, low-density populations.

Rais et al. (2015) conducted a study to examine factors influencing the diversity and spatial distribution of herpeto-fauna in the Chakwal District, Punjab, Pakistan. They gathered data from January 2011- December 2013 in selected sampling sites using standard methods. They used satellite images to identify and classify different landscape features of herpeto-faunal diversity varied from 2.07 (unprotected tropical thorn forest) to 0.27 (mixed habitat in a wildlife sanctuary),

68 while evenness oscillated between 1.76 (unprotected tropical thorn forest) and 0.21 (mixed habitat in a wildlife sanctuary). The two units with the highest similarity (0.82) were wetlands inside a protected area and wetlands outside of a protected site. Of the 12 variables tested, the factor analysis produced seven significant variables (r>0.80) influencing the herpeto-fauna of the area. The processed image shows that the area is still enriched by natural vegetation and forest. However, the natural sites are intersected by road networks that make them accessible. Changes in the land-use practices such as habitat conversion for residential development, housing schemes, and road development may cause reductions in the diversity of amphibio- reptiles. Data on current biodiversity is needed for planning and we have suggested options for herpeto-fauna conservation and management.

Sarwar et al. (2015) conducted a survey about the abundance of population and habitat types of KPK. Eighty two specimen of seven species of terrapins at sixteen different sites in River Indus and some of its tributaries from KPK and Punjab were observed. The species documented were, Pangshura smithii, Pangshura tectum, Geoclemys hamiltonii, Nilssonia gangeticus, Nilssonia hurum, Chitra indica and Lissemys punctata. It was observed that Swabi District of KPK was most populous area with three most populated sites; Yar Hussian stream, Allah Dher River and Badri stream.

Zaib-Un-Nisa et al. (2015) studied the presence of seven heavy metals in blood of three terrapin species from Balloki and Trimmu areas in Punjab. They collected the blood samples from Pangshura

69 smithii, P. tectum and Lissemys punctata and then placed in heparinized vials. Then heavy metals were detected in blood samples by using Atomic Absorption Spectrometer. Among seven heavy metals, Zinc concentrations were found maximum and Cd concentration was found minimum in blood of all the three species.

Khan et al. (2016) studied the distribution, status and protection of terrapins of Peshawar Valley. They recorded 2,791 specimen belonging to the family Trionychidae, including the Chitra indica, Nilssonia gangeticus, Nilssonia hurum and Lissemys punctata andersonii and the family Geoemydidae, including Pangshura smithii, Hardella thurjii and Pangshura tectum. Based on our present study data, Lissemys punctata (28.52%) and Nilssonia gangeticus (27.41%) were common, whereas, Nilssonia hurum (14.76%) and Pangshura smithii (11.04%) were less common. Chitra indica and Pangshura tectum were found at levels that may be categorized as scarce (7.31% and 7.49%, respectively). Hardella thurjii (3.48%) was rarely recorded. On the other hand, Lissemys punctata (28.52%) and Nilssonia gangeticus (27.41%) were common at all 18 sites sampled, followed by Pangshura smithii at 16 of 18 sites. The Geoclemys hamiltonii was unrecorded from Peshawar Valley during that study.

Chapter 3

MATERIALS AND METHODS MATERIALS AND METHODS

Charsadda, Peshawar, Nowshera, Mardan and D. I. Khan Districts were selected in KPK Province as study areas during January 2013 to December 2015 after baseline studies. Twenty three different study sites were selected from these selected five districts (Peshawar, Charsadda, Nowshera, Mardan and D. I. Khan) from Khyber Pakhtunkhwa. These study sites were selected from Indus River and some of its tributaries in the selected area like, Kabul River, Swat River, Jindi River, Budhni River, Bara River; some drains like Jalala Drain, Fazalabad Drain, Kashmalo Drain, Dub Drain and Hissara Drain; two canals one from lower Swat River and another Sheikh Canal from Kabul River (Fig. 3.1-3.3). Several most reliable methods and surveys techniques were employed for the observation and census of turtles. The observations were usually made from a raised position to get a clear view of the habitat during each visit to the twenty three study sites. The status of population of different species was recorded. Identification of the terrapin’s species in the study sites was carried out with the help of published literature (Khan, 2006, 2015; Khan et al., 2015; 2016).

COUNTING METHODS

A. DIRECT COUNTING

1. Habitat Searching /Transect method Several hours search was carried out to detect more possible turtles. This searching consists of about 20 ha. (Within 250 meter radius of the observation/sampling points). This method was very suitable for counting the species and number of turtles. Nearly 4 km area was selected for observation of the habitat. The turtles were active both in the days and night, some of turtles were found sitting on partly submerged logs, larger stones and even on mudflats by the side of water, while some are seen moving or resting just near shelters, they become alert to see the observers, some of them run away very fast and dive into the wetland or lost in the mud underwater. But finally were caught with the help of three-four persons. This practice was carried out for at least 1 hour to find the different species of turtles. Turtles emerging for sun basking and floating at the banks of the rivers and canals were observed and counted. Different species were observed and identified with the help of Binocular Minolta with the power of 10 X 50 mm from a distance. It was observed that there are suitable habitats, abundance of herbs and shrubs, food mostly Insects and small fishes. The status of population of different Turtles species was satisfactory, but the population was very poor on the temporary and shallow Water, where there were few dry and scattered herbs and shrubs. Approximately 4 km of study areas were covered for survey and finally the populations of different species of turtles were

72 estimated per square km. Their exact location and home range was recorded by G.P.S, So that where any biologist comes for study and they can easily locate the place where the recorded or reported species are found. Similarly night survey was done with the help of search lights and torches. Canals were surveyed, during canal closure season (December–January). Animals found above ground in the dry canal were identified and counted.

2. Capture through Nets Netting technique has been used for capturing the terrapins in cold weather as no basking activity was found during winter season. Small turtles were captured by using nets, such as cast net and drag net. It was done in small water reservoirs like drains, canals and small rivers. In this way, the maximum study sites were surveyed.

3. Boat Surveys As survey of rivers were made by using fishing boats and making observations while traveling within study sites, same routs were traveled on a return trip. In this way 4 km round trip was covered in one round. As soon as the species sighted, the approximate latitude and longitude and wetland types were recorded and documented.

4. Incidental Sightings Incidental sighting was also helpful to determine the presence and population status of the terrapin’s species. Dead turtle specimens were also recorded. In this way number of terrapins, species, date, time, latitude, location, and longitude and habitat type were recorded.

5. By Basking Behavior This method of sitting or locating the species is the most suitable but it can be applied mostly in sunny day. Due to cooler weather and cold water this cold blooded reptile avoid to live in water and so they come outside the water to enjoying sunshine and to keep their body temperature rise. Thus counting of the turtle's species becomes very easy at particular area during noon time. This method helps a lot to the observer for finding range, population and status of different species.

6. Captured through hooks Poultry intestinal baited hooks were used to capture turtles. Captured turtles were identified, counted and then released back into the same water safely.

B. INDIRECT COUNTING METHODS

1. Information from different sources Information have been collected from turtle’s traders, game watchers, local fishermen, boatmen, field staff of irrigation department and other members of local community. Special identification cards were shown during interviews to identify the terrapin species.

2. Presence of Signs like fecal pellets, tracks den or tunnels (egg laying excretion) Evidences from the impression of finger or foot prints, or tails, presence of fecal pellets, tracks and existence of tunnels (egg laying

74 excretion) are helpful this method a lot, so for finding the existence, range and rough population of the turtles.

The study was based mainly on direct observation; enumerations depended on basking, captured through hooks or nets and floating turtles, and calculated by the following formula

P = AZ 2YX P population A total area Z number observed Y average flushing distance X length of strip

Fig. 3.1. Map of KPK Province showing study sites.

Fig. 3.2. Map of study sites in Peshawar Valley: 1. Jalala Drain 2. Fazalabad Drain 3. Hisara Drain 4. Brach No. 6 of lower Swat River 5. Dub Drain 6. Kashmalo Drain 7. River Jindi 8. River Swat 9. Sardaryab (River Kabul) 10. Naguman (River Kabul) 11. Shaalam (River Kabul) 12. River Budhni 13. Sheikh Canal 14. River Bara 15. Kheshgi (River Kabul) 16. Hakimabad (River Kabul) 17. Kund Park (River Kabul + River Indus) 18. Darwazgai (Indus River).

Fig. 3.3. Map of study sites in D. I. Khan: 1. Purani Kirri 2. Pahar Pur 3. Mianwali Road 4. Indus view Road 5. Bhakkar Road.

Chapter 4

RESULTS RESULTS

Charsadda, Peshawar, Nowshera, Mardan and D. I. Khan were selected as study areas (districts) of KPK for the present study during January 2013 – December 2015. Several most reliable methods and survey techniques were employed for the observation, census and documentation of terrapins during 2013 to 2015. Nilssonia gangeticus (Cuvier, 1825) and Lissemys punctata andersonii (Webb, 1980a) were more common species and found as 28.98% and 25.24% respectively. Both of these species were observed in all the selected districts and all 23 study sites. Nilssonia hurum (Gray, 1831) and Pangshura smithii (Gray, 1863), were less common and found as 14.88% and 10.48%, respectively. P. smithii was observed in all selected five districts and were observed in 20 study sites out of 23. N. hurum was found in four out of five selected districts. This species was not recorded from Mardan District. Chitra indica (Gray, 1831), was found as 8.67% and was in intermediate level, this species was recorded in four districts and in seventeen study sites out of twenty three. This species was not recorded from Mardan District. The status of Pangshura tectum (Gray, 1830) was also in intermediate level and found as 06.38%. This species was recorded in all five selected districts and in sixteen study sites out of twenty three. The status of Hardella thurjii (Gray, 1831), was rare. H. thurjii was recorded from four out of five districts and found as 3.91%. This species was not found in Mardan District. Geoclemys hamiltonii (Gray, 1830) was found as rare and recorded 1.46% from D. I. Khan District only. This

79 species was not observed in any other study site of any other district (Table 4.1; Fig. 4.1).

Following are the results of the population density of each species of freshwater turtles in different study sites of selected districts of KPK:

CHARSADDA DISTRICT

Seven species of terrapins were recorded during the present study in Charsadda, Lissemys punctata and Nilssonia gangeticus were common. Chitra indica, Nilssonia hurum and Pangshura smithii were less common; Pangshura tectum and Hardella thurjii were recorded as rare. These species were recorded in good numbers at Kabul River, Swat River and Jindi River. Geoclemys hamiltonii was not observed in Charsadda District.

According to the present data, N. gangeticus was recorded as 29.76 %, L. punctata as 29.25%, N. hurum as 11.31%, C. indica as 10.01%, P. smithii as 9.87%, P. tectum 6.70% and H. thurjii as 3.10% (Table 4.2; Fig. 4.2).

PESHAWAR DISTRICT

Seven species of terrapins were recorded from Peshawar District, Lissemys punctata and Nilssonia gangeticus were common, Nilssonia hurum, Pangshura smithii and Chitra indica were less common, while Pangshura tectum and Hardella thurjii were found as rare. Geoclemys hamiltonii was not recorded from this district. These

80 species were observed in good numbers at Kabul River especially in Naguman.

According to the present data (2013-2015), L. punctata was recorded as 35.03%, N. gangeticus as 24.07%, N. hurum as 14.87%, P. smithii as 12.52%, C. indica as 09.00%, P. tectum 2.35% and H. thurjii as 2.15% (Table 4.3; Fig. 4.3).

NOWSHERA DISTRICT

Seven species of terrapins were observed in the Nowshera District. Nilssonia gangeticus and Nilssonia hurum were recorded as common, While Lissemys punctata, Pangshura tectum and Pangshura smithii were recorded as less common. They were more populated in Hakimabad site. Hardella thurjii and Chitra indica were found as rare. All these seven species were observed in all four study sites of Kabul River and Indus River. Geoclemys hamiltonii was not observed in Nowshera District.

According to the present data (2013-2015), N. hurum was recorded as 25.39%, N. gangeticus as 22.70%, L. punctata as 17.02%, P. tectum as 13.62%, P. smithii as 12.48%, H. thurjii as 6.10% and C. indica as 02.70% (Table 4.4; Fig. 4.4).

MARDAN DISTRICT

Only four species of terrapins were recorded from Mardan distrct during present study (2013-2015). Lissemys punctata and Nilssonia gangeticus were common, Pangshura smithii was less common, and While Pangshura tectum was recorded as rare. Geoclemys hamiltonii, Chitra indica, Nilssonia hurum and Hardella thurjii were not recorded in current studied sites during 2013-2015.

L. punctata was found abundant among the recorded species and that was 48.66% followed by N. gangeticus (36.90%). P. smithii and P. tectum were recorded as 10.16% and 4.28%, respectively (Table 4.5; Fig. 4.5).

D. I. KHAN DISTRICT

In this district, all the eight species of terrapins were recorded, Nilssonia gangeticus was more common. The status of Nilssonia hurum, Chitra indica and Lissemys punctata were observed as less common, while Pangshura smithii, Geoclemys hamiltonii and Hardella thurjii were in intermediate levels. Pangshura tectum was recorded as rare. L. punctata, N. gangeticus, N. hurum, C. indica and G. hamiltonii were observed in all five study sites of Indus River at D. I. Khan District.

According to present data (2013-2015), all the eight species of freshwater turtles of Pakistan were present in D. I. Khan District of KPK and Geoclemys hamiltonii was only recorded from this district

82 of selected study areas of KPK province. Nilssonia gangeticus was found as 35.31%, Nilssonia hurum, 15.34%; Chitra indica, 14.18%; and Lissemys punctata as 12.01%. While Pangshura smithii, Geoclemys hamiltonii, Hardella thurjii and Pangshura tectum were recorded as 8.25%, 7.38%, 5.64% and 1.88%, respectively (Table 4.6; Fig. 4.6).

DRAINS AND CANALS OF STUDY AREAS

According to present data the status of L. punctata (36.42%) and N. gangeticus (33.77%) were common in small water reservoirs (Drains and canals) of KPK. The status of P. smithii (10.73) was less common in these drains and canals. N. hurum (6.62%), P. tectum (5.83%) and C. indica (5.17%) were in intermediate levels, While H. thurjii (1.46%) was rare (Table 4.7; Fig. 4.11).

RIVERS OF STUDY AREAS

The status of N. gangeticus (27.65%), L. punctata (22.15%), N. hurum (17.16% were common, P. smithii (10.41%), C. indica (9.64%) were less common, P. tectum (6.53%), Hardella thurjii (4.58%) were rare while the status of G. hamiltonii (1.87%) was recorded as very rare in the rivers of selected study areas (Table 4.8; Fig. 4.11).

PESHAWAR VALLEY

In Peshawar valley the status of L. punctata (28.52%) and N. gangeticus (27.41%) were found as common, while P. hurum (14.76%) and P. smithii (11.04%) were found as less common, P. tectum (7.49%) and C. indica (7.31%) were found as in intermediate levels, while the status of H. thurjii (3.48%) was rare. G. hamiltonii was not recorded from valley of Peshawar in present study (Table 4.9; Fig. 4.7 and 4.12).

G. hamiltonii (7.38%) was observed only in the selected study sites from southern part of KPK (D. I. Khan), While N. gangeticus (35.31%) was more common species in this part of the province (Table 4.6; Fig. 4.6 and 4.12).

The total population density of terrapins were recorded more in Charsadda District (39.86%) followed by Nowshera District (20.25%) and D. I. Khan District (19.84%), the population density in Peshawar District (14.68%) was observed in intermediate level, While in Mardan District (5.37%) the density and population status of terrapins were poor (Tables 4.1 and 4.10; Fig. 4.8 and 4.10).

Table 4.1. Status of Population and Distribution of Freshwater Turtles of KPK Province.

S. Location Geographical Coordinate App. Observed Species No. Surv. C. N. N. L. H. P. smithii P. tectum G. Total % area indica ganget hurum punctata thurjii hami (Km) ica ltonii

1 Kashmalo 34.220361 N, 71.748956 E 4 - 29 09 42 09 17 07 - 113 3.25 drain

2 Dub drain 34.160653 N, 71.790753 E 4 21 51 14 67 - 13 - - 166 4.77

3 Hissara 34.281803 N, 71.82955 E 4 18 79 27 48 - 16 08 - 196 5.63 drain

4 Lower Swat 34.245989 N, 71.849339 E 4 - 16 - 09 - 16 21 - 62 1.78 River

5 Khiyali 34.216183 N, 71.668581 E 4 36 57 11 78 09 34 23 - 248 7.12 River

6 Jindi River 34.205394 N, 71.7266 E 4 19 129 58 98 11 15 03 - 333 9.56

7 Sardaryab 34.129483 N, 71.688142 E 4 45 52 38 64 14 26 31 - 270 7.75 River

8 Naguman 34.135110 N, 71.572151 E 4 25 39 22 40 03 31 12 - 172 4.94 River

9 Shaalam 34.099296 N, 71.579704 E 4 18 28 22 56 - 09 - - 133 3.82 River

10 Budhni 34.069724 N, 71.513442 E 4 03 39 17 38 06 - - - 103 2.96 River

11 Sheikh 34.022608 N, 71.539149 E 4 - 11 - 18 02 - - - 31 0.89 Canal

12 Bara River 33.998141 N, 71.691370 E 4 - 06 15 27 - 24 - - 72 2.07

13 Kheshgi 34.042646 N 71.900196 E 4 08 45 51 19 18 27 23 - 191 5.49

14 Hakimabad 34.016727 N, 72.035766 E 4 05 48 47 52 13 26 27 - 218 6.26

15 Kund Park 33.917708 N, 72.229829 E 4 04 39 48 33 04 16 24 - 168 4.08 2

16 Darwazgai 33.824637 N, 72.235751 E 4 02 28 33 16 08 19 22 - 128 3.68

17 Jalala 34.331657 N, 71.900840 E 4 - 32 - 50 - 12 05 - 99 2.84

18 Fazalabad 34.281163 N, 71.874189 E 4 - 37 - 41 - 07 03 - 88 2.53 drain

19 Purani kirri 32.448304 N, 71.330280 E 4 29 47 23 17 14 15 05 19 169 4.85

20 Pahar pur 32.075360 N, 71.094589 E 4 12 27 09 27 03 - - 04 82 2.35

21 Mianwali 31.958920 N, 71.006699 E 4 17 45 21 19 09 08 01 10 130 3.73 Road

22 Indus View 31.820077 N, 70.926104 E 4 19 79 26 05 - 13 - 01 143 4.11 road

23 Bhakar 31.738037 N, 70.927219 E 4 21 46 27 15 13 21 07 17 167 4.80 Road

Total 302 1009 518 879 136 365 222 51 3482

% 8.67 28.98 14.88 25.24 3.91 10.48 6.38 1.46

Fig. 4.1. Status of Population and Distribution of Freshwater Turtles of Khyber Pakhtunkhwa.

Table 4.2. Status of Population and Distribution of Freshwater Turtles in Charsadda District.

S. Location Geographical App. Observed Species No. Coordinate Surv. C. N. N. L. H. P. P. Total % area indica gangetic hurum punctata thurjii smithii tectum (km) a 1 Kashmalo 34.220361 N 4 - 29 09 42 09 17 07 113 8.14 Drain 71.748956 E

2 Dub drain 34.160653 N 4 21 51 14 67 - 13 - 166 11.9 6 71.790753 E

3 Hissara 34.281803 N 4 18 79 27 48 - 16 08 196 14.1 Drain 2 71.829550 E

4 Branch No.6 34.245989 N 4 - 16 - 09 - 16 21 62 4.47 (L. Swat 71.849339 E River)

5 Khiyali 34.216183 N 4 36 57 11 78 09 34 23 248 17.8 (River Swat) 7 71.668581 E

6 Nimouri 34.205394 N 4 19 129 58 98 11 15 03 333 23.9 (River Jindi) 9 71.726600 E

7 Sardaryab 34.129483 N 4 45 52 38 64 14 26 31 270 19.4 (River 5 71.688142 E Kabul)

Total 139 413 157 406 43 137 93 1388

% 10.01 29.76 11.31 29.25 3.10 9.87 6.70

Fig. 4.2. Status of Population and Distribution of Freshwater Turtles in Charsadda District.

Table 4.3. Status of Population and Distribution of Freshwater Turtles in Peshawar District.

S. Location Geographical App. Observed Species No. Coordinate Surv. C. N. N. L. H. P. P. Total % area indica gangetica hurum punctata thurjii smithii tectum (km) 1 Naguman 34.135110 N 4 25 39 22 40 03 31 12 172 33.66 (River Kabul) 71.572151 E

2 Shaalam 34.099296 N 4 18 28 22 56 - 09 - 133 26.03 (River Kabul) 71.579704 E

3 Budhni River 34.069724 N 4 03 39 17 38 06 - - 103 20.16 71.513442 E

4 Sheikh Canal 34.022608 N 4 - 11 - 18 02 - - 31 6.07 71.539149 E

5 Bara river 33.998141 N 4 - 06 15 27 - 24 - 72 14.09 71.691370 E

Total 46 123 76 179 11 64 12 511

% 9.00 24.07 14.87 35.03 2.15 12.52 2.35

Fig. 4.3. Status of Population and Distribution of Freshwater Turtles in Peshawar District.

Table 4.4. Status of Population and Distribution of Freshwater Turtles in Nowshera District.

S. Location Geographical App. Observed Species No. Coordinate Surv. C. N. N. L. H. P. P. Total % area indica gangetica huru punctata thurjii smithii tectum (km) m 1 Kheshgi 34.042646 N 4 08 45 51 19 18 27 23 191 27.09 (River Kabul) 71.900196 E

2 Hakimabad 34.016727 N 4 05 48 47 52 13 26 27 218 30.92 (River Kabul) 72.035766 E

3 Kund Park 33.917708 N 4 04 39 48 33 04 16 24 168 23.83 (River Kabul 72.229829 E +River Indus)

4 Darwazgai 33.824637 N 4 02 28 33 16 08 19 22 128 18.16 (River Indus) 72.235751 E

Total 19 160 179 120 43 88 96 705

% 2.70 22.70 25.39 17.02 6.10 12.48 13.62

Fig. 4.4. Status of Population and Distribution of Freshwater Turtles in Nowshera District.

Table 4.5. Status of Population and Distribution of Freshwater Turtles in Mardan District.

S. Location Geographical App. Observed Species No. Coordinate Surv. area (km) C. N. N. L. H. P. P. Total % indica gangetica hurum punctata thurjii smithii tectum

1 Jalala drain 34.331657 N 4 - 32 - 50 - 12 05 99 52.94 71.900840 E

2 Fazalabad 34.281163 N 4 - 37 - 41 - 07 03 88 47.06 drain 71.874189 E

Total - 69 - 91 - 19 08 187

% - 36.90 - 48.66 - 10.16 4.28

Fig. 4.5. Status of Population and Distribution of Freshwater Turtles in Mardan District.

Table 4.6. Status of Population and Distribution of Freshwater Turtles in D. I. Khan District.

S. Location Geographical App. Observed Species No. Coordinate Surv. C. N. N. L. H. P. P. G. Total % area indica gangetica hurum punctata thurjii smithii tectum hamiltonii (km) 1 Purani kirri 32.448304 N 4 29 47 23 17 14 15 05 19 169 24.46 (Chashma 71.330280 E right bank canal + indus River)

2 Pahar pur 32.075360 N 4 12 27 09 27 03 - - 04 82 11.87 (Indus 71.094589 E river)

3 Mianwali 31.958920 N 4 17 45 21 19 09 08 01 10 130 18.81 Road (Jhok 71.006699 E lal Shah)

4 Indus View 31.820077 N 4 19 79 26 05 - 13 - 01 143 20.69 road 70.926104 E

5 Bhakar 31.738037 N 4 21 46 27 15 13 21 07 17 167 24.17 Road (Kirri 70.927219 E Juma Khan)

Total 98 244 106 83 39 57 13 51 691

% 14.18 35.31 15.34 12.01 5.64 8.25 1.88 7.38

Fig. 4.6. Status of Population and Distribution of Freshwater Turtles in D. I. Khan District.

Table 4.7. Status of Population and Distribution of Freshwater Turtles in Drains and Canals of Khyber Pakhtunkhwa.

S. No. Location Geographical App. Observed Species Coordinate Surv. C. N. N. L. H. P. P. Total % area indica gangetica hurum punctata thurjii smithii tectum (km) 1 Kashmalo 34.220361 N 4 - 29 09 42 09 17 07 113 14.97 Drain 71.748956 E

2 Dub Drain 34.160653 N 4 21 51 14 67 - 13 - 166 21.99 71.790753 E

3 Hissara Drain 34.281803 N 4 18 79 27 48 - 16 08 196 25.96 71.82955 E

4 Branch No.6 34.245989 N 4 - 16 - 09 - 16 21 62 8.21 (L. Swat 71.849339 E River)

5 Sheikh Canal 34.022608 N 4 - 11 - 18 02 - - 31 4.11 71.539149 E

6 Jalala Drain 34.331657 N 4 - 32 - 50 - 12 05 99 13.11 71.900840 E

7 Fazalabad 34.281163 N 4 - 37 - 41 - 07 03 88 11.66 Drain 71.874189 E

Total 39 255 50 275 11 81 44 755

% 5.17 33.77 6.62 36.42 1.46 10.73 5.83

Fig. 4.7. Population status of Freshwater Turtle Species in Peshawar Valley.

Table 4.8. Status of Population and Distribution of Freshwater Turtles in Rivers of Khyber Pakhtunkhwa.

S. Location Geographical Coordinate App. Observed Species No. Surv.area C. N. N. L. H. P. P. G. Total % (km) indica gangetica hurum punctata thurjii smithii tectum hamiltonii

1 Khiyali 34.216183 N, 71.668581 E 4 36 57 11 78 09 34 23 - 248 9.09

2 Nimouri 34.205394 N, 71.7266 E 4 19 129 58 98 11 15 03 - 333 12.21

3 Sardaryab 34.129483 N, 71.688142 E 4 45 52 38 64 14 26 31 - 270 9.90

4 Naguman 34.135110 N, 71.572151 E 4 25 39 22 40 03 31 12 - 172 6.31

5 Shaalam 34.099296 N, 71.579704 E 4 18 28 22 56 - 09 - - 133 4.88

6 Budhni River 34.069724 N, 71.513442 E 4 03 39 17 38 06 - - - 103 3.78

7 Bara river 33.998141 N, 71.691370 E 4 - 06 15 27 - 24 - - 72 2.64

8 Kheshgi 34.042646 N, 71.900196 E 4 08 45 51 19 18 27 23 - 191 7.00

9 Hakimabad 34.016727 N, 72.035766 E 4 05 48 47 52 13 26 27 - 218 7.99

10 Kund Park 33.917708 N, 72.229829 E 4 04 39 48 33 04 16 24 - 168 6.16

11 Darwazgai 33.824637 N, 72.235751 E 4 02 28 33 16 08 19 22 - 128 4.69

12 Purani kirri 32.448304 N, 71.330280 E 4 29 47 23 17 14 15 05 19 169 6.20

13 Pahar pur 32.075360 N, 71.094589 E 4 12 27 09 27 03 - - 04 82 3.00

14 Jhok Lal Shah 31.958920 N, 71.006699 E 4 17 45 21 19 09 08 01 10 130 4.77

15 Indus View road 31.820077 N, 70.926104 E 4 19 79 26 05 - 13 - 01 143 5.24

16 Kirri Juma Khan 31.738037 N. 70.927219 E 4 21 46 27 15 13 21 07 17 167 6.12

Total 263 754 468 604 125 284 178 51 2727

% 9.64 27.65 17.16 22.15 4.58 10.41 6.53 1.87

Fig. 4.8. Status of Population of Freshwater Turtles in selected Districts of KPK.

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Table 4.9. Status of Population and Distribution of Freshwater Turtles of Peshawar Valley.

S. Location Geographical App. Surv. Observed Species No. Coordinate area C. N. N. L. H. P. P. tectum Total % (km) indica gangetica hurum punctata thurjii smithii

1 Kashmalo Drain 34.220361 N 4 - 29 09 42 09 17 07 113 4.05

71.748956 E

2 Dub Drain 34.160653 N 4 21 51 14 67 - 13 - 166 5.95

71.790753 E

3 Hissara Drain 34.281803 N 4 18 79 27 48 - 16 08 196 7.02

71.82955 E

4 Branch No.6 34.245989 N 4 - 16 - 09 - 16 21 62 2.22

(L. Swat River) 71.849339 E

5 Khiyali (River Swat) 34.216183 N 4 36 57 11 78 09 34 23 248 8.89

71.668581 E

6 Nimouri (River Jindi) 34.205394 N 4 19 129 58 98 11 15 03 333 11.9 3 71.7266 E

7 Sardaryab (River 34.129483 N 4 45 52 38 64 14 26 31 270 9.67 Kabul) 71.688142 E

8 Naguman (River 34.135110 N 4 25 39 22 40 03 31 12 172 6.16 Kabul) 71.572151 E

9 Shaalam (River 34.099296 N 4 18 28 22 56 - 09 - 133 4.77 Kabul) 71.579704 E

10 Budhni River 34.069724 N 4 03 39 17 38 06 - - 103 3.69

71.513442 E

11 Sheikh Canal 34.022608 N 4 - 11 - 18 02 - - 31 1.11

71.539149 E

12 Bara River 33.998141 N 4 - 06 15 27 - 24 - 72 2.58

71.691370 E

13 Kheshgi (River 34.042646 N 4 08 45 51 19 18 27 23 191 6.84 Kabul) 71.900196 E

14 Hakimabad (River 34.016727 N 4 05 48 47 52 13 26 27 218 7.18 Kabul) 72.035766 E

15 Kund Park( River 33.917708 N 4 04 39 48 33 04 16 24 168 6.02 Kabul +Indus river) 72.229829 E

16 Darwazgai (River 33.824637 N 4 02 28 33 16 08 19 22 128 4.59 Indus) 72.235751 E

17 Jalala Drain 34.331657 N 4 - 32 - 50 - 12 05 99 3.55

71.900840 E

18 Fazalabad Drain 34.281163 N 4 - 37 - 41 - 07 03 88 3.15

71.874189 E

Total 204 765 412 796 97 308 209 2791

% 7.31 27.41 14.76 28.52 3.48 11.04 7.49

101

Charsadda

Peshawar

Nowshera

Mardan

Dera Ismail Khan

Fig. 4.9. Status of Total Population Density of Freshwater Turtles in Selected Districts of KPK.

102

Table 4.10. Status of Population and Distribution of Freshwater Turtles in selected districts of KPK.

S. District Division Observed Species No. C. indica N. gangetica N. hurum L. punctata H. thurjii P. smithii P. tectum G. hamiltonii Total %

1 Charsadda Peshawar 139 413 157 406 43 137 93 - 1388 39.86

2 Peshawar Peshawar 46 123 76 179 11 64 12 - 511 14.68

3 Nowshera Peshawar 19 160 179 120 43 88 96 - 705 20.25

4 Mardan Mardan - 69 - 91 - 19 08 - 187 5.37

5 Dera Ismail D. I. Khan 98 244 106 83 39 57 13 51 691 19.84 Khan

Total 3482 302 1009 518 879 136 365 222 51

% 8.67 28.98 14.88 25.24 3.91 10.48 6.38 1.46

103

0 C. indica N. gangetica N. hurum L. punctata H. thurjii P. smithii P. tectum G. hamiltonii

Fig. 4.10. Status of Population Density of different Species of Freshwater Turtles in Selected Districts of KPK.

104

0 G. hamiltonii C. indica N. gangetica N. hurum L. punctata H. thurjii P. smithii P. tectum

Drains/Canals Rivers

Fig. 4.11. Comparison of Turtle Population in Drains/Canals with Rivers of KPK.

105

0 C. indica N. gangetica N. hurum L. punctata H. thurjii P. smithii P. tectum G. hamiltonii

Peshawar Valley Dera Ismail Kkhan

Fig. 4.12. Comparison of Population of Freshwater Turtles of Peshawar Valley with Southern district (D. I. Khan).

106

BIOLOGY AND DISTRIBUTION OF FRESHWATER TURTLES SPECIES OF KHYBER PAKHTUNKHWA

Lissemys punctata andersonii (Indian Flap-Shell Turtle)

Phylum: Chordata Class: Reptilia Order: Testudines Family: Trionychidae Genus: Lissemys Species: Lissemys punctata Subspecies: Lissemys punctata andersonii

Common Name(s): English: Indian Flap-shell turtle, Indus Flap-shelled turtle, spotted flap-shell turtle, and Indus mud turtle.

Synonym(s): Emyda granosa Schoepff, 1801 Testudo granulosa Suckow, 1798 Testudo punctata Lacépède 1788 Testudo punctata Bonnaterre 1789 Testudo sonnerati Meyer 1790 Testudo granulata Daudin 1801

107

Trionyx coromandelicus Geoffroy Saint-Hilaire 1809 Emyda dura Anderson 1876.

Distribution This species is generally found in Bangladesh, India, Myanmar, Nepal, and Pakistan. In Pakistan, It is found in Indus River, and its tributaries (Streams, Drains, Canals and Rivers), lakes and ponds (Fig. 4.13).

Subspecies: – Currently three subspecies are recognized: 1) Lissemys punctata punctata (Southern Indian Flap-shell Turtle) (Distribution: Southern Peninsular India (Kerala, Tamil Nadu). 2) Lissemys punctata andersoni Webb 1980, (Distribution: Bangladesh, Northern India, Myanmar, Nepal and Pakistan). 3) Lissemys punctata vittata (synonymy: Emyda vittata Peters 1854) (Distribution: Central India).

Diagnosis Carapace depressed and oval, narrowly edged with pale yellow, creamy flaps of plastron present. Head and limbs gray, with light yellow spots on head and neck, older juveniles and young adult with more vivid yellow spots on carapace. Head pattern usually showing pair of curved light marks on crown and light post ocular stripe. Plastron cream to Ivory, with gray patches over callosities. Large adult dark olive brown. Maximum Carapace length is 350mm (Fig. 4.14).

108

Habitat They are adaptable and durable, occurring in a variety of aquatic habitats, ranging from streams and rivers to reservoirs, marshes, ponds, lakes, canals and even in paddy fields. They are often found in situations that are dry for several months of each year, they occur in the big canals but are not plentiful there (Bhupathy et al., 2014).

Habits Frequently seen basking on logs and stones. It can survive period of drought by aestivating for a long time on land.

Feeding It is omnivorous.

Breeding season Nesting generally occurs in July-November. Clutch size varies from 4–16 eggs, which generally have a prolonged incubation period of about 300 days (Bhupathy et al., 2014).

Threats Trading for meat and pet.

Status Common.

Protection/ Conservation status This species is mentioned in Appendix II of CITES, while the status is in Lower risk in the “IUCN Red list threatened species”.

109

Fig. 4.13. Distribution of Lissemys punctata andersonii.

110

Fig. 4.14. Lissemys punctata andersonii (A) Dorsal view (B) Ventral view.

111

Nilssonia gangeticus (Indian Soft-Shell Turtle)

Phylum: Chordata Class: Reptilia Order: Testudines Family: Trionychidae Genus: Nilssonia Species: Nilssonia gangeticus (Cuvier, 1825).

Comman Names(s): English:- Indian soft-shell turtle, Ganges soft-shell turtle. Synonym(s): Aspideretes gangeticus (Cuvier, 1825) Trionyx gangeticus (Cuvier, 1825) Nilssonia gangetica (Cuvier, 1825) Aspideretes gangeticus (Ernst, 1989) Aspilus gataghol (Gray, 1872) Isola gangeticus (Baur, 1893) Nilssonia gangetica (Praschag, 2007)

Distribution This species is found in India, Bangladesh, Nepal and Pakistan. It is found throughout Indus flood plains and associated canals and marshes of Pakistan (Fig. 4.15).

112

Diagnosis Carapace depressed and oval. A slightly down turned snout on a large head, head green above with black, oblique stripes on the forehead and sides, which may be broken and in old specimens, entirely lost Color dull olive /grayish with black reticulations/yellow spots. 4-6 eye like markings on the back of young (Fig. 4.16).

Habitat Rivers, canals, ponds, and marshes, nearly in all aquatic situations, but generally in more permanent water than that inhabited by Lissemys punctata.

Habits These huge turtles inhabit rivers and large canals, particularly where the water is turbid with some current and a mud bottom.

Feeding Omnivorous, feeding mainly on aquatic vertebrates (Tikader and Sharma, 1985), sometimes eat spoiled eggs of own species and carrion (Das, 1985).

Breeding season Late April, also during monsoon rains (July - October).

Threats Meat trade, local and regional, egg collection, it is eaten in East India.

Status

113

Common.

Protection/Conservation status

This species is included in Appendix I of CITES, while the status is Vulnerable in the “IUCN Red list threatened species”.

114

Fig. 4.15. Distribution of Nilssonia gangeticus.

115

Fig. 4.16. Nilssonia gangeticus (A) Dorsal view (B) Ventral view

116

Nilssonia hurum (Indian Peacock Soft-Shell Turtle)

Phylum: Chordata Class: Reptilia Order: Testudines Family: Trionychidae Genus: Nilssonia Species: Nilssonia hurum (Gray, 1831)

Synonymy(s): Trionyx occellatus Gray 1830a, Trionyx ocellatus, Gymnopus ocellatus, Trionyx hurum Gray 1830b, Gymnopus duvaucelii Duméril and Bibron 1835, Trionyx sewaare Gray 1872, Trionyx bellii Gray 1872, Trionyx buchanani Theobald 1874, Isola hurum, Aspideretes hurum, Tyrse hurum, Amyda hurum.

Distribution Bangladesh, India and Pakistan Distribution. In Pakistan it occurs along Indus valley below Hyderabad (Fig. 4.17).

Diagnosis Carapace depressed, oval and coarsely pitted, head large with longish snout strongly down turned. Color olive green above, with black reticulations and narrow yellow spots, most prominent, behind the eyes. Eye like markings on the shell .Head and shell marking tend to

117 become indistinct with age may even disappear. Carapace length is up to 60 cm (Fig. 4.18).

Habits This is a relatively abundant large riverine species that is found in rivers and reservoirs Nocturnal, Aggressive, highly aquatic and a good burrower in bottom sediments (Das et al., 2010).

Feeding The species is omnivorous Das et al., 2010).

Breeding Season Nesting season is August – November and clutch size is 20-30.

Threats Meat trade.

Status Uncommon.

Protection I Conservation Status This species is included in Appendix I of CITES, while the status is Vulnerable in the “IUCN Red list threatened species”.

118

Fig. 4.17. Distribution of Nilssonia hurum.

119

Fig. 4.18. Nilssonia hurum (A) Adult (B) Juvenile.

120

Chitra indica (Narrow Headed Soft Shell Turtle)

Phylum: Chordata Class: Reptilia Order: Testudines Family: Trionychidae Genus: Chitra Species: Chitra indica (Gray, 1830)

Synonym(s): Trionyx indicus Gray, 1830. Gymnopus lineatus, Dumeril and Bibron, 1835.

Distribution Occurs in Indus flood plains to western Malaysia, India, Nepal and Bangladesh (Fig. 4.19).

Diagnosis Shell widely oval and flattened. Head small and elongated, snout rounded, neck indistinct from head, Oval “V” Shaped mark is present on the neck. Eyes situated close to nostrils. Color dull olive or grey above with a complicated pattern of wavy reticulations. Young ones have 4 indistinct eyelike marking and reticulations. Undersurface is white (Das and Singh, 2009) (Fig. 4.20).

121

Habitat A riverine species, found from upper reaches to delta of larger streams, especially in shallow section. In Pakistan, it also occurs in vast Indus canal system. Prefers streams with sandy-bottom (Tikader and Sharma, 1985). Spend most of the day submerged in the sandy bottoms of deep rivers. Females lay eggs on sandy banks.

Habit Very pugnacious, biting savagely and without warning.

Feeding Omnivores and feed on aquatic vegetation and fish, mollusks, and animals (Smith, 1931).

Breeding Seasons Lay from 60 to 110 eggs.

Threats Exploitation for meat in trade, local consumption of eggs, reported it is eaten in India, not in Pakistan.

Status Uncommon

Protection /Conservation status This species is included in CITES Appendix II, while the status is Endangered in the “IUCN Red list threatened species”.

122

Fig. 4.19. Distribution of Chitra indica.

123

Fig. 4.20. Chitra indica (A) Adult (B) Juvenile.

124

Pangshura tectum (Indian Roofed Turtle)

Phylum: Chordata Class: Reptilia Order: Testudines Family: Geoemydidae Genus: Pangshura Species: Pangshura tectum (Gray, 1831)

Synonym(s): Emys tectum (Gray, 1830) Kachuga tecta (Gray, 1830) Pangshura tecta (Gray, 1830) Batagur tecta (Le et al., 2007)

Distribution This species is found in the tributaries of Indus and Ganges Rivers, Nepal and Bangladesh (Fig. 4.21).

Diagnosis Carapace rich dark brown, in some cases narrowly edged with deep yellow or orange, vertical keel reddish, plastron yellow to orange, Neck distinctly striped. Red or orange crescent marking near eye. Head blackish, with broad bands of dull orange to red extending from behind eye to occipital. Limbs dark gray edged and spotted with yellow (Fig. 4.22).

125

Habitat Mainly lentic situations, preferring vegetation-chocked shallow streams and ditches both flowing and stagnant water (Khan, 1982).

Habits Small rivers and sometime large rivers. Not a strong swimmer.

Feeding It feed almost wholly upon vegetable material, preferring cucumber and melon (Smith, 1931) reported it as herbivorous.

Threats Pet trade to a limited extent. Seldom exploited for meat.

Breeding season Annual breeder.

Status Common in Pakistan.

Protection I Conservation status This species is included in CITES Appendix I, while the status is in Lower risk in the “IUCN Red list threatened species”.

126

Fig. 4.21. Distribution of Pangshura tectum.

127

Fig. 4.22. Pangshura tectum (A) Dorsal view (B) Ventral view.

128

Pangshura smithii (Indian Brown Roofed Turtle)

Phylum: Chordata Class: Reptilia Order: Testudines Family: Geoemydidae Genus: Pangshura Species: Pangshura smithii (Gray, 1863)

Synonym(s): Batagur smithii Gray, 1863 Kachuga smithii (Gray, 1863)

Distribution This species is found along the tributaries of and Indus-Ganges Rivers and Bangladesh. In Pakistan, along the streams connected to River Indus and associated wetlands (Fig. 4.23).

Diagnosis Carapace depressed and slightly keeled. Carapace olive brown to horn color, central ridge dark brown to black, with touches of russet in young. Head light olive to pale grayish yellow, darker on top with a brownish spot behind eye. Snout pointed and jaws serrated. Neck with faint cream stripe, limbs pale gray, margins of webs dull yellow. Carapace width 67 to 76 % of its length, strongly arched, highest 36.5 to 42.5 % or carapace length (Fig. 4.24).

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Habitat It found in lakes and ponds communicating with the river. It frequents muddy water with some current where there are logs, old bridge abutment, and other protruding objects. The turtle are quiescent from early December to early March (Minton, 1966) but some bask during the warmest hours. They are shy turtle and do not attempt to bite.

Habitat River currents and lentic situations, including backwaters (Moll, 1987).

Habits This turtle is common in river channels and in the larger channels and is occasionally they are omnivorous but prefer flesh (Minton, 1966; Das, 1985). They also eat meat, fish, frogs and fruits of several kinds.

Breeding Season Females found with eggs in early October (Minton, 1966). Eggs have smooth, firm shells. Nests constructed mainly on river banks.

Threats They are significantly reduced in India due to exploitation for food as well as habitat destruction (Tikader and Sharma, 1985) rarely eaten in Pakistan.

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Status Common.

Protection/ Conservation status This species is Included CITES Appendix I, while IUCN recorded it as at Lower risk.

131

Fig. 4.23. Distribution of Pangshura smithii.

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Fig. 4.23. Pangshura smithii (A) Dorsal view (B) Ventral view.

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Hardella thurjii (Crowned River Turtle)

Phylum: Chordata Class: Reptilia Order: Testudines Family: Geoemydidae Genus: Hardella Species: Hardella thurjii (Gray, 1831)

Synonymy: Emys thurjii Gray, 1831 Emys flavonigra Lesson, 1831 Clemmys thurgii Fitzinger, 1835 Kachuga oldhami Gray, 1869 Hardella indi Gray, 1870

Distribution This species is found in lndo-Gangetic plain, Bangladesh and Nepal. In Pakistan, This species is confined to Indus River and its tributaries (Fig. 4.25).

Diagnosis Carapace is large up to 65 cm. Shell thick and heavy in adults, moderately depressed, four yellow-orange stripes on each side of the head. Carapace dark brown or dark grey with grey-black veritable keel. Carapace flaky flat with interrupted dark grey with grey-black

134 veritable keel. Carapace flaky flat with interrupted vertebral keel. Plastron cream, glowing yellow band like diadem around head. Occasionally short yellow to amber stripe on crown. Limbs dark gray, narrowly edged with pale yellow posterior (Das and Bhupathy, 2009) (Fig. 4.26).

Habitat Slow flowing to lentic water, most common in shallow weed-choked pond and canals; rarely emerges for basking (Tikader and Sharma, 1985).

Habits Several specimens were observed or collected in shallow, vegetation- chocked wetlands. Others were recorded from deep quite inlets of the Indus or from canals. These turtle are highly aquatic but sluggish, spending more time resting on the bottom. The disposition of the species is quite and gentle.

Feeding They feed or eat fruit and vegetable (Tikader and Sharma, 1985) of many kinds but rarely showed interest in animal food, although one small turtle ate part of a frog.

Breeding season Courtship occurs from April to July; eggs are laid from September to January (Khan, 2006).

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Threats Threatened by over-exploitation of adults and eggs as food and by habitat destruction. Flesh has good flavor, thus large numbers are eaten in India (Tikader and Sharma, 1985).

Status Less Common.

Protection /Conservation status This species is included in CITES Appendix II, while IUCN reported it as Vulnerable.

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Fig. 4.25. Distribution of Hardella thurjii.

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Fig. 4.26. Hardella thurjii (A) Dorsal view (B) Ventral view.

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Geoclemys hamiltonii (Spotted Pond Turtle)

Phylum: Chordata Class: Reptilia Order: Testudines Family: Geoemydidae Genus: Geoclemys Species: Geoclemys hamiltonii (Gray, 1830)

Synonym(s): Emys guttata Gray, 1831 Emys picquotii Lesson, 1831 Melanochelys pictus Murray, 1884 Clemmys palaeindica Lydekker, 1885 Geoclemys sivalensis Tewari & Badam, 1969.

Distribution This species is restricted to Indo-Gangetic plain and Bangladesh. In Pakistan, this species is widely distributed (Fig. 4.27).

Diagnosis Head black with yellow spots and numerous white spot present on the grey neck and limbs .Carapace elongated with three keels. Carapace black more or less wedge--shaped. Yellow marks more prominent on centrals and marginally and more numerous and vivid in young

139 largest. Adults may be almost uniformly blackish (Azam and Nazar, 2009) (Fig. 4.28).

Habitat Strictly aquatic, preferring shallow, clear water, usually chocked with aquatic vegetation (Tikader and Sharma, 1985) in pond, marshes, and rivers. Apparently most common in upper deltaic regions of rivers (Indus and Ganges). They are found in large and small lakes and sloughs in quite shallow, rather cleat water with considerable aquatic vegetation (Das and Bhupathy, 2010).

Habits Relatively slow swimmer.

Feeding Carnivorous species they feed readily on fishes (Tikader and Sharma, 1985) insects and snails (Minton, 1966) but refused vegetable food.

Breeding season Courtship in February-March (Minton, 1966).

Threats Local consumption and trade; eggs and meat heavily used for home consumption, primarily in eastern India (Tikader and Sharma, 1985).

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Status Rare

Protection / Conservation status This species is mentioned in CITES Appendix I, while IUCN reported it as Vulnerable.

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Fig. 4.27. Distribution of Geoclemys hamiltonii.

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Fig. 4.28. Geoclemys hamiltonii (A) Adult (B) Juvenile.

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Chapter 5

DISCUSSIONS

Habitat destruction and alteration associated with rise in human population and several other anthropogenic activities are major factors influencing the terrapin’s population in KPK. According to data, during the 2013-2015 the abundance of population of some freshwater turtle species has declined due to hunting, habitat destruction, fragmentation, agricultural and several other anthropogenic actions.

Pakistan is indeed very fertile in its reptile biodiversity. The varied and interesting composition of the herpeto-fauna of Pakistan is rich due to the peculiar zoogeographical position of Pakistan which lies at the transitional zone among three zoo-geographical regions i.e. Palearctic, Ethiopian and Oriental regions among world’s six regions. The protection of reptiles has been receiving of attention in recent years. But for the better of survival they need strict legal protection and restoration of natural reservoir in which they live.

Distribution and population status of terrapins were conducted in Peshawar, Charsadda, Nowshera, Mardan and D. I. Khan districts of KPK Province during January 2013 – December 2015. Eight species i.e. Lissemys punctata andersonii (Webb, 1980a), Pangshura smithii (Gray, 1863), Pangshura tectum (Gray, 1863), Chitra indica (Gray, 1831), Nilssonia gangeticus (Cuvier, 1825), Nilssonia hurum (Gray, 1831), Hardella thurjii (Gray, 1831), and Geoclemys hamiltonii (Gray, 1831) were observed.

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In this study, seven species of terrapins were recorded in the Charsadda District. Two of the six species viz. Lissemys punctata and Nilssonia gangeticus were observed to be common, while Chitra indica, Nilssonia hurum, Pangshura smithii and Pangshura tectum were less common. Hardella thurjii was rare. These species were observed in good numbers at Swat River, Jindi River and Kabul River.

During the three years study, (Jan. 2013 – Dec. 2015) the occurrence of N. gangeticus as 29.76%, L. punctata as 29.25%, N. hurum as 11.31%, C. indica as 10.01%, P. smithii as 9.87%, P. tectum as 6.70% and H. thurjii as 3.10% were recorded from Charsadda District.

In Peshawar District, Seven species were observed, Lissemys punctata and Nilssonia gangeticus were recorded as common, Nilssonia hurum, Pangshura smithii and Chitra indica as less common, while Hardella thurjii and Pangshura tectum were rare.

During present study (2013-2015), L. punctata was recorded as 35.03%, N. gangeticus as 24.07%, N. hurum as 14.87%, P. smithii as 12.52%, C. indica as 9.00%, P. tectum as 2.35% and H. thurjii as 2.15%.

Seven species were observed in the Nowshera District. Nilssonia hurum, Nilssonia gangeticus and Lissemys punctata were found as

145 common, Pangshura smithii and Pangshura tectum as less common while Chitra indica was in rare status.

During present study (2013-2015), N. hurum was recorded as 25.39%, N. gangeticus as 22.70%, L punctata as 17.02%, P. tectum as 13.62%, P. smithii as 12.48%, H. thurjii as 6.10% and C. indica as 2.10%.

In the District of Mardan , four species were found , Lissemys punctata and Nilssonia gangeticus were recorded as common, Pangshura smithii as less common while Pangshura tectum was recorded as rare.

During present study (2013-2015), L. punctata was observed as 48.66%, N. gangeticus as 36.90%, P. smithii as 10.16% and P. tectum as 4.28%.

In the District of D. I. Khan, all the eight species occurring in Pakistan were recorded. Nilssonia gangeticus was recorded as common, Nilssonia hurum, Lissemys punctata and Chitra indica were as less common, Pangshura smithii, Geoclemys hamiltonii and Hardella thurjii in intermediate level, while Pangshura tectum was in rare status.

During present study (2013-2015), Nilssonia gangeticus was observed as 35.31%, Nilssonia hurum as 15.34%, Chitra indica as 14.18%, Lissemys punctata as 12.01%, Pangshura smithii as 8.25%,

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Geoclemys hamiltonii as 7.38%, Hardella thurjii as 5.64% and Pangshura tectum as 1.88%.

Habitat destruction and alteration associated with increase in human’s population, poaching and many other anthropogenic activities are major causes for depletion of terrapins in Asia and especially in Sub continent. Asia is quiet rich in habitats and biodiversity of terrapins. Asia's dense turtle diversity occurs in four hotspot i.e. the Indo-Gangetic Plain, Southeast Asia, South Chinese coastal region and New Guinea. Globally terrapins and tortoises are the most threatened group of vertebrates. The Species Survival Commission (SSC) of IUCN has already found 122 to be threatened. Analysis by IUCN, and partners suggests that about 40-60% terrapins and tortoise are in imminent danger of extinction. Despite this dire situation, few organizations have made concerted efforts to conserve terrapins and tortoises.

Turtles are the most heavily exploited for human’s consumption. High unsustainable levels of exploitation for consumption is directly responsible for decline in conservation of many turtles (Klemens and Thobjamarson, 1995). During the current study, the local peoples have continuously captured turtles of all sizes for consumption and for sale in international or local markets. International consumers are predominantly from East Asia. Trading of terrapins and tortoises in Asia is occurring in such a large scale that it has threatened the survival of several terrapin’s species.

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Terrapins play important parts in aquatic ecosystems including seed dispersal, vegetation management, control of insects and snails and keeping water clean and hygienic by preying upon sick and weak animals and also scavenging dead animals (Gibbons et al., 2000). Turtles also plays a vital role in trophic chain and act as ecological indicators (Luiselli and Akani, 2003).

Suwelo (2001) worked on the tortoises and terrapins of Southeast Asian countries. He investigated that large number of turtles have been harvested from these countries for many purposes like for human’s consumption, medicines, for pet trade and also for religious purpose like to release in Buddhist sites in temples. During last two decades the terrapin’s trade has increased and changed drastically to critical point.

Azam et al. (2003) conducted a survey on population status and distribution of terrapins in the River i.e. Sukkur Barrage, Guddu Barrage, Jamaldin Wall and pond areas near to Kandhkol. Six species i.e. Nilssonia gangeticus, Pangshura smithii, Pangshura tectum, Hardella thurjii, Chitra Indica and Lissemys punctata were observed. In this survey, Pangshura smithii and Chitra indica were observed as abundant in different parts of the study area.

Azam et al. (2005) conducted a survey on terrapins of the River Indus and recorded six species including Pangshura tectum, Pangshura smithii, Hardella thurjii, Chitra indica, Nilssonia gangeticus and Lissemys punctata.

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Kitimasak et al. (2005) worked on the status of population and distribution of the narrow headed soft-shell turtle Chitra chitra in Thailand and reported that due to vanishing of habitat the status of Chitra chitra is rare and the natural population is in declining condition. During present study, the developmental activities, such as road and building construction which require a large amount of sand from nesting habitat is another threat to terrapin’s population.

Akbar et al. (2006) studied the population status and distribution of terrapins in Punjab. They collected 3528 individuals of terrapins of two families’ viz., Geoemyedidae (Pangshura smithii, Pangshura tectum, Geoclemys hamiltonii, Hardella thurjii) and Trionychidae (Nilssonia gangeticus, Nilssonia hurum, Chitra indica and Lissemys punctata) were identified. Pangshura smithii and Pangshura tectum had abundant status of population whereas, Hardella thurjii and Chitra indica were observed as rare. During present study Lissemys punctata and Nilssonia gangeticus were abundant which show dissimilarity with Akbar et al. (2006) report in Punjab.

Noureen (2007) conducted a survey to estimate the status of terrapin’s population in D. I. Khan. She reported poaching activities about the “Kail” tribe which is living on the banks of Indus River for years. They have been poaching terrapins for eating purposes but now a days they have started selling these to earn money. She visited 13 different communities in D. I. Khan along the Indus River bank. These communities are involved in poaching of two species of soft- shell turtles i.e. Ganges soft-shell turtles and Peacock soft-shell turtles, while the hard-shell turtles are not more important for them.

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Both these Nilssonia species are endangered. They cut the Plastron from these turtles as this part is commercially more important for them. Big dealers from Punjab visit the area at regular interval to collect the dried body parts of these turtles. Plastron and the chest pellicle cost of Rs 50-250. Kails move in groups to capture turtles and cover the area of at least 4 km upstream and downstream. According to “Kail” community, all the 8 native species of terrapins of Pakistan are found in D. I. Khan District. Ganges soft-shell turtles, Brown roofed turtles, Indian roofed turtles, and Indian flap-shell turtles are in abundance in D. I. Khan District. The data of present study shows the same result of occurrence these species.

Fatima (2008) recorded eight species in four districts of Sindh Province. She reported four Species from Badin District and six Species from each of Sukkur, Thatta and Sanghar districts of Sindh. In the present study, eight species of terrapins were recorded from KPK Province, in which seven species from Peshawar Valley and eight species from D. I. Khan Distrct (South district). L. punctata and N. gangeticus were found to be more common which shows similar result as Fatima, 2008.

Azam and Nazar (2009) recorded six species of terrapins from four riverine wetlands in Punjab during a survey, these include Chashma Barrage, Taunsa Barrage, Ghazi Ghat and Head Punjnad. These recorded species were Chitra indica, Nilssonia gangeticus, Nilssonia hurum, Pangshura smithii, Geoclemys hamiltonii and Lissemys punctata. P. smithii was found most abundant species of the recorded specimens. Other species were C. indica, N.

150 gangeticus, N. hurum, G. hamiltonii and L. punctata. P. smithii, N. gangeticus, G. hamiltonii were found at all the four surveyed sites. C. indica was recorded at three sites including Taunsa Barrage, Ghazi Ghat and Head Punjnad and N. hurum was found in only one site Head Punjnad. P. smithii, was most abundant species of the counted turtles, while G. hamiltonii, N. gangeticus, L. punctata, C. indica and N. hurum were less common. Four species of terrapins were recorded from Chashma Barrage Viz., P. smithii, N. gangeticus, G. hamiltonii, and L. punctata, as this site is located on Mianwali to D. I. Khan road. Which is very close to one of the present study site (Purani Kirri) from Chashma Right bank Canal. As in present study G. hamiltonii was only recorded from all the five selected study sites including Chashma right bank canal of D. I. Khan District. Both these works show the presence of G. hamiltonii in this area.

Azam and Saeed (2011) conducted surveys at Taunsa Barrage, Guddu Barrage and Punjnad Head work to study the abundance, distribution and threats to the terrapin’s population at these areas. Five species of terrapin’s viz., Pangshura smithii, Lissemys punctata, Nilssonia gangeticus, Chitra indica and Geoclemys hamiltonii were observed from the study sites. P. smithii was recorded from all the study sites while C. indica, G. hamiltonii and N. gangeticus were recorded only at Taunsa Barrage. L. punctata was recorded both from Punjnad Head work and Taunsa Barrage. Illegal trade of terrapins from local communities was a major threat at studied sites. Use of pesticide to capture fishes was another threat faced by turtles and other aquatic fauna as it results

151 in mass of brutal mortality of terrapins and other fauna. In the present study, seven species of terrapins were observed in Peshawar Valley viz., Peshawar, Charsadda, Nowshera and Mardan districts. Only four species viz., L. punctata and N. gangetica, P. smithii and P. tectum were observed from Mardan District. While in southern district (D. I. Khan) of KPK all the eight native species of Pakistan were observed.

Mahmood et al. (2012) conducted the study in the Korang River of Islamabad and reported that Indian flap Soft-shell turtle was the most abundant species contributing up to 56% of the total turtles. Indian Soft-shell turtle was 30%. The present study showing the same result and confirmed earlier studied results.

Kayani et al. (2015) studied the morphology of terrapins found in Rawalpindi and Islamabad area. They studied twenty specimens from three different species i.e. Lissemys punctata, Nilssonia gangeticus and Pangshura smithii. They collected these turtles from thirteen different transects in study areas.

Khan (2015) pointed out some threats of terrapins. Habitat lost is one of major threats to terrapins in Pakistan according to him. During the summer rainy season (July-September), sited rivers over flow, converting the Indus valley in to a huge boundless lake. Flood water carry turtles far in the valley, in which mostly missing their way back. Their hard bony shell protect them from scratches and bumps sustained while crawling long distances on hard stony soils. But some of them crushed under vehicles and trains. Some of them fall into the

152 hands of uncaring peoples, who may pelt them with stones just for fun. Other lingering threats are turtle eating tribes and some carnivore animals like Jackals, foxes, Dogs, cats, monitors, snakes, cow, Kites and Mongoose. Often nests soaked by flood water and killing the embryos.

Lissemys punctata was the most common species during the present study, probably because it likes shallow waters of rivers, marshes, and often extend in sewage system of metropolitan cities. Minton (1966) also reported the same behavior of the Indian flap-shell turtle. Taking all together, our data indicate collectively that Lissemys punctata has a healthy population and found in all sites of KPK. The second abundant species was Nilssonia gangeticus which has good population in the surveyed sites.

Khan et al. (2015) conducted a study in four districts of Sindh and recorded all the eight species. They reported four Species from Badin district and six species from each of Sukkur, Thatta and Sanghar districts of Sindh. They also recorded all the eight species of Pakistan from the district of D. I. Khan of KPK. In another study, Noureen (2007) also reported all the eight of terrapin’s species in D. I. Khan Distrcit. During the present study all the eight species were recorded from D. I. Khan District while, seven species were observed in the Valley of Peshawar. Geoclemys hamiltonii was not observed in Peshawar Valley. Same result was recorded by Safi and Khan (2014) and Khan et al. (2015; 2016).

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Rais et al. (2015) recorded 33 species of Amphibo-reptiles belonging to 15 families from six different units of Chakwal Tehsil, Punjab Province of Pakistan. The species richness evidences revealed that the recorded number of species was slightly lower than the estimated number of species viz., 35 and 36 predicted by Abundance-based Coverage Estimator (ACE) and Chao 1, respectively. The more individuals (6,586; accounting for 50 % of the total individuals) were recorded from the protected mixed habitat (Wildlife sanctuary) followed by 2,486 (18%) from wetlands inside protected area while the lowest number (154) was recorded from unprotected scrublands and tropical thorn forests.

Sarwar et al. (2015) studied habitat analysis for terrapins of Indus River and some streams in KPK and Punjab provinces. They recorded eighty two individuals belong to seven different species of terrapins in sixteen different study sites in River Indus and some of its tributaries in KPK and Punjab. These species were, Pangshura smithii, Pangshura tectum, Geoclemys hamiltonii, Nilssonia gangeticus, Nilssonia hurrum, Chitra indica and Lissemys punctata. The L. punctata was the common, with relative frequency (RF) of 24.4%, followed by N. gangeticus (18.3%), N. hurum (17.1%), C. indica (17.1%), P. smithii (12.2%), P. tectum (7.3%), and G. hamiltonii (3.7%). It was observed that Swabi has more turtle’s population and its three study sites were; Badri Nallah, Yar Hussian Stream and Allah Dher Stream. The current research has the same result for the status and abundance of turtle’s population in the study areas.

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Pakistan joined CITES in 1976. Government follows all the rules and regulations as directed by CITES. National council for conservation of wildlife (NCCW) coordinates with all the provincial wildlife departments and these wildlife departments implement wildlife rules and regulations according to their act and policies and also follow upon the Appendices (Appendix I, II and III) of CITES. The Government of KPK added the terrapins on 22nd August 2007 by official notification in Wildlife (Protection, Preservation, Conservation and Management) Act, 1975 (NWFP Act No. V of 1975) (Fig. 5.1).

Every year, millions of terrapins are consumed through Asian food markets. Presently, several species of turtles are in decline. Nilssonia hurum is traded in East Asian markets at volumes of 60-80 tons per week (IUCN, 2015).

In Asian countries, the terrapins are mostly utilizing in medicine, food, jewelry, tourist souvenirs, pets and leather. In current study, it was also observed that soft-shelled turtles are major targeted terrapins by local peoples as parts of these turtles are in high demand in the Chinese markets and used in Chinese food and medicines. Some terrapin’s traders contact the local peoples and offer them good amount to start the hunting and adopt it as their permanent business. Local techniques and instruments are used for turtle’s capturing (Fig. 5.2 – 5.4).

Arshad (2015) reported that 1.90 Metric ton flesh of terrapin’s worth of 6.165 million (US$) was seized by Pakistan Customs from the

155 traffickers during 2014-2015. Pakistan Customs also seized about two thousands live terrapins during this period from the seven different groups who tried to smuggle these to East Asian countries and Iran. Turtles are not included in the list of notified items under section 2(S) of the Customs Act (1969), However, the penal action as envisaged in clause (9) of Section 156 (1) of the Customs Act, 1969 was carried out and penalty was imposed on the accused. The Wildlife smugglers of large cities especially from Lahore approach local poachers for illicit harvest of terrapins. Processed body parts of turtles are transported from local markets to big markets.

Shahid Reported in “Dawn news” on 29th August, 2015 that Pakistan has become the first country in south Asia to adopt DNA barcoding to control the poaching. The DNA barcoding is a biological technique that uses a short genetic marker in an organism’s DNA to identify its species. This technique was gaining fruitful results to detect and stop cross-border smuggling of endangered species in the advanced countries. Over two thousand kg of flesh of turtles destined for Thailand, was confiscated at the Jinnah International airport, Karachi in last year through the DNA barcoding method for the first time. The worth was estimated about US$ 60 million.

Capturing of turtles for supply to foreigners and export is one of main threat to these turtles. Fishermen also kill these terrapins during fishing, canal closure during winter season and de-silting are also harmful to turtles. In the current research work, it was also noticed that canals are periodically closed during hibernation period which is another cause of death of turtles. The running water

156 maintains the body temperature of terrapins and these cold blooded vertebrates’ face severe environmental conditions due to unavailability of water and shortage of food due to canal closure in “Bhal” winter. Dogs and some other animals like monitors, kites, crows, jackals, foxes and cats were observed wandering during “Bhal” (canal closure) in search of food, these animals eat dead and trapped turtles and their hatchlings in shallow water during present study. Some turtles are accidentally killed with nets, whereas, some fisherman consider them the enemies of fishes, therefore, they kill the captured terrapins to save their fishes. 3 dead bodies of Pangshura smithii, 8 of Nilssonia gangeticus, 2 of Nilssonia hurum and 5 of Lissemys punctata were observed during present study in different study areas (Fig. 5.5).

Diversion of water for irrigation and the drainage of wetlands is another key cause of the degradation of many wetlands of Study area especially in Peshawar Valley. Small wetlands formed by the seepage of the irrigation canals are targeted for drainage, other threatened by decreasing ground water levels due to draining programs (SCARP) in Peshawar Valley. The drainage programs have also caused loss of natural water bodies. Most of the drains system (Hisara Drain, Dub drain and Kashmalo Drain) of Charsadda District are facing this problem.

Cultivation on wetland’s banks is a common practice among several areas that can destroy or alter nesting sites of turtles. Slash and burn agriculture near the wetlands during the nesting times of terrapins is also a cause of decrease in population. Continued cutting and

157 clearing of riparian vegetation along wetlands leads to decreased productivity of terrapins and also a cause for flooding. Siltation is the most common problem faced wetlands in KPK. Due to the denudation of catchment area, the inflow of water brings with it a certain amount of silt. This inflow increases during the rainy season and causes siltation of wetland.

Introduced fish species such as Carp (Cyprinus caprio) and Gambusia (Gambusis Spp.) prosper with many of the alterations that are occurring in wetlands such as altered water regimes and pollution, are blamed for many of the problems affecting inland waters such as increased turbidity, loss of native fish, invertebrates and water plant diversity (Kennard et al., 2005).

According to locals, terrapins of all the eight species were hunted by poachers of locals and outsiders a few years ago to the point that they were almost wiped out, but still we observed a reasonable population here during present study, which indicates because of ideal habitat for terrapins and the capability of terrapins to recover from harvest within a relatively short period of time.

Geoclemys hamiltonii was recorded only in D. I. Khan District, while other seven species were Common, less common, intermediate level and rare in both D. I. Khan and in Peshawar Valley during the present study. We noticed the lack of knowledge about conservation of wildlife including terrapins in local communities.

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During the study, we observed the following anthropogenic threats to turtle’s population (Fig. 5.6 – 5.11).

1. The foremost threat to terrapins is uncontrolled poaching and poor implementation of wildlife (Protection, Preservation, conservation and management Act, 1975) of KPK province. Due to this reason, poaching and capturing of turtles in a large number is common. They are illegally supplied to foreigners and their export to South Asia is in normal practice (Fig. 5.6).

2. Illegal trade (for consumption, medicine and Pet trade) (Fig. 5.7).

3. Habitat destruction (Damming and channeling of rivers, logging, slash and burn agriculture to population).

4. Natural habitat loss is one of the major threats to terrapins as during in Mon soon season (July to September. Often wandering turtles fall in to the hands of uncaring peoples who may pelt them with stones just for fun.

5. Urbanization and development of road networks along the wetlands.

6. Some locals especially some Nomadic tribes eat turtles and their eggs.

7. Stray dogs, cats, crow and kites were observed wondering extensively during canal closure in search of food. These animals eat the eggs, new hatchlings and turtles.

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8. De siltation of canals and rivers is another cause of killing of turtles during hibernation because hibernated turtles have been carried out from their natural habitat along with the silt which leads to high mortality ratio of turtles.

9. During the closures of canals, turtles faced shortage of water as well as scarcity of food resources which results in population decline (Fig. 5.8).

10. Nesting sites of terrapins are not protected (Fig. 5.9).

11. Fishermen also use different unsustainable and brutal methods like adding pesticides to water, using electric currents to stun the fish and blowing dynamite. This is also a reason that the population of terrapins are decreasing from the area (Fig. 5.10).

12. Accidental killings of turtles are also common by capturing in nets while sometimes they were killed by fishermen for protection of their fishes as they are considered as fish enemy (Fig. 5.10 & 5.11).

13. Lack of awareness about the role of turtles in aquatic ecosystems.

14. Poverty and unemployment.

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PRIORITY ACTIONS 1. Habitat destruction and alteration, harmful and unsustainable fishing techniques may be avoided.

2. The legislation banning the trade in turtles should be implemented in its true letter and spirit.

3. Department of Wildlife of KPK and Department of Fisheries should control poaching of turtles and their mortality in fishing nets.

4. Turtle farming practices need to be initiated to reduce the hunting pressure.

5. Awareness among the local masses should be created about the conservation and importance of biodiversity in ecosystems including turtles (Fig. 5.12).

6. Community should be encouraged to participate in the protection/conservation and management affairs about wildlife.

7. There is a dire need for the development of policy for the conservation and sustainable use of reservoir’s resources. Therefore, a comprehensive reservoir management plan must be developed and implemented without any further delay.

8. Monitoring and assessment of ecological changes need to be doing on regular bases.

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9. Public awareness, media campaign and other similar activities can result in the sustainable utilization about wildlife and resources of the reservoir. Sign boards highlighting significance of wildlife of the reservoir should be placed on public places, roads and important ways.

Before this study, no scientific data has been reported about the population, distribution and status of terrapins of KPK. This is the first comprehensive scientific study to provide a baseline data. Hopefully, this study will serve as a springboard for further research study, conservation and future plan for management about terrapins in KPK province. Further research studies are needed to collect more data for preparing the conservation plan for the management of terrapins in other areas of Khyber Pakhtunkhwa. On the basis of present study, it is concluded that the terrapins are an important part of our ecosystem and need immediate attention for its conservation and management.

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Fig. 5.1. Notification for addition of terrapins of KPK in Wildlife Act.

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Fig. 5.2. Some of the equipments for turtle’s poaching: (A) Hooks (B) Spear rods (C) Net.

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Fig. 5.3. Capturing techniques for Turtles: (A) Through drag net (B) Through generator (Electric current).

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Fig. 5.4. Captured turtles:

(A) Through net (B & C) Through hooks.

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Fig. 5.5. Dead Specimen of freshwater turtles: (A) Dead Lissemys punctata crushed by vehicle on road. (B) Dead Nilssonia gangeticus.

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Fig. 5.6. Trading activity of body parts of turtles: (A) Slaughtered turtles (B & C) Body parts are being drying.

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Fig. 5.7. Trading activity for turtles.

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Fig. 5.8. Another Trading activity for turtles.

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Fig. 5.9. Canal closure during winter season.

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Fig. 5.10. Eggs in nests of Freshwater turtles.

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Fig. 5.11. Turtle’s capturing: (A) Through angle (B) Through net (C) Through Electric current.

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Fig. 5.12. Net making.

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Fig. 5.13. Awareness is giving to local community about turtles.

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CONCLUSION

Study of distribution and current population status of terrapins was conducted in Charsadda, Peshawar, Nowshera, Mardan and D. I. Khan Districts of Khyber Pakhtunkhwa. Eight species viz. Lissemys punctata, Chitra indica, Nilssonia hurum, Nilssonia gangeticus, Hardella thurjii, Pangshura smithii, Pangshura tectum, and Geoclemys hamiltonii were recorded.

On the basis of three years study (2013-2015), it was concluded that Geoclemys hamiltonii (Spotted pond turtle) is only found only in D. I. Khan District. This species was not observed in any other study areas. Nilssonia gangeticus and Lissemys punctata were more common in all the selected areas of KPK and both these species were found in every study site. The frequency of population of these two species were in satisfactory position, however the hunting pressure and illegal trading of theses turtles are in peaks and can damage drastically the population if not protected.

The population of Chitra indica, Hardella thurjii and Pangshura tectum are recorded as in rare status in KPK. All these three turtle’s species were recorded randomly in different study sites, however the frequency of population were in poor position. These species need an immediate and strong protection.

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The population of Pangshura smithii and Nilssonia hurum were recorded in intermediate level and both these were observed randomly in different study sites.

Due to habitat destruction, eutrophication, agricultural activities, over grazing of aquatic vegetation and deficiency of water, population of terrapins has been decreasing day by day.

Pakistan has been gifted with a very valuable resource in the form of fresh water turtles which are near to be endangered or extinct, if not properly conserved. Poaching, habitat destruction and alterations, harmful and unsustainable fishing techniques and unprotected nesting sites are major threats of freshwater turtles in KPK. Some strong legislations should be made and implemented to manage this critical situation in order to conserve their population in future. It is required that immediately some priority actions must be taken to conserve them. Wildlife department of KPK and Fisheries department should take notice of poaching of turtles and also the turtles by catch during fishing. Turtle farming practices should be initiated to reduce the hunting pressure. Local poaching communities should provide with alternate livelihood. Awareness should be created among the locals about the importance of wildlife. These terrapins are important part of our aquatic ecosystems and need an urgent attention for restoration, conservation and management. Further research works are needed to collect more data about terrapins.

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LIST OF PUBLICATIONS

AMTYAZ SAFI

1. Forstner, M. R. J., Sirsi, S., Gomez, A. V. and Amtyaz Safi. Population Genetics of some Hard- shelled Asian turtles (Orlitia borneensis, Batagur baska and Batagur bornensis). (Under publication) 2. Amtyaz Safi. Normal Anatomy and Histology of some organs of digestive and reproductive systems of striped piggy fish, Pomadasys stridens (Forsskal, 1775) (Family; Pomadasyidae) of Karachi Coast, Pakistan. (Under publication) 3. Amtyaz Safi and Malik, S. Diversity and current population status of freshwater fishes of Bajaur Agency, Pakistan. (Under publication) 4. Amtyaz Safi, Hashmi, M. U. A., Khan, I. S and Latif, T. A. 2016. A review of vertebrate biodiversity and environmental pollution on Keenjhar Lake: A Ramsar site. Canadian Journal of Pure & Applied Sciences. (Under publication). http://www.cjpas.net (Canada) 5. Khan, M. Z., Amtyaz Safi, Kanwal, R., Hashmi, M. U. A., Sidiqui, S., Zehra, A., Yasmeen, Y., Fatima, F., Hussain, B., Ghalib, S. A. and Ubaidullah 2016. A review of distribution, threats, conservation and status of freshwater turtles in Sindh. Canadian Journal of Pure & Applied Sciences. 10(3): 3997-4009. http://www.cjpas.net (Canada) 6. Khan, M. Z., Al-Sheryani, M. J., AlKamzari, A. M., Hashmi, M. U. A., Young, L., Khafaga, T., Yamaguchi, N., Khan, I. S., Amtyaz Safi, Siddiqui, S. and Hany El Shaer. 2016. Observations of rock semaphore gecko (Pristurus rupestris) in al Jabal al Akhdar scenic reserve, Sultanate of Oman: a review; Canadian Journal of Pure & Applied Sciences. 10(2): 3883-3890. http://www.cjpas.net (Canada) 7. Begum, A., Khan, M. Z., Amtyaz Safi, Kanwal, R., Hashmi, M. U. A., Sidiqui, S., Zehra, A., Yasmeen, Y. and Ghalib, S. A. 2016. Distribution, status and current trends in the population of coastal birds of Baluchistan. Canadian Journal of Pure & Applied Sciences. 10(2): 3853-3864. http://www.cjpas.net (Canada) 8. Khan, M. Z., Amtyaz Safi, Kanwal, R. and Ghalib, S. A. 2016. Population status, Distribution and Conservation of Freshwater turtles of Peshawar valley, PAKISTAN. Canadian Journal of Pure & Applied Sciences. 10(1): 3732-750. http://www.cjpas.net (Canada) 9. Khan, M. Z., Amtyaz Safi, Fatima, Farina, Hashmi, M. U. A., Hussain, B. Siddiqui, S. and Ghalib, S. A. 2015. An evaluation of distribution, status and abundance of freshwater turtles in the selected areas of Sindh and Khyber Pakhtunkhwa provinces of Pakistan. Canadian Journal of Pure & Applied Sciences. 9(1): 3201- 3219. http://www.cjpas.net (Canada) 10. Amtyaz Safi, Khan, M. Z., 2014. Distribution and current population of freshwater turtles of District Charsadda of Khyber Pakhtunkhwa, Pakistan. The Journal of Zoology studies. 1(4): 01-06. http://www.journalofzoology.com (India) 11. Hashmi, M. U. A., Khan, M. Z., Huda, N., Gabol, K. and Amtyaz Safi. 2014. Observation of the Status, Distribution, Habitat and Population Estimation of the Indian Spiny Tailed Lizard Saara hardwickii (Gray, 1827) of Thatta District of Sindh Pakistan. American Journal of Zoological Research. 2(3): 46-50. http://pubs.sciepub.com/ajzr/2/3/2 (USA) 12. Amtyaz Safi, Khan, M. A, Khan, M. Z, & Hashmi, M. U, A., 2014. Length-Weight relationship and condition factor of striped piggy fish, Pomadasys stridens (Forsskal, 1775) (Family; Pomadasyidae) of Karachi Coast, Pakistan. Journal of entomology and zoology study. 2(5): 25-30. http://www. entomoljournal.com (India) 13. Amtyaz Safi, Khan, M. A. and Khan, M. Z. 2014. Study of some morphometric and meristic characters of striped piggy fish, Pomadasys stridens (Forsskal, 1775) (Family; Pomadasyidae) of Karachi Coast, Pakistan. The Journal of Zoology studies. 1(4): 31-38. http://www.Journalofzoology.com (India) 14. Amtyaz Safi, Khan, M. A. and Khan, M. Z. 2014. Study of some morphometric and meristic characters of Saddle grunt fish, Pomadasys maculatus (Bloch, 1793) (Family; Pomadasyidae) of Karachi Coast, Pakistan. American Journal of Marine Science. 2(2): 38-42. http://pubs.sciepub.com/marine/2/2/2 (USA) 15. Amtyaz Safi, Khan, M. A, Khan, M. Z, & Hashmi, M. U, A., 2014. The Sex Ratio, Gonadosomatic Index & Stages of Gonadal Development of Saddle Grunt fish, Pomadasys maculatum (Bloch, 1793) of Karachi Coast, Pakistan. Canadian Journal of Pure & Applied Sciences. 8(1): 2621-2627. http:// www.cjpas.net (Canada) 16. Amtyaz Safi, Khan, M. A, Khan, M. Z, & Hashmi, M. U, A., 2013. The Sex Ratio and Gonadosomatic Index of Sind Sardine fish, Sardinella sindensis (Day, 1878) (Family: Clupeidae), from Karachi Coast, Pakistan. International journal of biological research. 1(2): 34-40. http://www.sciencepubco.com /index.php/IJBR (Germany)

17. Amtyaz Safi, Baptista, R. B and Almeida Val, V. M. F., 2013. The effect of CO2 and

temperature on Tambaqui (Callosoma‐ macropomum) fish of Amazon, Brazil. International journal of biological research. 1(2): 41-47. http://www.sciencepubco.com /IJBR (Germany) 18. Amtyaz Safi, Khan, M. A, Khan, M. Z, & Hashmi, M. U, A., 2013. Studies of the Fecundity of Sind Sardine fish, Sardinella sindensis (Day, 1878) (Family: Clupeidae), from Karachi Coast, Pakistan. International journal of biological research. 1(2): 15- 18. http:// www. sciencepubco.com/index.php/IJBR (Germany) 19. Hashmi, M. U. A, Khan, M. Z, Amtyaz Safi, Huda, N., 2013. Current Status, Distribution and threats of Varanus Spp. (Varanus bengalensis & Veranus griseus) in Karachi & Thatta of Sindh. International Journal of Fauna and Biological Studies. 1(1): 34-38. http://www.faunajournal.com (India) 20. Amtyaz Safi, Khan, M. A, Khan, M. Z, & Hashmi, M. U, A. 2013. Observation on the food and feeding habits of striped piggy, Pomadasys stridens (Forsskal, 1775) (Family: Pomadasyidae) From Karachi Coast Pakistan. International Journal of Fauna and Biological Studies. 1(1): 7-14. http:// www.faunajournal.com (India) 21. Amtyaz Safi, Khan, M. A, Khan, M. Z, & Hashmi, M. U, A., 2013. Studies on Gonadosomatic Index & Stages of Gonadal Development of Striped piggy fish, Pomadasys stridens (Forsskal, 1775) (Family; Pomadasyidae) of Karachi Coast, Pakistan. Journal of entomology and zoology study. 1(5): 28-31. http://www.entomoljournal. com (India) 22. Khan, M. A., Amtyaz Safi and Siddique, S. 2013. Length-Weight relationship of Pomadasys maculatum (Bloch, 1793) From Karachi Coast Pakistan. International Journal of biology and biotechnology. 10(3): 471 - 474. http://www.ijbbku.com (Pakistan) 23. Amtyaz Safi, Khan, M. A., 2013. Studies on the Fecundity and sex ratio of striped piggy fish, Pomadasys stridens (Forsskal, 1775) (Family; Pomadasyidae) From Karachi coast, Pakistan. International Journal of biology and biotechnology. 10(3): 431-436. http://www.ijbbku. com (Pakistan) 24. Khan, M. A and Amtyaz Safi. 2005. Food and feeding habits of saddle grunt fish, Pomadasys maculatum (Bloch, 1793) (Family: Pomadasyidae) From Karachi Coast Pakistan. International Journal of biology and biotechnology. 2(4): 875-881. http://www.ijbbku.com (Pakistan) 25. Khan, M. A. and Amtyaz Safi. 2004. Studies on the Fecundity and sex ratio of the Saddle Grunt Fish, Pomadasys maculatum (Bloch, 1793) (Family: Pomadasyidae) From Karachi Coast Pakistan. International Journal of biology and biotechnology. 1 (1):111-115. http://www.ijbbku.com (Pakistan) PROJECTS:

► Have completed a project (2015) under HEC (Higher education commission) of Pakistan for research work in Texas State University USA under Prof. Dr. Michael Forstner and completed research on the topic “Population Genetics of Orlitia borneensis (Malaysian Giant turtle).

►Have completed a project on Amazonian Fish (2012); scholarship from (CNPqMiistry of “ciece, Techology ad Iovatio of Brazil ad copleted research o the topic

“The effect of CO2 and temperature on Tambaqui (Callosoma macropomum) fish of Amazon, Brazil” in INPA (National Institute of research in Amazon), Manaus, Amazona, Brazi. PEER REVIEWER:

 Journal of Marine biology and Oceanography (USA)  International Journal of Modern Plant and Animal Sciences (USA)  Russian Journal of Herpetology (Russia)  International Journal of Fisheries and Aquaculture (Nigeria)  African Journal of Agricultural Research (www.academicjournals.org/Ajar)  African Journal of Biotechnology (AJB) (www.academicjournals.org)

EDITOR:

► Editor of INTERNATIONAL JOURNAL OF AGRICULTURE AND EARTH “CIENCE IJAE“. http://iiardpub.org/editorials.php?j=IJAES

International Institute of Academic Research and Development (IIARD).

REPRINTS OF SOME RELATED PUBLICATIONS

Canadian Journal of Pure and Applied Sciences Vol. 10, No. 3, pp. 3997-4009, October 2016 Online ISSN: 1920-3853; Print ISSN: 1715-9997 Available online at www.cjpas.net

A REVIEW OF DISTRIBUTION, THREATS, CONSERVATION AND STATUS OF FRESHWATER TURTLES IN SINDH

*M Zaheer Khan, Roohi Kanwal, Syed Ali Ghalib, Farina Fatima, Afsheen Zehra, Saima Siddiqui, Ghazala Yasmeen, Amtyaz Safi, Muhammad Usman A Hashmi, Babar Hussain, Muhammad Asif Iqbal, Uzma Manzoor and Ubaid Ullah Faculty of Science, Department of Zoology (Wildlife Section), University of Karachi, Karachi-75270, Pakistan

ABSTRACT

There are two families, six genera and eight species of freshwater turtles found in Pakistan, and the same species have also been recorded in Sindh province, six of which are threatened, and all species are listed in CITES Appendices I / II. Family Geoemydidae consists of Hard shelled turtles viz Spotted Pond turtle (Geoclemys hamiltonii), Crowned river turtle (Hardella thurjii), Brown roofed turtle (Pangshura smithii), and Indian roofed turtle (Pangshura tectum) and the second Family Trionychidae comprises of Soft shell turtles viz. Indian narrow-headed soft-shell turtle (Chitra indica), Indian soft-shell turtle (Nilssonia gangeticus), Indian peacock soft –shell turtle (Nilssonia hurum) and Indian flapshell turtle (Lissemys punctata). In Sindh province, Thatta, Sujawal, Badin, Dadu, Khairpur, Sanghar and Sukkur Districts have been identified as hotspots for freshwater turtle populations. Legally, all freshwater turtles in Sindh have been protected under the Sindh Wildlife Protection Ordinance 1972. Many efforts have been made by the Government, Non- governmental organizations and Academia for the protection and conservation of turtle population in Pakistan. The World Conservation Union for Nature - IUCN, WWF Pakistan, Sindh Wildlife Department, Zoological Survey of Pakistan and Department of Zoology (Wildlife Section), University of Karachi are contributing in efforts for the conservation of freshwater turtles in Sindh. But still, freshwater turtles are facing serious threats due to habitat destruction, urbanization, developmental projects and illegal trading.

Keywords: Sindh, population, distribution, freshwater turtles, threats.

INTRODUCTION cuisines. Their fat is also used as a major component of cosmetic industry in USA and other countries. Freshwater turtles play a major role in maintaining balance in ecosystem of any wetland. They act as Pharmaceutical industries are also utilizing plastron of scavengers by decaying dead organic matter. They act as Turtles for preparing specific medicines. In China and indicators of a healthy aquatic ecosystem. Some are Taiwan, specialized medicinal compositions are prepared carrion eating species that feed on aquatic weeds and by using plastrons. China and Taiwan are considered as reduce eutrophication. There are 313 species of Tortoises the major markets that are famous for plastron imports. and Fresh water Turtles present worldwide, while 128 According to a statistical review, annually hundreds of Freshwater Turtle species have been included in IUCN tons of plastron are imported by Taiwan. Red List of Threatened species (Fritz and Havas, 2007). Economically, freshwater turtles are considered as more Guilinggao jelly is the specialized medicinal composition valuable as compared to the fisheries because of the that made up from boiling of plastron of turtles along with presence of good quality flesh and fats which are highly some herbs so it is also called as Turtle Herbal Jelly. It is demanded by international markets for different purposes. also used for improvement of circulation in body, good Flesh of turtles is mostly used in different Continental and muscle growth, resolving acne problems and for cure of American cuisines, which serve as a luxurious dish in many kidney diseases. many restaurants. The calipee is the fatty gelatinous yellowish material present over the lower shell of a turtle, Pakistan has eight species of freshwater turtles. Based on which is the symbol of delicacy in dishes of many absence or presence of horny scutes or scales on their carapace, freshwater turtles divide into two categories, *Corresponding author e-mail: [email protected] Soft shell Turtles and Hard shell Turtles, respectively. 3998 Canadian Journal of Pure and Applied Sciences

Soft shell turtle species includes Indian softshell turtle, export to all parts and products of wildlife. Peacock softshell turtle, Indian narrow-headed softshell turtle, and Indian flapshell turtle, while Spotted pond Formerly in legal ordinances of provinces of Pakistan, no turtle, Indian roofed turtle, Brown roofed turtle and protection was given to the species of freshwater turtles Crowned river turtle are Hard shell Turtles. and they were not considered as Protected in different wildlife protection acts of the provinces. However, Freshwater turtles are residing in the whole Indus River present situation is different from past. Along with several system. This system is comprises of many canals, other conservational measures, there are amended acts, irrigation ditches, ponds, agricultural ponds and water which have declared the freshwater turtles as protected reservoirs. All these tributaries of Indus River system are species. Appendices I and II of the CITES restricted the providing rich habitat for turtles. Major threats to the international trade, export and import of wildlife species species are illegal hunting, poaching, and trading for including the freshwater turtles, their parts and their export. products as well. Section 12 of Sindh Wildlife Protection Ordinance, 1972 also banned the export of protected Pakistan is continuously struggling for conservation and wildlife species including freshwater turtles. Pakistan has protection of these threatened species and became the also been facing threats to freshwater turtles which signatory of the Convention of International Trade in include scarcity of water in rivers, and canals, water Endangered Species of Wild Fauna and Flora (CITES) diversion and extraction projects for irrigation purposes, and CITES appendix I contains the four species and water pollution, habitat deterioration and fragmentation appendix II contains three freshwater turtles from due to unsustainable development. In this paper we Pakistan. reviews the distribution, threats, conservation efforts and status of freshwater turtles in Sindh. Conservation measures of all the species of wildlife are directly associated with legal decisions. In Pakistan, DISCUSSION Provincial governments are responsible for adopting all conservational measures in their own provinces. Sindh is the third largest province of Pakistan located in Implementation of Wildlife Protection Ordinances is the West of South Asia, having the area of about 140,915 major task for all provincial governments. In 1981, square kilometers (Fig. 1). Sindh is having very strong Federal Government passed a rule to ban the export of all belongings to Indus River and having a great variety of wild mammals and reptiles. It also includes the restricted ecosystems. In east, desert ecosystem lies in the form of

Fig. 1. Map of Sindh with Districts. Khan et al. 3999

Table 1. Status of Freshwater Turtles in Sindh.

S. CITES Appendix Family Scientific Name Common Name IUCN Status No. I II 1 Geoemydidae Geoclemys hamiltoni Spotted Pond Turtle Vulnerable + 2 Pangshura smithii Brown Roofed Turtle Near Threatened + 3 Pangshura tectum Indian Roofed Turtle Vulnerable + 4 Hardella thurjii Crowned River Turtle Vulnerable 5 Trionychidae Nilssonia gangeticus Indian Soft shell Turtle Vulnerable + 6 Nilssonia hurum Peacock Soft shell Turtle Vulnerable + 7 Lissemys punctata Indian Flapshell Turtle Least Concern + 8 Chitra indica Indian narrow headed Endangered + soft shell Turtle

Fig. 2. Geoclemys hamiltoni (Spotted Pond Turtle).

vast Thar Desert commonly known as Tharparkar. In the Khan, 2015), six of which are globally threatened. All west, mountainous ranges are existing known as Khirthar species are listed in CITES Appendices I / II (Table 1) mountain range. In north, Punjab province is present and their import and export is prohibited. while from southern side, Sindh is bordered by the Arabian Sea. Distribution Following areas of Sindh which are considered as The climatic conditions are moderate, hot in summer, and hotspots for Freshwater Turtles, these includes Thatta mild in winter. In summer season, temperature varies District, Sujawal District, Badin District, Dadu District, from 35 to 48 degree Celsius, while during winter Khairpur District, Sanghar District and Sukkur District. temperature ranges from 2 to 20 degree Celsius. Sindh is directly affected by two different monsoonal systems, one 1. Thatta District from southwest system that comes from Indian Ocean Thatta is the historical district of Sindh Province. This while other from northeast system coming from district is having very strong bonding with Indus River. Himalayan Mountains. Annual average rainfall is about Thatta district is situated in southern portion of Sindh six to seven inches. province. According to climatic distribution, this is included in lower region of Sindh. Major livelihood for Distribution and Status of Freshwater Turtles the people of Thatta is dependent on the fishing practices. There are six genera and eight species of Freshwater Thatta is distributed into four tehsils, Thatta, Mirpur Turtles recorded in Sindh (Fig. 2 - 9) (Khan et al., 2012a , Sakro, Ghora bari and Keti Bander. The Keti Bander is 4000 Canadian Journal of Pure and Applied Sciences

Fig. 3. Pangshura smithi (Brown Roofed Turtle).

Fig. 4. Pangshura tectum (Indian Roofed Turtle).

the coastal area, while Ghora bari is very famous because Keenjhar Lake of the presence of various fish farms there. Mir Pur Sakro Keenjhar Lake (Fig. 13) is a Ramsar site located in Thatta contains a major canal named as Ghulamullah Canal (Fig. District of Sindh. It covers approximately 14,000 ha of 10) or Mirpur Sakro Canal (Fig. 11). This canal and fish area and having latitude and longitude of 68o 03’ E and farms at Ghora bari (Fig. 12) serves as a very rich habitat 24o 56’ N. It is considered as one of largest freshwater for freshwater turtle populations. Major wetlands in lakes of Sindh and it is the major source of water supply Thatta district are Keenjhar, Haleji and Hadero Lakes. to Karachi city, Thatta city and Ketibunder. The main Khan et al. 4001

Fig. 5. Hardella thurjii (Crowned River Turtle).

Fig. 6. Nilssonia gangeticus (Indian soft shell Turtle or Ganges Soft shell Turtle). water supply to Keenjhar Lake comes from River Indus. were merged together after development of a dam at The location of Keenjhar Lake is about 19km North and Bangla (Khan and Abbas, 2011). This lake provides a rich North East to Thatta District, while it is situated 113km habitat for Fresh water turtles survival. away from Karachi city. Many seepage lagoons and marshes are surrounding the Keenjhar Lake, which are Haleji Lake connected with semi desert areas bearing limestone rock Haleji Lake (Fig. 14) is an important wetland of Sindh beds. This man made freshwater lake was formed in 1930 located in Thatta district. Its total area is about 6.58km2 when two small lakes named Keenjhar and Kalri Lake along with the maximum depth of 5 to 6 m. This 4002 Canadian Journal of Pure and Applied Sciences

Fig. 7. Nilssonia hurum (Indian Peacock soft shell Turtle).

Fig. 8. Lissemys punctata (Indian Flap shell Turtle). important Ramsar site is situated at 67o 46’38"E and 24o Hadero Lake 48’N having an altitude of 4 m. This lake is located Hadero Lake is a saline water lake which is located at 88km away from Karachi (Khan et al., 2012a,b; Khan et longitude of 24 o 49'N and latitude of 67 o 52'E in Thatta al., 2014). It is very rich in Biodiversity and a variety of district of Sindh province. Primarily it affirmed as Game species of fauna and flora are inhabitant of this lake. Sanctuary in 1971 but later on it was declared as Wildlife Haleji Lake is surrounded by lagoons which serves as a Sanctuary in 1977. Hadero Lake is natural lake that is natural habitat for fresh water turtles. located at the periphery of the stony desert. Its covered area is 1321 hectares. Livelihood of the local population Khan et al. 4003

Fig. 9. Chitra indica (Indian narrow headed soft shell Turtle).

Fig. 10. Ghulamullah Canal. is dependent on fishing from the lake. In past a number of 2. Badin District fresh water turtles had been observed in the vicinity of Badin District is located in the lower portion of Sindh this lake. called as Lar, It is having a critical geographical location that lies in between Tharparkar Desert and Arabian Sea. 4004 Canadian Journal of Pure and Applied Sciences

Fig. 11. In Mirpur Sakro Canal, Brown Roofed Turtle (Pangshura smithii) is ready for jumping.

Fig. 12. Fish farms at Ghora Bari.

The geographical coordinates are 24º-5' to 25º-25' north There are 24 important lakes and wetlands present in and 68º21' to 69º 20' east. Badin District is distributed in Badin District which serve as key potential areas for five tehsils which includes Matli, Talhar, Tando Bago, distribution of freshwater turtle populations. Major canal Badin and Golarchi. running through Thatta and Badin District is LBOD (Left Khan et al. 4005

Fig. 13. A view of Keenjhar Lake.

Fig. 14. A view of Haleji Lake.

Bank Outfall Drain). Fish farming is the major profession 3. Sujawal District of the local population of Badin district. There are about Sujawal is a newly formed district of Sindh Province. Its 370 Fish farms developed by local people that also have Latitude is 24°36'23" of North and longitude is 68°4'19" freshwater turtle population. of East. Indus River is the main demarcation line between 4006 Canadian Journal of Pure and Applied Sciences

Fig. 15. Nara Canal.

Fig. 16. A view of Sukkur Barrage.

Thatta District and Sujawal District. Administratively, it crops. Fish farming is also common. Important fish of this is subdivided into five tehsils named as Jaati, MirPur district is Palla that has been cultured in fish farms. Bathoro, Shah Bandar, Kharochan and Sujawal. The total Freshwater turtles have been mostly recorded from the area covered by this district is about 7335 km². The major near Sujawal. livelihood for local people is cultivation of agricultural Khan et al. 4007

4. Dadu District Sanghriaro Lake are the important lakes of Sanghar Dadu District is an important district of Sindh Province. It District. comprises of Mehar, Khairpur Nathan Shah, Dadu, Johi and Sehwan tehsils. Its total area is about 190704 square Chotiari Wetland Complex km. Geography of Dadu district is unique. It contains Chotiari Wetland Complex is the combination of many three different types of ecosystems, Kohistan or Hilly freshwater and Saline wetlands that covers an area of areas, Barrage area, and Lower lands river area. In east about 18000 hectares. This complex has the major water Indus River is existing. There are many waterways which reservoir named as Chotiari Dam. The geographical are flowing in this district locally called as Nais. The coordinates of Chotiari wetlands complex are 26°1' N major wetland in Dadu District is Manchhar Lake. Other latitude and 69°4' E longitude. It is bounded by Thar important lakes are Sanjri Dhand and Unheri Dhand. desert from East and North while in southern portion Nara canal is present. The major wetlands in Chotiari wetland Manchar Lake complex are Naro, Khor, Meena, Sajaran, Phuleil, Gun, Manchar Lake is a natural freshwater shallow lake that Wari, Jajur, Bholo and Jadpur (Rais et al., 2008). created by a vast depression formed in between hilly ranges. Khirthar Hills are present in the west, while Laki 7. Sukkur District hills are present in the south and Indus River flows in the Sukkur District comprises of four tehsils includes Sukkur, east. The deepness of this lake is 10km. This big water Rohri, Saleh Pat and Pano Aqil. Climatic condition of reservoir is sufficient to supply water for drinking Sukkur is very harsh and intense. Sukkur is famous for purposes to whole district as well as it is also a major Sukkur Barrage. Thick and dense Riverine forest is also a supplier of water to irrigation canals and agricultural unique ecological characteristic of Sukkur. It grows along croplands. This is also an important source of livelihood with the bank of Indus River. for local communities in the form of fishing practices. Local anglers called as Mohanas or Meerbahar used to Sukkur Barrage live in boats inside the lake. In past it was considered as Sukkur Barrage (Fig. 16) was constructed in 1932 over major roosting area for migratory birds but because of River Indus to control the flow of water in River Indus. In construction of MVND (Main Nara Valley Drain), most past it was also called as Lloyd Barrage. It has 66 gates. It of saline water drains out into Manchar Lake that result in irrigates about 7.63 million acres of area. The land of loss of natural fauna and flora from the lake. Drainage of Sukkur is very fertile and productive due to presence of Chemical effluents and other pollutants in lake also result this major irrigation canal system. Sukkur barrage is not in serious contaminations in water that leads to only responsible to fertile lands of Sukkur district but it biodiversity loss including that of turtles. also supply water through its canal system to Khairpur district, Mirpurkhas district, Sanghar district, Tharparkar 5. Khairpur District district and Hyderabad district. Sukkur Barrage is also Its total covered area is 15910 km2. There is complete responsible for drinking water supply, irrigation and flood network of canals present to irrigate the whole area, that control in Sukkur district. There is a very well developed is the reason Khairpur is a very fertile area for cultivation canal system that form unique networking and irrigation of all types of crops. system. There are seven canals that emerge out from Sukkur Barrage. Four canals originate from left bank Nara Canal while three canals originate from right bank. Nara Canal It a major canal emerging from Nara Tehsil of Khairpur is the major canal which is largest canal in Sindh. After district. It considered as largest canal of Sindh that Nara Canal, Rohri Canal exist and the third canal is Mir originates from Sukkur Barrage, extends from Nara Tehsil Wah Canal, while forth is Abul Wah Canal. Three canals of Khairpur District to Sanghar, and finally drains off in originate from Right bank named as Dadu Canal, Rice Runn of Kutch Area. Nara wetland complex is very Canal and Khirthar Canal. All other canals are permanent, famous and ecologically important combination of while Rice Canal is a seasonal canal for cultivation of approximately 200 wetlands of different sizes, which are Rice fields. present on both sides of Nara Canal (Fig. 15). These serve as important habitats for freshwater turtles. Threats Sindh is the highly populated province of Pakistan. Most 6. Sanghar District of the districts are under-developed and poverty is one of Sanghar District situated in the middle area of Sindh the main reasons for their interest in trade of turtles. River Province. It comprises of six tehsils named as Jam Nawaz Indus, Indus basin and the tributaries of River Indus Ali, Khipro, Sanghar, Shadad Pur, Sinjoro and Tando includes canals, lakes, waterways, streams, swamps, Adam. Total covered area of Sanghar District is 9874km2. marshes and ponds, all provides feeding and breeding It is famous because of the presence of a wetland complex grounds for freshwater turtles. called as Chotiari wetland complex. Bakar Lake and 4008 Canadian Journal of Pure and Applied Sciences

Another threat for freshwater turtles in Sindh is the profession of the local communities residing near Industrial waste material is an important cause of reduced wetlands, and people depend on fishing for their survival. population of freshwater turtles. It results in disturbed Most of those areas in interior Sindh are rural areas and breeding biology, infertility, eggs shell thinning and local tribal communities like Mohana communities or physiological disorders in freshwater turtles. Kail communities are involved in trade of turtles along with fishing. Most of the soft shell turtles in Sindh are struggling for their existence and continuously fighting with high level Sand mining also has very disastrous effects on ecology of illegal killing for trade and export. The people kill and habitat of freshwater turtles. Commercial sand mining them and cut their parts to sell them to local consumers. from the rivers not only cause erosion but also destruct Alternate livelihood opportunities should be provided to the nesting areas of the turtles. It also modifies the them for enhancing their financial resources. direction of flow of water, configuration of riverbanks and makes water more turbid. All these factors directly China is the major market for Freshwater turtles. Being a influence on the growth of waterweeds, on under water neighboring country, it is very easy for traders to export activities of turtles and it also has hazardous effects on whole turtles or their parts to China. health of that aquatic ecosystem. Another important factor which is influenced by sand mining in rivers is reduction Environmental and climate changes and natural disasters in dissolved oxygen in water which ultimately results in are also major threats for turtle survival. Pollution, disturbance of aquatic life. contamination of water with industrial, agricultural, or domestic waste, pesticides sprays, fertilizers, global Trade of Calipee warming, and pathogens, all serve as threat for existence Calipee is the soft cartilaginous part of plastron of Soft of Freshwater turtles. Habitat modification, habitat shell Turtles. It is considered as most valuable part of degradation, and destruction are also important factors for turtle`s body. It can use in soups and other dishes. It is their loss. very interesting fact that being a Muslim country, Pakistan is not utilizing these parts of turtle for edible Urbanization, developmental projects, construction of purposes but most of these used to export to neighboring dams, barrages and roads are also important reason for countries like China. their decreased populations. Globally, turtle habitats are being extensively degraded, destroyed and fragmented, People from rural areas utilize this resource of nature to and where they still exist in reasonable populations turtles earn their riches. Mostly middlemen play an important are being subjected to subsistence hunting as well as for role by connecting the link between local fishermen and collection for regional and international consumption foreign traders. It recorded that many consignments markets, in addition to the growing international pet trade seized by custom in Pakistan, which supplied to China. (Klemens, 2000). The shipment contains tons of calipee, and tagged as dried fish. Conservation Efforts In Pakistan, many efforts have been made by the different Turtle habitats are being extensively degraded, destroyed governmental and nongovernmental organizations for the and fragmented because of anthropogenic activities conservation of turtles. IUCN Pakistan, WWF Pakistan, (Klemens, 2000). Some time natural habitat of freshwater Sindh Wildlife Department, Zoological Survey of turtles destructed because of developmental activities and Pakistan and Department of Zoology, University of urbanization. In Sindh, several developmental projects are Karachi are actively working and contributing for making under progress like Wind Mill projects Jhimpir (Thatta), studies regarding the protection and conservation of Thar Coal project (Tharparkar), Double carriageway freshwater turtles in Sindh. The Scientific and Cultural project (Thatta to Karachi), Solar power project Society of Pakistan (SCSP) provided capacity (Khairpur) and Thermal power projects. All these sort of development through training workshops to university developmental activities although are beneficial for students for conservation and management of freshwater mankind but also hazardous to natural habitat of wild turtles. The IUCN Commission on Ecosystem fauna. Management (CEM), West Asia also conducted several training programs for conservation and management of All crop growing activities and major deforestation also ecosystem at University of Karachi during 2013-2016. responsible for water seepage problems, modification of waterways and canal blockage. Agricultural wastewater Many researchers have worked on the distribution and and pesticides usage is also disastrous to population of conservation of freshwater turtles particularly in different fresh water turtles, Khan and Law (2005) also reported locations in Sindh. Noureen (2009) reported eight species pesticides threats to turtles. of freshwater turtles in Indus River system. Arshad and Khan et al. 4009

Noureen (2010) conducted a survey to identify the causes Khan, MZ., Jabeen, T., Ghalib, SA., Siddiqui, S., Alvi, of mass scale mortality of freshwater turtles downstream MS., Khan, IS., Yasmeen, G., Zehra, A., Tabbassum, F., Sukkur Barrage. Regarding illegal trading, Noureen et al. Hussain, B. and Sharmeen, R. 2014. Effect of Right Bank (2012) investigated the consequences and status of Outfall Drain (RBOD) on Biodiversity of the Wetlands of freshwater turtles in Pakistan. Recently, Khan (2015) Haleji Wetland Complex, Sindh. Canadian Journal of reported the distribution of freshwater turtles in Indus Pure and Applied Sciences. 8(2):2871-2900. Valley with morphology, natural history, and threats. Khan, MS. 2015. Status and Distribution of Freshwater Habitat loss was found to be the major threat for all Turtles in Pakistan. Bull. Chicago Herp. Soc. 50(4):51-53. species. Another study, Khan et al. (2015) described the distribution and status of freshwater turtles in Sindh and Khan, MZ., Safi, A., Fatima, F., Ghalib, SA., Hashmi, Khyber Pakhtun Khuwa (KPK). In this study, eight MUA., Khan, IS., Siddiqui, S., Zehra, A. and Hussain, B. species of freshwater turtles were recorded in Sindh and 2015. An Evaluation of Distribution, Status and population of turtles was estimated to be higher in Sindh Abundance of Freshwater Turtles in Selected areas of as compared to that in KPK. Sindh and Khyber Pakhtunkhwa Provinces of Pakistan. Canadian Journal of Pure and Applied Sciences. Recommendations 9(1):3201-3219. The legislation for conservation of turtles should be Klemens, MW. 2000. A new paradigm of conservation. properly implemented. Distribution areas and hotspots Turtle Conservation. 1-334. should highlighted. Community based awareness should be utilized. Alternate livelihood opportunities should be Noureen, U. 2009. Freshwater Turtles of Pakistan: Illegal provided to local people to avoid fresh water turtle trade. trade in Sindh: Preliminary findings of trade in Major threats should be detected and resolved. Habitat Freshwater Turtle Parts. A survey report submitted to the destruction should be discouraged. Export of parts of Ministry of Environment’s Pakistan Wetlands turtles should be checked, and local markets should be Programme. pp 36. monitored to minimize the use of turtles in as pet trade. Noureen, U., Khan, A. and Arshad, M. 2012. Exploring REFERENCES illegal trade in freshwater turtles of Pakistan. Rec. Zool. Surv. Pakistan 21:19-24. Arshad, M. and Noureen, U. 2010. Investigating mass Rais, M., Khan, MZ., Ghalib, SA., Nawaz, R., Akbar, G., scale mortality of freshwater turtles downstream Sukkur Islam, SL. and Begum, A. 2008. Global conservation Barrage, Indus River, Sindh. A report submitted to the significance of Chotiari wetlands complex, Sanghar, Ministry of Environment’s Pakistan Wetlands Program. Sindh. The Journal of Animal and Plant Sciences. 23 pp10. (6):1609-1617. Fritz, U. and Havas, P. 2007. Checklist of Chelonians of World. Vertebrate Zoology. 57(2)149-368. Received: August 10, 2016; Revised: Sept 26, 2016; Khan, MZ. and Law, FCP. 2005. Adverse Effects of Accepted: Sept 28, 2016 Pesticides and related Chemicals on Enzyme and Hormone Systems of Fish, Amphibians and Reptiles. Proc. Pakistan Acad. Sci. 42(4):315-323. Khan, MZ. and Abbas, D. 2011. Aquatic Vertebrates of Haleji and Keenjhar Lakes. Lap Lambert Academic Publishing, Germany. pp216. Khan, MZ., Ghalib, SA., Siddiqui, S., Siddiqui, TF., Farooq, RY., Yasmeen, G, Abbas, D. and Zehra, A. 2012a. Current Status and Distribution of Reptiles of Sindh. Journal of Basic & Applied Sciences. 8(1):26-34. DOI: http://dx.doi.org/10.6000/1927‐5129.2012.08.01.05. Khan, MZ., Abbas, D., Ghalib, SA, Yasmeen, R., Siddiqui, S., Mehmood, N., Zehra, A., Begum, A., Jabeen, T., Yasmeen, G. and Latif, T. 2012b. Effects of Environmental Pollution on Aquatic Vertebrate and Inventories of Haleji and Keenjhar Lakes: Ramsar Sites. Canadian Journal of Pure and Applied Sciences. 6(1):1759-1783.

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POPULATION STATUS, DISTRIBUTION AND CONSERVATION OF FRESHWATER TURTLES OF PESHAWAR VALLEY, KHYBER PAKHTUNKHWA, PAKISTAN

M Zaheer Khan, *Amtyaz Safi, Syed Ali Ghalib and Roohi Kanwal Wildlife Section, Department of Zoology, University of Karachi, Karachi - 75270, Pakistan

ABSTRACT

A total of 2,791 individuals of freshwater turtles were recorded from 18 study sites, located within four districts of Peshawar Valley (Peshawar, Charsadda, Nowshera and Mardan districts) belonging to the family Trionychidae, including the Indian Narrow-headed Softshell Turtle (Chitra indica), Indian Softshell Turtle (Nilssonia gangetica), Indian Peacock Softshell Turtle (Nilssonia hurum) and Indian Flapshell Turtle (Lissemys punctata andersoni) and the family Geoemydidae, including Brown Roofed Turtle (Pangshura smithii), Crowned River Turtle (Hardella thurjii) and Indian Roofed Turtle (Pangshura tectum). Based on our present study data, Lissemys punctata (28.52%) and Nilssonia gangetica (27.41%) were common, whereas, Nilssonia hurum (14.76%) and Pangshura smithii (11.04%) were less abundant. Chitra indica and Pangshura tectum were found at levels that may be categorized as scarce (7.31% and 7.49%, respectively). Hardella thurjii (3.48%) was rarely recorded. On the other hand, Lissemys punctata (28.52%) and Nilssonia gangetica (27.41%) were common at all 18 sites sampled, followed by Pangshura smithii at 16 of 18 sites. The Spotted Pond Turtle (Geoclemys hamiltonii) was unrecorded during the present study, but this species had been reported from different parts of Pakistan by other authors. Habitat destruction, desilting of canals, harmful and unsustainable fishing techniques, such as dynamite explosion, electric-shocks and pesticides, and unprotected status of nesting sites were recorded as major threats to freshwater turtles in Peshawar Valley.

Keywords: Peshawar Valley, freshwater turtles, distribution, population status, conservation.

INTRODUCTION

Peshawar Valley includes the districts of Peshawar, Charsadda, Nowshera, Mardan, Swabi and parts of Malakand, Mohamand and Khyber Agencies. The total length of the Valley is approximately 8,800 km2 lying between 71º15’ and 72º47’E and 33º40’ and 34º31’N (Fig. 1).

The order Testudines comprises of 13 families of tortoises, terrapins and sea turtles. A total of 289 living species of tortoises and terrapins are currently extant, and inhabit a great diversity of habitats (Azam and Saeed, 2011; Safi and Khan, 2014; Akbar et al., 2006; Khan, 2003, 2004; Khan et al., 2012, 2015). Two families of freshwater turtles are found in Pakistan, Geoemydidae which contains Hardshell turtles such as Spotted Pond Turtle (Geoclemys hamiltonii), Crowned River Turtle (Hardella thurjii), Brown Roofed Turtle (Pangshura smithii), and Indian Roofed Turtle (Pangshura tectum), while the other family, Trionychidae comprises of softshell turtles such as the Indian Narrow-headed Softshell Turtle (Chitra indica), Fig. 1. Maps of Pakistan and Khyber Pakhtunkhwa (KPK) showing Study areas of Peshawar Valley. *Corresponding author e-mail: [email protected] 3733 Khan et al.

Indian Softshell Turtle (Nilssonia gangetica), Indian and determination of dispersal ranges of turtles in the Peacock Softshell Turtle (Nilssonia hurum) and Indian water bodies of Peshawar valley and record the natural Flapshell Turtle (Lissemys punctata andersoni). Soft shell and anthropogenic threats faced by the freshwater turtle turtles are larger in size as compared to hard-shell turtles. species and to suggest action plan for their conservation. Among freshwater turtles that are human consumed, softshell turtles are considered to be the best due to their Table 1. IUCN and CITES Status of Freshwater Turtles of low bone to meat ratio and larger proportions of cartilage Pakistan. and gelatinous skin. This demand has made softshell turtles the most important components of the freshwater Species Common CITES SSC Red turtle trade in Asia (Walters, 2000). Name Status List Status Chitra Indian Appendix Endangered Terrapins play important role for maintaining healthy indica Narrow- II ecosystem of freshwater, as they act as scavengers, headed herbivores, omnivores and carnivores, provide dispersal Softshell mechanism for seeds, scavenging dead organic matter and Turtle help to maintain healthy populations of aquatic life Hardella Crowned Appendix Lower Risk (Lovich, 1994; Safi and Khan, 2014), Softshell turtles are thurjii River II source of traditional Chinese medicine, and their shells Turtle are supposed to be highly effective for purifying blood Pangshura Brown Appendix Lower Risk and to cure many diseases (Zuberi, 2009; Safi and Khan, smithii Roofed II 2014). A medicine by the local name Guilinggao has been Turtle extracted from plastron and used for treatment of various Pangshura Indian Appendix Vulnerable heart diseases. Plastron is commonly used to extract a tectum Roofed I product called ‘Turtle Jelly’. The use of extracts of turtles Turtle in cosmetic industry is also in practice. Some Geoclemys Spotted Appendix Vulnerable pharmaceutical industries are also developing on the basis hamiltonii Pond I of turtle byproducts which has lead to declines in their Turtle respective populations. Nilssonia Indian Appendix Vulnerable gangetica Softshell I CITES Appendix-I lists the Indian Softshell Turtle, Turtle Peacock Softshell Turtle, Spotted Pond Turtle and the Nilssonia Indian Appendix Vulnerable Indian Sawbacked Turtle. Whereas, Crowned River hurum Peacock I Turtle, Indian Narrow-headed Softshell Turtle and Brown Softshell Roofed Turtle are listed in Appendix-II of the Convention Turtle on International Trade in Endangered Species of Wild Lissemys Indian Non Lower Risk Fauna and Flora - CITES (Shah, 1996; Mehmood et al., punctata Flapshell CITES 2012). The Indian Flapshell Turtle is not listed in CITES andersoni Turtle Species database of 2014 (Table 1).

MATERIALS AND METHODS Turtles play a vital role in ecological stability of food chains in wetlands and management of environmental In this study, 18 sites located in four districts (Peshawar, regime. They may contribute in reduction of algal bloom. Charsadda, Nowshera and Mardan) of Peshawar valley Anthropogenic disturbance to lentic and lotic ecosystems were selected for survey during Jan 2013 to November can change ranging behavior, with subsequent change in 2015. Indus River, distributaries of River Kabul demographic processes. For example, stress in freshwater (Sardaryab, Naguman and Shahalam), Tributaries of turtles suppresses egg laying and reproduction River Indus (River Budhni, River Bara, River Jindi, River (Thompson, 1993; Safi and Khan, 2014). In Pakistan, the Swat, River Kabul) and some small water bodies (Drains trade of freshwater turtles was highlighted in 1990 (Baig, and Canals) like Kashmalo drain, Hisara drain, Fazalabad 2006; Safi and Khan, 2014). drain, Dub drain, Jalala drain, Branch No. 6 Canal and Sheikh Canal were surveyed in the valley of Peshawar as In Khyber Pakhtunkhwa (KPK), commercial exploitation shown in Figures 2-11. of turtles for their body parts commenced in the year 2006

(Baig, 2006). No prior scientific studies have been The populations of turtles were recorded during each visit reported on population status, distribution and to eighteen study sites. Species were identified in the field conservation of freshwater turtles of the valley. The main purpose of the present study is the population estimation 3734 Canadian Journal of Pure and Applied Sciences on the basis of standard published literature (Khan, 2003, identification cards were shown during interviews to 2004, 2015). identify the terrapin species. However, the present research is based on monitoring and Direct counting of basking turtles has been done by direct sightings of turtles by categorizing them into Minolta Binoculars of 10x50mm power. Netting basking, captured and floating turtles. The given formula technique was also used for capturing the terrapins for has been used for population estimation of turtles identification. Canals were surveyed, during canal closure following Khan et al., 2015: season. Animals found above ground in the dry canal were identified and counted. Poultry intestinal baited P=AZ hooks were used to capture terrapins. Information has 2YX been collected from Game watchers, local fishermen, P = Population boatmen, and field staff of Department of Irrigation, A = Total area Government of KPK. Evidences from the impression of Z = Number observed finger or foot prints, tails, presence of fecal pellets, egg Y = Average flushing distance laying excretion were also collected. Interviews were X = Length of strip conducted from the local community to obtain information about population status of terrapins. Special

Fig. 2. Map of study sites in Peshawar Valley: 1. Jalala drain, 2. Fazalabad drain, 3. Hisara drain 4. Behlola (Brach No. 6 of lower Swat River), 5. Dub drain, 6. Kashmalo drain (Turangzai), 7. Nimouri (River Jindi), 8. Khyali (River Swat), 9. Sardaryab (River Kabul), 10. Naguman (River Kabul), 11. Shaalam (River Kabul), 12. River Budhni, 13. Sheikh canal, 14. River Bara, 15. Kheshgi (River Kabul), 16. Hakimabad (River Kabul), 17. Kund Park (River Kabul + River Indus) and 18. Darwazgai (Indus River). 3735 Khan et al.

Fig. 3. River Jindi in Charsadda.

Fig. 4. River Swat (Khyali) in Charsadda.

3736 Canadian Journal of Pure and Applied Sciences

Fig. 5. River Kabul (Sardaryab) in Charsadda.

Fig. 6. River Budhni in Peshawar.

3737 Khan et al.

Fig. 7. River Kabul (Shahaalam) in Peshawar.

Fig. 8. River Kabul (Naguman) in Peshawar.

3738 Canadian Journal of Pure and Applied Sciences

Fig. 9. Kund Park (River Kabul meets Indus River) in Nowshera.

Fig. 10. River Kabul in Nowshera.

3739 Khan et al.

Fig. 11. River Swat in Charsadda.

Fig. 12. Indian Softshell Turtle (Nilssonia gangetica). 3740 Canadian Journal of Pure and Applied Sciences

RESULTS AND DISCUSSION recorded, which belong to families Trionychidae and Geoemydidae (Table 2 and Figs. 12-18). In the present study, 2,791 specimens of turtles were

Table 2. Population Distribution of Freshwater Turtles of Peshawar Valley.

S. No. Location Geographical Approx Observed Species Coordinates Surveyed area (km) C. N. N. L. H. P. P. Total % indica gangetica hurum punctata thurjii smithii tectum

1 Kashmalo 34.220361 N 4 - 29 09 42 09 17 07 113 4.05 drain 71.748956 E 2 Dub drain 34.160653 N 4 21 51 14 67 - 13 - 166 5.95 71.790753 E 3 Hisara drain 34.281803 N 4 18 79 27 48 - 16 08 196 7.02 71.82955 E 4 Branch No.6 34.245989 N 4 - 16 - 09 - 16 21 62 2.22 (L. Swat 71.849339 E River) 5 Khyali (River 34.216183 N 4 36 57 11 78 09 34 23 248 8.89 Swat) 71.668581 E 6 Nimouri 34.205394 N 4 19 129 58 98 11 15 03 333 11.93 (River Jindi) 71.7266 E 7 Sardaryab 34.129483 N 4 45 52 38 64 14 26 31 270 9.67 (River Kabul) 71.688142 E 8 Naguman 34.135110 N 4 25 39 22 40 03 31 12 172 6.16 (River Kabul) 71.572151 E 9 Shaalam 34.099296 N 4 18 28 22 56 - 09 - 133 4.77 (River Kabul) 71.579704 E 10 Budhni River 34.069724 N 4 03 39 17 38 06 - - 103 3.69 71.513442 E 11 Sheikh Canal 34.022608 N 4 - 11 - 18 02 - - 31 1.11 71.539149 E 12 Bara river 33.998141 N 4 - 06 15 27 - 24 - 72 2.58 71.691370 E 13 Kheshgi 34.042646 N 4 08 45 51 19 18 27 23 191 6.84 (River Kabul) 71.900196 E 14 Hakimabad 34.016727 N 4 05 48 47 52 13 26 27 218 7.18 (River Kabul) 72.035766 E 15 Kund Park 33.917708 N 4 04 39 48 33 04 16 24 168 6.02 (River Kabul 72.229829 E +Indus river) 16 Darwazgai 33.824637 N 4 02 28 33 16 08 19 22 128 4.59 (River Indus) 72.235751 E 17 Jalala drain 34.331657 N 4 - 32 - 50 - 12 05 99 3.55 71.900840 E 18 Fazalabad 34.281163 N 4 - 37 - 41 - 07 03 88 3.15 drain 71.874189 E Total 204 765 412 796 97 308 209 2791

% 7.31 27.41 14.76 28.52 3.48 11.04 7.49

3741 Khan et al.

Fig. 13. Indian Peacock Softshell Turtle (Nilssonia hurum).

Fig. 14. IndianNarrow-headed Softshell Turtle (Chitra indica). 3742 Canadian Journal of Pure and Applied Sciences

Fig. 15. Indian Flapshell Turtle (Lissemys punctata andersoni).

Fig. 16. Indian Roofed Turtle (Pangshura tectum). 3743 Khan et al.

Fig. 17. Brown Roofed Turtle (Pangshura smithii).

Fig. 18. Crowned River Turtle (Hardella thurjii). 3744 Canadian Journal of Pure and Applied Sciences

Based on our results, the occurrence of Lissemys Khan, 2014; Khan et al., 2015). Another study, punctata and Nilssonia gangetica was recorded to be Akber et al. (2006) reported all the eight species from common with 28.52% and 27.41% whereas, Punjab province. According to them, Pangshura Nilssonia hurum and Pangshura smithii were smithii and Pangshura tectum were abundant, where recorded as less common with 14.76% and 11.04%, as Hardella thurjii and Chitra india were rare at respectively. Chitra indica (7.31%) and Pangshura different localities of Punjab province of Pakistan. tectum (7.49%) were recorded as scarce. Hardella thurjii was recorded as rare with 3.48%. Lissemys Khan et al. (2015) conducted a study in four districts punctata (28.52%) and Nilssonia gangetica (27.41%) of Sindh province and recorded all the eight species. were common in all the eighteen sites sampled, They reported four species from Badin district and followed by Pangshura smithii found in sixteen sites six species from each of Sukkur, Thatta and Sanghar out of eighteen. The largest numbers and species districts of Sindh. diversity were recorded at River Jindi (11.93% of all captures) having seven different species, followed by In the present study, seven species of freshwater Sardaryab (A distributor of River Kabul) (9.67%) and turtles were recorded in Peshawar division viz. Khyali (River Swat) (8.89%) having all seven Peshawar, Charsadda and Nowshera districts, while species. The reason was that these water bodies have in Mardan district (Mardan Division) only four greater water capacity (Figs. 19-21). species, namely Lissemys punctata and N. gangetica, Pangshura smithii and Pangshura tectum were Lissemys punctata is the most abundant species, found, as we have studied only two sites in Mardan probably because it likes shallow streams, stagnant because Peshawar Division (Peshawar, Charsadda waters of rivers, marshes, ponds, lakes, and often and Nowshera districts) are rich in aquatic resources extends into sewage systems of metropolitan cities, as main rivers and streams are passing in this division as previously reported by Minton (1966). Taking of the Khyber Pakhtunkhwa. Charsadda and together, our data indicate collectively that Lissemys Nowshera districts of Peshawar division have more punctata has a healthy population and is found in water resources and that is the reason that these two nearly all sites in Peshawar Valley that surveyed. The districts have been adversely affected from flood in second-most abundant species is Nilssonia gangetica the past. which has large populations at the surveyed sites. Mehmood et al. (2012) conducted the study in the Every year, millions of freshwater turtles are Korang River of Islamabad and reported that consumed through Asian food markets. Presently, Lissemys punctata was the most abundant species, several species of turtle are in decline. Indian contributing up to 56% of the total turtles by Peacock Softshell Turtle (Nilssonia hurum) is traded numbers. Lissemys punctata were 30%, while in East Asian markets at volumes of 60 to 80 tons per Pangshura smithii was recorded as least abundant week (IUCN, 2015). (08%) during their study. The present study shows the same results and confirms earlier studies. In Peshawar valley, we noticed that there is lack of knowledge on conservation of wildlife, including In a recent study, Khan et al. (2015) reported the terrapins, within local communities. According to distribution of all the eight species from the district of them, terrapins were harvested a few years ago to the Dera Ismail Khan of Khyber Pakhtunkhwa province, point that they have been nearly exterminated. another study, Noureen (2007) also observed all species in Dera Ismail Khan of KPK. Nonetheless, a population persists here, which indicate that terrapins have recovered from harvest During the present study, seven species were within a short period of time. recorded in the valley of Peshawar, while Geoclemys hamiltonii was not recorded in the valley (Safi and

3745 Khan et al.

Fig. 19. Population status and distribution of Freshwater turtles in Peshawar Valley.

3746 Canadian Journal of Pure and Applied Sciences

3747 Khan et al.

Fig. 20. A - D, Distribution and population status of Freshwater turtles in four districts of Peshawar Valley.

Fig. 21. Population status of Freshwater turtle species in Peshawar Valley. 3748 Canadian Journal of Pure and Applied Sciences

Fig. 22. Some of the Equipments used for turtle poaching.

Fig. 23. Turtles captured through net.

During the study, we observed the following North-West Frontier Province Wildlife (Protection, anthropogenic threats to turtle population (Figs. 22 and Preservation, Conservation and Management) Act, 1975. 23): 1. The foremost threat to freshwater turtles especially is Due to this factor, poaching and capturing of turtles in a uncontrolled poaching and poor implementation of the huge number is common. 3749 Khan et al.

2. Illegal trade for consumption, traditional Chinese 3. Department of Wildlife KPK and Department of medicine and pet trade is in practice. Fisheries should control poaching of turtles and their mortality in fishing nets. 3. Habitat destruction such as damming and channeling of rivers, logging, slash and burn agriculture has been taking 4. Turtle farming practices should be initiated to reduce place. the hunting pressure.

4. Natural habitat loss is one of the prime threats to 5. Awareness should be created among the local masses freshwater turtles as during the Monsoon season (July to about the conservation and importance of biodiversity September), rivers overflow, and carry turtles far into the including turtles. valley, when the water recedes, most of them cannot find their way back. Often, wandering turtles fall in to the REFERENCES hands of vandals who may pelt them with stones for fun. Akbar, M., Hassan, MM. and Nisa, Z. 2006. Distribution 5. Urbanization and development of road networks along of freshwater turtles in Punjab, Pakistan. Caspian Journal the water resources has also badly affected the overall of Environmental Sciences. 4(2):142-146. distribution of turtles. Azam, MM. and Saeed, K. 2011. Abundance and 6. Many turtles have been captured by fishermen during distribution of freshwater turtles at Guddu and Taunsa regular fishing practices. Accidental killings of turtles are barrages and Head Punjnad. Records of the Zoological also common via capture in nets, and sometimes, they Survey of Pakistan. pp14. have been killed by fishermen for protection of their fishes, as turtles are considered a predator of fish. Baig, KJ. 2006. Environmental baseline survey and monitoring of Taunsa Barrage: emergency rehabilitation 7. Some locals, especially nomadic tribes, eat turtles and and Modernization Project: a report submitted to their eggs. Zoological Science Department. Pakistan Museum of Natural History, Islamabad. pp22. 8. Stray dogs, cats, crows and kites were observed wandering extensively during canal closure in search of Khan, MS. 2003. Uptodate checklist of amphibians and food. These animals eat the eggs of terrapins, hatchlings reptiles of Pakistan. J. Nat. Hist. Wildl. 2:11-7. and turtles. Khan, MS. 2004. Annotated Checklist of Amphibians and 9. De siltation of canals is a major cause of killing of Reptiles of Pakistan. Asiatic Herpetological Research. turtles during hibernation because hibernated turtles have 10:191-201. been carried from their natural habitat along with the silt which leads to high mortality. Khan, MS. 2015. Status and distribution of freshwater turtles of Pakistan. Bulletin of the Chicago Herpetological 10. During the closures of canals, turtles are affected due Society. 50(4):51-53. to shortage of water as well as scarcity of food resources. Khan, MZ., Ghalib, SA., Siddiqui, S., Tanveer, TF., 11. Nesting sites of freshwater turtles are unprotected. Farooq, RY., Yasmeen, G, Abbas, D. and Zehra, A. 2012. Current Status and Distribution of Reptiles of 12. Fishermen use various harmful and unsustainable Sindh. Journal of Basic and Applied Sciences. 8(1):26-34. techniques, such as dynamites, electro fishing and DOI: http://dx.doi.org/10.6000/1927 5129.2012.08.01.05 pesticides for fishing. Khan, MZ. Safi, A., Farina, F. Hashmi,‐ MUA. Hussain, 13. There is lack of awareness about the role of turtles in B., Siddiqui, S. and Ghalib, SA. 2015. An evaluation of ecosystem maintenance. distribution, status and abundance of freshwater turtles in the selected areas of Sindh and Khyber Pakhtunkhwa Priority Actions provinces of Pakistan. Canadian Journal of Pure and Applied Sciences. 9(1):3201-3219. 1. Habitat destruction, harmful and unsustainable fishing techniques may be avoided. Lovich, JE. 1994. In Biological diversity: Problem and Challenges. Eds. Majumdar, SK., Brenner, JF., Lovich, 2. The legislation banning the trade in turtles needs to be JE., Schalles, JF. and Miller, EW. Pennsylvania Academy implemented. of Science, Easton, PA, USA. 381-391. 3750 Canadian Journal of Pure and Applied Sciences

Minton, SA. Jr. 1966. A Contribution to the Herpetology of West Pakistan. Bulletin of the American Museum of Natural History. 134:29-184.

Mehmood, T., Siddiq, MK., Rais, M. and Nadeem, MS. 2012. Distribution and relative abundance of freshwater turtles in Korang River Islamabad-Rawalpindi, Pakistan. Pakistan Journal of Zoology. 44(3):889-893.

Noureen, U., Khan, A. and Arshad, M. 2012. Exploring illegal trade in freshwater turtles of Pakistan. Records of the Zoological Survey of Pakistan. 21:19-24.

Noureen, U. 2007. A Preliminary visit to Dera Ismail Khan to assess the status of freshwater turtles of Pakistan. (unpublished report). Pakistan Wetland Program, Sindh, Pakistan.pp23.

Safi, A. and Khan, MZ. 2014. Distribution and current population of freshwater turtles of District Charsadda of Khyber Pakhtunkhwa, Pakistan. The Journal of Zoology Studies. 1(4):31-38.

Shah, N. 1996. Wildlife trade in Sindh, A report published by WWF-Pakistan, Lahore for TRAFFIC International. pp57.

Suwelo, IS. 2001. The threatened species of Indonesian tortoises, terrapins and turtles. Tiperpaper. 28(2):11-13.

The World Conservation Union. 2015. IUCN Red List of Threatened Species - 2015-4. http://dx.doi.org/10.2305/IUCN.UK.2000.RLTS.T39619 A10251753.en. accessed on December 6, 2015.

Thompson, M. 1993. Hypothetical considerations of the biomass of chelid tortoises in the River Murray and the possible influences of predation by introduced foxes. In: Herpetology in Australia: a diverse discipline. Eds. Lunney, D. and Ayers, D. Transactions of the Royal Zoological Society of New South Wales, Chipping Norton, Australia.

Walters, O. 2000. A study of hunting and trade of freshwater turtles and tortoises at Danau Sentarum. Borneo Research Bulletin. 31:323-335.

Zuberi, B. 2009. Pakistani turtles in danger. All things Pakistan.www.solar-arid.org updated 25 Feb. 2007 and accessed at 30 June 2009.

Received: Nov 26, 2015; Revised: Dec 17, 2015; Accepted: Dec 22, 2015

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AN EVALUATION OF DISTRIBUTION, STATUS AND ABUNDANCE OF FRESHWATER TURTLES IN THE SELECTED AREAS OF SINDH AND KHYBER PAKHTUNKHWA PROVINCES OF PAKISTAN

M Zaheer Khan1, *Amtyaz Safi1, Farina Fatima2, Syed Ali Ghalib1, M Usman Ali Hashmi1, Iqbal Saeed Khan1, Saima Siddiqui1, Afsheen Zehra1 and Babar Hussain3 1Wildlife Section, Department of Zoology, University of Karachi, Karachi-75270 21372 Freeport Drive, Mississauga, ONT L5C 1S6, Canada 3The World Conservation Union (IUCN), 1 Bath Island Road, Karachi.

ABSTRACT

In the present work, studies on the distribution and status of freshwater turtles were conducted in Charsadda, Peshawar, Nowshera and Dera Ismail Khan Districts of Khyber Pakhtunkhwa (KPK) province, and Thatta, Badin, Sanghar and Sukkur districts of Sindh province. Eight species - Lissemys punctata, Pangshura smithii, Pangshura tectum, Chitra indica, Nilssonia gangeticus, Nilssonia hurum, Hardella thurjii, and Geoclemys hamiltonii were recorded. In Sindh, Geoclemys hamiltonii was recorded as rare in Badin, Sanghar and Sukkur districts, while other species were abundant, common or uncommon. Pangshura tectum was recorded only from Sukkur district while Chitra indica was recorded in all the four selected districts of Sindh. Geoclemys hamiltonii was recorded only in D.I. Khan district of KPK. Lissemys punctata was the most abundant and most widely distributed species in Khyber Pakhtunkhwa. Population of freshwater turtles in Sindh is much higher than that in Khyber Pakhtunkhwa. Currently, due to habitat destruction, eutrophication, agricultural farming and other anthropogenic activities, population of Geoclemys hamiltonii has also decreased in Sindh.

Keywords: Pakistan, freshwater turtles, distribution, status.

The freshwater resources of Pakistan are dominated by INTRODUCTION the Indus River system, which serves as drainage basin for Himalayas. Most of wetlands support the resident and Globally, turtles are among the endangered of the major migratory birds, fish fauna and aquatic vegetation. Due to groups of vertebrates, surpassing birds, mammals, several anthropogenic activities to cater the needs of cartilaginous and bony fishes, and amphibians. According growing population, the degradation of freshwater to the current IUCN 2013 Red List, 135 turtle species are ecosystem by a variety of stressors has increased officially regarded as globally Threatened [(Critically exponentially. As a result, many ecosystems are in need Endangered (CR), Endangered (EN), or Vulnerable of some drastic corrective restoration. (VU)]. Of the 335 total species of turtles and tortoises, 107 (31.9%) are CR or EN, 167 (49.9%) are Threatened Turtles are represented in Pakistan by 05 families, 13 (CR, EN, or VU), and 175 (52.2%) are threatened or genera and 15 species (Khan, 2006). The freshwater turtle extinct (van Dijk et al., 2014). fauna of Pakistan is entirely Oriental at both the generic and species levels (Table 1). Pakistan is a man’s carved northwestern political division of Indo-Pakistan subcontinent and not a natural geological There are 02 families, 06 genera and 08 species of entity. Its varied topography and bioclimate are reflected freshwater turtles found in Pakistan, namely in the diversity of its soil, climates, habitats, flora and Geoemydidae which consists of hardshelled turtles viz fauna (Khan, 1980; Mufti et al., 1997). Around 167 Spotted Pond turtle (Geoclemys hamiltonii), Crowned reptile species have been recorded from Pakistan river turtle (Hardella thurjii), Brown roofed turtle (Auffenberg and Khan, 1991; Ghalib et al., 1976; (Pangshura smithii), and Indian roofed turtle (Pangshura Rehman and Iffat, 1997). As many as 105 species have tectum) and the second, Trionychidae which comprises of been recorded from Sindh (Khan et al., 2012). softshell turtles viz. Indian narrow-headed soft-shell turtle (Chitra indica), Indian soft-shell turtle (Nilssonia *Corresponding author e-mail: [email protected] gangeticus), Indian peacock soft-shell turtle (Nilssonia 3202 Canadian Journal of Pure and Applied Sciences

Fig. 1. Map of Pakistan (Showing study areas in Sindh and KPK). hurum) and Indian flapshell turtle (Lissemys punctata COUNTING METHODS andersonii) (Azam and Saeed, 2011; Noureen, 2007; A. DIRECT COUNTING Noureen et al., 2012; Safi and Khan, 2014). 1. Habitat Searching /Transact Method At each site several hours search was carried out to detect In Pakistan, rather nominal scientific work has been as many turtles as possible with in a circular central zone reported on the status and distribution of freshwater along the wetlands, such as lakes, ponds, marshes, water turtles mainly concentrated in Sindh and KPK provinces. reservoirs, canals and rivers, etc. This searching consisted The main objective of this study was to determine the of approximately 20 ha within a 250 meter radius of the population distribution, status and abundance of observation/ sampling points. At first, the suitable place freshwater turtle species in Sindh and Khyber with suitable habitat was chosen. Nearly 1 sq. km. area Pakhtunkhwa provinces, particularly in the districts rich was selected for the study to observe the surface of in wetlands which potentially provide habitats for turtles. habitat. The turtles were active both in the day as well as at night, some of turtles were found sitting on partly MATERIALS AND METHODS submerged logs, larger stones and even on mudflats by the side of water, while some were seen moving or resting After baseline studies, Thatta, Badin, Sanghar and Sukkur just near their shelters and they became alert to see the districts were selected as study areas in Sindh province, observers and some of them ran away very fast and dived while Charsadda, Peshawar, Nowshera and Dera Ismail into the water or lost in the mud underwater. Species were Khan districts were selected in Khyber Pakhtunkhwa counted and identified in the field. In this way, several km province (Figs. 1, 2, 3). Several survey techniques were of study areas were surveyed and finally the population of employed for observation and census of turtles. During different species of turtle was estimated per square km. each visit to the four study areas in each province, the Their exact locations and home ranges were recorded by population of each species of turtle was recorded. GPS, so that where any observer and biologist or Identification of the species in the field was carried out naturalist, comes for study they can easily locate the place with the help of published literature. where the recorded or reported species are found. Khan et al. 3203

Fig. 2. Study areas in Sindh "Thatta, Badin, Sanghar and Sukkur districts". 1. Khipro Lake, 2. Nara Canal, 3. Bakar, 4. Gujri, 5. Sinjhoro, 6. Ithpar Lake, 7. Soonhari Lake, 8. Sadhori lake, 9. Mehmood Wari, 10. Golarchi, 11. Phoosna Lake, 12. Matchari Dhand, 13. Tando Bago, 14. Shaikh Kheerio Peer, 15. Hadero Lake, 16. Keenjhar Lake, 17. Karo Lake, 18. Mehboob Shah Lake, 19. Kharajo, 20. Nara Canal, 21. Rohri Canal, 22. K.F. Feeder, 23. Mirwa Canal, 24. Khirther Canal, 25. Dadu Canal 26. Rice Canal.

Similarly night survey was done with the help of search making observations while travelling from one end to the lights and torches. other, and the same route was followed on the return trip. In this way, 6 km round trip was covered. As soon as the 2. Capture through Nets species was sighted, the time, locations and habitat types Some species of small turtles were captured by using nets, were recorded. such as cast net. It was done in small area and in this way, most of the lakes were surveyed. 4. Incidental Sightings Incidental sighting is also helpful to determine the 3. Boat Surveys presence and population status of the species. In this way Surveys of freshwater turtles in river, large lakes and number of species, date, time, location and habitat type water reservoirs were made by using fishing boats and were recorded. 3204 Canadian Journal of Pure and Applied Sciences

Fig. 3. Study areas in KPK (Charsadda, Peshawar, Nowshera and DI Khan).

5. Basking Behavior Irrigation Department and other members of local In winter, the temperature of the water becomes very low. community of different villages. Due to cooler weather and cold water, this cold blooded reptile avoids living in water and so they come outside the 2. Presence of Signs like fecal pellets, tracks, den or lake to enjoy sunshine to keep them warm. Thus, counting tunnels (egg laying excretion) of the turtle species becomes very easy at particular area Evidences from the impressions of fingers or foot prints, during this season. or tail, presence of fecal pellets, tracks and existence of tunnels (egg laying excretion) are helpful for finding the B. INDIRECT COUNTING METHODS existence, range and rough population of the species. 1. Information from different sources Information was collected from the staff of Wildlife The study was based mainly on direct observation; Department, local fishermen, boatmen, field staff of enumerations depended on basking and floating turtles, Khan et al. 3205

Status of Freshwater turtles of Sindh

30 25 20

% 15 10 5 0 L. C. indica N. hurum N. P. smithii P. tecta H. thurjii G. punctacta gangeticus hamiltonii Species

Fig. 4. Status of different species of Freshwater turtles in Sindh province.

Status of Freshwater turtles of KPK

30 25 20

% 15 10 5 0 L. C. indica N. hurum N. P. smithii P. tecta H. thurjii G. punctacta gangeticus hamiltonii Species

Fig. 5. Status of different species of Freshwater turtles in KPK province. calculated by the following formula (Mehmood et al., Thatta District 2012). In Thatta district, six species of freshwater turtles were P = AZ observed, Lissemys punctata (Webb, 1980a) and 2YX Pangshura smithii (Gray, 1863), were abundant. Chitra P-population A- total area Z-number observed indica (Gray, 1831), Nilssonia gangeticus (Cuvier, 1825) Y-average flushing distance X-length of strip and Nilssonia hurum (Gray, 1831) were common, Hardella thurjii (Gray, 1831) was less common (Table 2, RESULTS AND DISCUSSION Figs. 8 - 11, 13 and 15). These species were recorded in good numbers at Hadero Lake and Ghulamullah Canal. Sindh Province According to the data of one year, C. indica was recorded In the selected areas of Sindh province, following results as 21%, P. smithi as 22.2%, L. punctata as 26.52%, H. of the population of each species of freshwater turtles thurjii as 8.54%, N. gangeticus as 8.72% and N. hurum as were documented: 12.68% (Table 2).

3206 Canadian Journal of Pure and Applied Sciences

Table 1. IUCN and CITES Status of Freshwater Turtles of Pakistan.

Family Species IUCN Status CITES Status Geoemydidae Geoclemys hamiltonii Vulnerable Appendix I Geoemydidae Hardella thurjii Vulnerable Appendix II Geoemydidae Pangshura smithii Near threatened Appendix II Geoemydidae Pangshura tectum Low risk Appendix I Trionychidae Chitra indica Endangered Appendix II Trionychidae Nilssonia gangeticus Vulnerable Appendix I Trionychidae Nilssonia hurum Vulnerable Appendix I Trionychidae Lissemys punctata Least concern Non CITES

Table 2. Population Distribution of Freshwater Turtles of Thatta District.

Approx Observed Species S. Location surveyed Chitra Pangshura Lessemys Hardella Nilssonia Nilssonia No Total % area (km) indica smithii punctata thurjii gangeticus hurum 1 Hadero Lake 4 70 80 92 30 32 52 356 15.8 2 Haleji Lake 4 62 74 83 21 25 60 325 14.4 3 Keenjhar 4 55 64 89 30 20 40 298 13.2 Lake 4 Mahboob 4 51 70 77 20 20 33 271 12 Shah Lake 5 Kharajo 4 66 69 71 22 22 31 281 12.5 Lake 6 Karo Lake 4 48 57 69 29 33 38 274 12 7 Ghulam 4 125 87 115 40 44 31 442 19.6 ullah Canal Total 477 501 596 192 196 285 2247 % 21 22.2 26.52 8.54 8.72 12.68

Table 3. Population Distribution of Freshwater Turtles of Badin District.

Approx Observed species S. Location surveyed Nilssonia Chitra Lissemys Geoclemys No. Total % area (km) hurum indica punctata hamiltonii 1 Golarchi (Jaffar ali Lake) 5 28 71 75 07 181 26 2 Phoosna Lake 5 39 62 60 06 167 23.9 3 Charwo and Khanjo Lake 5 26 56 53 05 140 20.1 4 Matchary Dhand 5 20 48 37 08 103 16.2 5 Shaikh Kerrio Peer 5 14 44 33 04 95 13.46 Total 127 281 258 30 696 % 18 40 37 4.31

Badin District Hardella thurjii was less common, while Geoclemys In this area, four species were recorded, Lissemys hamiltoniii was rare (Table 4, Figs. 8, 10 – 13 and 15). C. punctata and Chitra indica were abundant, Nilssonia indica was recorded as 19.4%, P. smithii as 19.08 %, L. hurum as less common, while Geoclemys hamiltonii as punctata as 23.33%, H. thurjii as 14.68 %, N. gangeticus rare (Table 3, Figs. 8-10 and 12). C. indica was recorded as 20.2% and G. hamiltonii as 3.20% (Table 4). as 40%, L. punctata as 37%, G. hamiltonii as 4.31%, and N. hurum as 18% (Table 3). Sukkur District Studies were conducted at Sukkur barrage on the right Sanghar District and left bank of Indus River on the right bank area of In Sanghar district, six species were recorded. Lissemys Sukkur Barrage, six species were recorded, Chitra indica punctata was abundant, Nilssonia gangeticus, Pangshura was to be abundant, Pangshura tectum, Pangshura smithi smithii and Chitra indica were common. They were and Nilssonia gangeticus were common and Hardella highly populated in Chotiari and Bakar reservoir areas. thurjii was less common, while Geoclemys hamiltonii was Khan et al. 3207

Table 4. Population Distribution of Freshwater Turtles of Sanghar District.

Approx Observed Species S. Location surveyed Chitra Nilssonia Pangshura Hardella Geoclemys Lissemys Total % No. area (km) indica gangeticus smithii thurjii hamiltonii punctcta 1 Khipro 5 71 74 63 45 10 80 343 12.7 Lake 2 Nara Canal 5 64 76 69 50 27 83 369 13.7 3 Sanghriaro Lake 5 80 85 88 61 31 89 434 16.17 (Chotiari) 4 Bakar Lake 5 57 60 52 40 07 60 276 10.2 5 Soonhari 5 41 52 44 47 09 67 260 9.69 Lake 6 Gujri 5 60 51 47 33 01 71 263 9.80 7 Ithpar 5 45 58 38 32 01 60 234 8.72 8 Sadhori Lake 5 53 39 50 46 00 56 244 9 9 Mehmood- -wari 5 52 47 61 40 00 60 260 10.67 Dhand Total 523 542 512 394 86 626 2683 % 19.4 20.20 19.08 14.68 3.20 23.33

Status of Freshwater turtles in different areas of Sindh

45 40 L. punctacta 35 C. indica 30 N. hurum 25 N. gangeticus % 20 P. smithii 15 P. tecta 10 H. thurjii 5 G. hamiltonii 0 Thatta Badin Sanghar Right bank of Left bank of Sukkur Barrage Sukkur Barrage Districts

Fig. 6. Distribution and status of Freshwater turtles in different districts of Sindh. found to be rare (Table 5, Figs. 8 and 11 - 15). C. indica Khyber Pakhtunkhwa Province was recorded 41.66%, P. smithii as 13.63%, H. thurjii as In the selected areas of Khyber Pakhtunkhwa province, 8.33%, N. gangeticus as 12.37%, P. tectum as 20.45%, the population of each species of freshwater turtles was and G. hamiltonii as 3.53% (Table 5). recorded:

On the Left bank of Sukkur barrage, six species were Charsadda District recorded, Chitra indica was abundant, while Nilssonia In Charsadda District, seven species of freshwater turtles gangeticus, Pangshura tectum, Pangshura smithii and were observed, Lissemys punctata (Webb, 1980a), Hardella thurjii were common. Geoclemys hamiltonii was Nilssonia gangeticus (Cuvier, 1825) and Nilssonia hurum rare (Table 6, Figs. 8 and 11 - 15). C. indica was recorded (Gray, 1831) were abundant. Pangshura smithii (Gray, 30.99%, P. smithii as 13.30%, H. thurjii as 17.04%, N. 1863) and Chitra indica (Gray, 1831), were common, gangeticus as 15.95%, P. tectum as 14.85%, and G. Hardella thurjii (Gray, 1831) and Pangshura tectum hamiltonii as 7.83% (Table 6). P. tectum was recorded (Gray, 1873) were less common (Table 7, Figs. 8 – 11 and only from the Indus in Sindh in this study area. 13 - 15). These species were recorded in good numbers in 3208 Canadian Journal of Pure and Applied Sciences

Table 5. Population Distribution of Freshwater Turtles in the Rigth Bank in Indus, Sukkur District.

Approx Observed Species S. Location surveyed Chitra Nilssonia Pangshura Pangshura Hardella Geoclemys No. Total % area (km) indica gangeticus smithii tecta thurjii hamiltonii 1 Khirthar 6 52 17 19 20 10 08 126 31.81 Canal 2 Dadu 6 60 13 18 28 11 04 134 33.83 Canal 3 Rice 6 53 19 17 33 12 02 136 34.34 Canal Total 165 49 54 81 33 14 396 % 41.66 12.37 13.63 20.45 8.33 3.53

Table 6. Population Distribution of Freshwater Turtles in the Left Bank of Indus, Sukkur District.

S. Approx Observed Species Location surveyed Chitra Nilssonia Pangshura Pangshura Hardella Geoclemys Total % No. area (km) indica gangeticus smithi tecta thurjii hamiltonii 1 Nara 6 80 53 35 31 41 25 265 24.1 Canal 2 Rohri 6 90 52 41 42 50 21 296 26.9 Canal 3 K. F. 6 86 30 40 50 52 23 281 25.6 Feeder 4 Mirwah 6 84 40 30 40 44 17 255 23.2 Canal Total 340 175 146 163 187 86 1097 % 30.99 15.95 13.30 14.85 17.04 7.83

Status of freshwater turtles in different districts of KPK

40 35 L. punctacta 30 C. indica 25 N. hurum N. gangeticus

% 20 P. smithii 15 P. tecta 10 H. thurjii 5 G. hamiltonii 0 Charsadda Peshawar Nowshera D. I. Khan Districts

Fig. 7. Distribution and status of Freshwater turtles in different districts of KPK.

River Jindi, River Swat (Khyali) and River Kabul 15.64%, N. gangeticus as 22.09%, and A. hurum as (Sardaryab). According to the data of one year, C. indica 18.40% (Table 8). was recorded as 12.99%, P. smithii as 10.69%, P. tectum as 5.28%, L. punctata as 29.50%, H. thurjii as 3.79%, N. Nowshera District gangeticus as 18.54%, N. hurum as 19.22% (Table 7). Six species were recorded in the Nowshera District. Lissemys punctata was abundant, N. gangeticus, N. Peshawar District hurum, P. smithii and P. tectum were common, while H. In this area, five species were recorded, Lissemys thurjii was less common (Table 9, Figs. 9-11 and 13-15). punctata was abundant, N. hurum, N. gangeticus and P. P. tectum was recorded as 13.59%, P. smithii as 14.15%, smithii were common, while Chitra indica was less L. punctata as 17.88%, N. hurum as 30.35%, A. common (Table 8, Figs. 8 – 11 and 15). C. indica was gangeticus as 17.88% and H. thurjii as 6.15% recorded as 9.82%, L. punctata as 34.05%, P. smithii as (Table 9). Khan et al. 3209

Fig. 8. Indian narrow-headed soft-shell turtle (Chitra indica).

Fig. 9. Indian peacock soft-shell turtle (Nilssonia hurum).

Dera Ismail Khan District Habitat destruction associated with human population In this district, seven species were recorded, N. increase and several human activities may very well be a gangeticus was found to be most abundant, L. punctata, factor in Pakistan. The status of freshwater turtle species N. hurum and C. indica were common, while G. has decreased, due to hunting, habitat destruction, hamiltonii, P. smithii and H. thurjii were less common, fragmentation, agricultural and several anthropogenic Geoclemys hamiltonii was observed only in this area of actions. In Sindh, due to habitat destruction, KPK (Table 10, Figs. 8 – 13 and 15). C. indica was eutrophication, use of chemical fertilizers, over grazing of recorded 12.52%, P. smithii as 7.92%, H. thurjii as aquatic vegetation and paucity of water, the population of 6.08%, N. gangeticus as 37.94%, N. hurum as 15.84%, L. Geoclemys hamiltonii (Spotted Pond Turtle) has punctata as 11.23% and G. hamiltonii as 8.47% (Table decreased as during the present study, this species was 10). recorded as rare in Badin, Sanghar and Sukkur districts, 3210 Canadian Journal of Pure and Applied Sciences

Fig. 10. Indian flap shell turtle (Lissemys punctata andersonii).

Fig. 11. Indian soft-shell turtle (Nilssonia gangeticus). while in Khyber Pakhtunkhwa, this species was recorded thurjii, Chitra indica and Lissemys punctata were only in Dera Ismail Khan district (Fig. 6 and 7). recorded. While, Pangshura smithii and Chitra indica were observed as abundant in various parts of the study area During a field survey on distribution and status of (Azam et al., 2005). Another study Akber et al. (2006) freshwater turtles conducted in 2003, the Indus River at reported the distribution of fresh water turtles in Punjab, Sukkur Barrage, Guddu Barrage, Jamaldin Wali and pond Pakistan. A total of 3528 specimens of freshwater turtles areas adjacent to Kandhkot, six species Aspideretes belonging to the species Pangshura smithii, P. tectum, gangeticus, Pangshura smithii, P. tectum, Hardella Geoclemys hamiltonii, Hardella thurjii, Nilssonia Khan et al. 3211

Fig. 12. Spotted pond turtle (Geoclemys hamiltonii).

Fig. 13. Crowned river turtle (Hardella thurjii). gangeticus, Nilssonia hurum, Chitra indica, and Lissemys whereas, Hardella thurjii (0.88%) and Chitra indica punctata were identified. Pangshura smithii (43.62%) (0.54%) were rare. and P. tectum (42.06%) had abundant population status 3212 Canadian Journal of Pure and Applied Sciences

Fig. 14. Indian roofed turtle (Pangshura tecta).

Fig. 15. Brown roofed turtle (Pangshura smithii).

Freshwater turtles have served as an important food food. During our present study, it was also observed that resource in tropical and subtropical of many Asian Soft-shell turtles are targeted by local communities countries. However, several countries of our region have because parts of these turtles are in demand in the Chinese made few attempts for conservation asnd management of international markets and used in traditional Chinese the resource. In Asian countries, the freshwater turtles are medicines. Some freshwater turtle traders contact the little exploited for jewellery, tourist souvenirs and leather. local communities and offer them good amounts of They are mostly utilized to some extent as medicine and money to start the business and adopt it as their work. Khan et al. 3213

Fig. 16. Local community activity for trading.

Fig. 17. Trading of some body parts of Freshwater Turtles.

Local techniques and instruments are used for turtle to Karachi, from where turtles and their body parts are capturing (Figs. 16-17). Some causes of population exported to other countries such as Hong Kong, China, declines were also recorded which include large scale South Korea and Vietnam (Noureen, 2009; Noureen et illegal capturing of turtles for export from Chashma al., 2012). Barrage, Taunsa Barrage, Head Qadirabad, Head Rasool, Head Trimmu, Head Balloki and Chiniot area (Azam et The fishermen also capture turtles during fishing with nets al., 2005). In Sindh, the freshwater turtle trade is destined and angling, some turtles are accidentally killed with nets, 3214 Canadian Journal of Pure and Applied Sciences

Table 7. Population Distribution of Freshwater Turtles in Charsadda District (KPK).

Approx S. Name of locality L. C. N. N. P. P. H. surveyed Total % No. (water Body) punctata indica hurum gangetica tecta smithii thurjii area (Km) 1. Kashmalo Drain 3 20 - 06 13 - 09 07 55 7.44 (TurangZai) 2. Dub Drain 3 48 17 21 27 - 04 - 117 15.83 (Mardan road) 3. Hisara Drain 3 36 13 24 37 - 07 - 117 15.83 (Near Kashmir Kalay) 4. Branch No. 6 3 06 - - 05 07 16 - 34 4.60 from Main canal of Lower Swat (Behlola) 5. River Swat 3 39 27 09 17 13 17 05 127 17.19 (Khyali) Near Tarnab 6. River Jindi 3 28 16 53 19 - 08 09 133 18.00 (Nimouri) 7. River Kabul 3 41 23 29 19 19 18 07 156 21.11 (Sardaryab) Total 218 96 142 137 39 79 28 739 % 29.50 12.99 19.22 18.54 5.28 10.69 3.79

Table 8. Population Distribution of Freshwater Turtles in Peshawar District (KPK).

Approx S. Name of locality L. C. N. N. P. surveyed Total % No. (water Body) punctata indica hurum gangetica smithii area (Km) 1. Naguman (River 2 24 16 18 25 26 109 33.44 Kabul) 2. Shaalam 2 36 16 21 18 06 97 29.75 (River Kabul) 3. River Budhni 2 23 - 09 21 - 53 16.26 4. River Bara 2 22 - 12 - 19 53 16.26 5. Sheikh canal 2 06 - - 08 - 14 4.29 (Kabul River Canal) Total 111 32 60 72 51 326 % 34.05 9.82 18.40 22.09 15.64

whereas, some fisherman consider them the enemies of destruction of habitat Chitra indica species has become fish, therefore, they kill the captured turtles to save their rare everywhere and population seems to be declining. fish. In our study, 08 dead Pangshura smithi, 17 Nilssonia Habitat destruction is the major threat, as the activities, gangeticus, 11 Chitra indica and 05 N. hurum were such as road and building construction require a large recorded at Charsadda, Peshawar, Thatta, Sukkur and amount of sand to be removed. It represents another Sanghar districts. During the present study, illegal problem of population decline, by eliminating or capturing mostly from Thatta District (Hadero Lake, degrading the quality of sand at beach nesting habitats. Haleji Lake, Karo Lake and Mahboob Shah Lake), from Chitra indica is primarily found in large rivers with sandy Sanghar district (Chotiari Wetland complex), and Badin or muddy bottom (Das, 1995; Ernst and Barbour, 1989; District (Phoosna Lake and Shaikh Keerio Peer) was Tikader and Sharma, 1985). At present, this species is noted. abundant in Sindh but may soon be wiped out or will become rare if habitat destruction continues. In Thailand, Kitimasak et al. (2005) surveyed the distribution and population status of the Narrow Headed Reptiles have served as a food resource. Exploitation for Softshell Turtle (Chitra indica) and reported that due to food is heaviest in the tropical and sub tropical regions, Khan et al. 3215

Table 9. Population Distribution of Freshwater Turtles in Nowshera District (KPK).

Approx Observed Species S. No. Location surveyed N. N. L. P. H. P. tecta Total % area (Km) hurum gangeticus punctata smithi thurjii 1 Kheshgi (River 4 40 28 17 16 20 15 136 25.33 Kabul) 2 Hakimabad (River 4 46 25 41 22 20 11 165 30.73 Kabul) 3 Kund Park (Kabul 4 46 24 30 15 22 - 137 25.51 + Indus rivers) 4 Darwazgai (Indus 4 31 19 08 20 14 07 99 18.44 River) Total 163 96 96 73 76 33 537 % 30.35 17.88 17.88 13.59 14.15 6.15

Table 10. Population Distribution of Freshwater Turtles in Dera Ismail Khan District (KPK).

Name of Approx S. L. C. N. N. P. G. H. locality (water Surveyed Total % No. punctata indica hurum gangetica smithii hamiltonii thurjii Body) area (Km) 1. Purani kirri 4 12 22 19 45 12 19 12 141 25.97 (Chashma Right Bank Canal Plus Indus River) 2. Mela wali 4 20 05 06 11 - 03 - 4 5 8.29 3. Mianwali 4 12 13 19 39 05 09 08 105 19.34 Road (Dhap Shumali) 4. Indus View 4 04 11 21 73 09 - - 118 21.73 Road 5. Bhakar Road 4 13 17 21 38 17 15 13 134 24.68 (Kiri Juma Khan) Total 61 68 86 206 43 46 33 543 % 11.23 12.52 15.84 37.94 7.92 8.47 6.08

but also occurs in temperate areas. Of all reptiles, turtles Brown roofed turtle and Crowned river turtle, Indian soft are the most heavily exploited for human consumption shell turtle listed in Appendix are in (CITES Appendix- (Figs. 16-20). High, unsustainable levels of exploitation II), while Indian flap Shell turtle is not listed in CITES for food are directly responsible for the precarious (see Table 1). conservation status of many turtles (Klemens and Thobjarnarson, 1995). Trade volumes for freshwater Diversion of water for irrigation and the drainage of turtles and tortoises in Asia are also huge, to the level that wetlands are the key causes of the degradation of many it has threatened the survival of several species. In 2006 wetlands of Pakistan. Small wetlands created by the and 2007, during two surveys at Chatuchak market in seepage from the irrigation systems are targeted for Bangkok, Thailand, they recorded a significant trade in drainage to be used as agriculture lands, other threatened non–native CITES listed freshwater turtles and tortoises by the discharge of saline water into the wetlands, as well to be used as pets. They documented 688 individuals of as by decreasing ground water levels due to draining 19 species from different regions of the world, many of programs. The drainage programs have also caused loss which are globally threatened with extinction. Five of natural water bodies. At present, only 25% of the water species were listed on CITES Appendix I, precluding all from the Indus River actually reaches the Indus Delta. international trade, and an additional six species in Most of the lakes in Thatta and Badin districts are facing Appendix II (Nijman and Shepherd, 2007). this problem.

According to the CITES List, Spotted pond turtle, Indian Cultivation on river banks is a common practice among peacock soft shell turtle, Indian saw back turtle (CITES several areas of Pakistan that can destroy or alter turtle Appendix-I), while Narrow headed soft shell turtle, nesting sites. Continued clearing of aquatic vegetation 3216 Canadian Journal of Pure and Applied Sciences

Fig. 18. Another trading activity of local community for Freshwater Turtles. along watersheds leads to siltation, turbidity, decreased the wetland as a whole, resulting in loss of wetland productivity and increased flooding. In the present study, biodiversity (Brock et al., 2005). Many agriculture lands, according to many field observations siltation is the most especially in Sindh, face acute salinity and water logging. common problem faced by every wetland in Sindh. Due to the denudation of catchments area, the inflow of water Dogs were observed wandering during canal closure in brings with it a certain amount of silt. This inflow search of food; these dogs eat dead fishes, trapped fishes increases during the rainy season and causes siltation of and turtles in shallow waters. Dead bodies of spotted pond wetland, and presently Haleji Lake faces this problem. turtles and Indian soft-shell turtles were observed being eaten by dogs (Akber et al., 2006). In our study, it was Increasing salinity in freshwater rivers and wetlands tends also observed that the turtles were eaten by dogs in Thatta to decrease the species richness of aquatic communities of and Badin districts. Drought is also one of the important Khan et al. 3217

Fig. 19. Another trading activity of local community.

Fig. 20. Burning of seized body parts of Turtles by Wildlife Department in Peshawar (Courtesy by: Dawn news).

factors for mortality and habitat destruction of freshwater management plan. The present study revealed that Sindh turtles. province has a richer chelonian fauna as compared to Khyber Pakhtunkhwa (Tables 2-10). On the basis of our Undoubtedly over-exploitation, habitat destruction and study, three species Pangshura tectum, Geoclemys habitat alteration were recorded as common threats to all hamiltonii and Hardella thurjii were recorded as rare in species during one year study. Before the present study, KPK, and Pangshura tectum, Geoclemys hamiltonii and very less scientific data have been reported on the Nilssonia hurum in Sindh, while other species are population, distribution, status and abundance of abundant, common or less common in both the provinces. freshwater turtles in these districts of Sindh and KPK. The population status of Lissemys punctata is better than Hopefully, this study will serve as a springboard for that of other freshwater turtles of Pakistan (Figs. 4-7). further research, conservation, education and future 3218 Canadian Journal of Pure and Applied Sciences

CONCLUSION Khan, MS. 1980. Affinities and Zoogeography of herpetiles of Pakistan. Biologia. 26:113-117. It is concluded that due to habitat destruction, Khan, MS. 2006. Amphibians and Reptiles of Pakistan. eutrophication and other anthropogenic activities, the Kriegar Publishing Company, Malabar, Florida, USA. population of freshwater turtles is on the decrease. The freshwater turtles are important part of our ecosystems Kitimasak, W., Thirakhupta, K. and Boonyaratpalin, S. and need attention for their conservation and management 2005. Distribution and Population Status of the Narrow- including control over trading activities. Further studies Headed Softshell Turtles Chitra spp. in Thailand. The are needed to collect more data for preparing the Natural History Journal of Chulalongkorn University. 5 conservation and management plan for freshwater turtles (1):31- 42. in Pakistan. There is a need to increase public awareness Klemens, MW. and Thorbjarnarson, JB. 1995. Reptiles to enhance public participation in conservation activities as a food resource. Biodiversity and Conservations. particularly directed towards freshwater turtles and their 4(3):281-298. habitats. Mehmood, T., Siddiq, MK., Rais, M. and Nadeem, MS. REFERENCES 2012. Distribution and relative abundance of Freshwater turtles in Korang River Islamabad-Rawalpindi, Pakistan. Akbar, M., Mushtaq-ul-Hussan, M. and Zaib-u-Nisa. Pakistan J. Zool. 44(3): 889-893. 2006. Distribution of freshwater Turtles in Punjab. Pakistan. Caspian. J. Env. Sci. 4(2):142-146. Mufti, SA., Wood, CA. and Hasan, SA. (Eds.) 1997. Biodiversity of Pakistan. Pakistan Museum of Natural Auffenberg, W. and Khan, NA. 1991. Studies of Pakistan History, Islamabad. Reptiles. Notes on Kachuga smithi. Hamadryad. 16:25- 29. Nijman, V. and Shepherd, CR. 2007. Trade in non- native, CITES – listed, Wildlife in Asia, as exemplified Azam, MM., Fakhri, MS. and Saifullah. 2005. Some by the trade in Freshwater turtles and tortoises Observation on the distribution and abundance of (Chelonidae) in Thailand. Contribution to Zoology. 76 (3). freshwater turtles in the River of Indus. Rec. Zool. Surv. Pakistan. 16:46-51. Noureen, U. 2009. Freshwater Turtles of Pakistan: Illegal trade in Sindh: Preliminary findings of trade in Azam, MM. and Saeed, K. 2011. Abundance and Freshwater Turtle Parts. A survey report submitted to the distribution of freshwater turtles at Guddo and Taunsa Ministry of Environment’s Pakistan Wetlands barrages and Head Punjnad. Rec. Zool. Surv. Pakistan. Programme. pp. 36. Brock, MA., Nielsen, DL. and Crossle, K. 2005. Change Noureen, U., Khan, A. and Arshad, M. 2012. Exploring in biotic communities developing sediments under illegal trade in freshwater turtles of Pakistan. Rec. Zool. experimental salinity and water regimental. Freshwater Surv. Pakistan. 21:19-24. Biology. 50(8):1376-1390. Noureen, UA. 2007. Preliminary visit to Dera Ismail Cuvier, G. 1825. Rearches sur les ossomens fossils de Khan to assess the status of freshwater turtles of Pakistan quadropedes. (3rd edi.). Paris. (unpublished report). Pakistan Wetlands Program, Pakistan. 1-23. Das, I. 1995. Turtles and Tortoises of India. Bombay. Oxford University. Press. pp. 179. Rehman, H. and Iffat, F. 1997. A Revised Checklist of Ernst, CH. and Barbour, RW. 1989. Turtles of the world. Reptiles of Pakistan Records Zoological Survey of Smithsonian Institution Press, Washington, DC., USA. Pakistan. 13:63-70. pp. 313. Safi, A. and Khan, MZ. 2014. Distribution and current Gray, JE. 1831-1844. The Zoological miscellany. population status of freshwater turtles of district of London. Nos. 1-6. Charsadda of Khyber Pakhtunkhwa, Pakistan. Journal of Gray, JE. 1863. Notice of a new species of Batagaur from Zoology Studies. 1(4):31-38. northwestern. India Proc. Zool. Soc. London. 1863:253. Tikader, BK. and Sharma, RC. 1985. Handbook of Indian Ghalib, SA., Rehman, H., Iffat, F. and Hasnain, S. 1976. Testudines. The Radiant Process Private Limited, A Checklist of the Reptiles of Pakistan. Records Calcutta, India. pp156. Zoological Survey of Pakistan. 8 (1&2):37-59. Van Dijk, PP., Iverson, JB., Rhodin, AGJ., Shaffer, HB. Khan, MZ., Ghalib, SA., Siddiqui, S., Siddiqui, TF., and Bour, R. 2014. Turtles of the world. In: Annotated Farooq, RY., Yasmeen, G., Abbas, D. and Zehra, A. checklist of taxonomy, synonymy, distribution with maps, 2012. Current status and distribution of reptiles of Sindh. and conservation status. ((7th edi.). Eds. Rhodin, AGJ., J. Basic and Applied Sciences. 8 (1):26-34. Pritchard, PCH., van Dijk, PP., Saumure, RA., Buhlmann, Khan et al. 3219

KA., Iverson, JB. and Mittermeier, RA. Conservation Biology of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Monographs 5(7):000.329-479, doi:10.3854/crm.5.000. checklist.v7.2014. Webb, RG. 1980. The identily of Testudo Punctata Lacepede, 1788 (Testudines, Trionychidae). Bull. Mus. Natn. Hist. Nat., Paris. 4(2):547-557.

Received: Nov 16, 2014; Revised: Nov 28, 2014; Accepted: Dec 19, 2014

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ISSN 2348-5914 JOZS 2014; 1(4): 31-38 Distribution and current population status of freshwater turtles JOZS © 2014 of District Charsadda of Khyber Pakhtunkhwa, Pakistan Received: 19-08-2014 Accepted: 09-09-2014 Authors: Amtyaz Safi and Muhammad Zaheer Khan

Abstract

A total of 365 specimens of freshwater turtles belonging of Two Families Viz., Geoemydidae Amtyaz Safi Department of Zoology, Sir Syed (Crowned river turtle, Hardella thurjii; Brown roofed turtle, Pangshura smithii and Indian Govt. Girls College Nazimabad, roofed turtle; Pangshura tecta) and Family Trionychidae (Indian narrow-headed soft-shell Karachi-74600, Pakistan turtle, Chitra indica; Indian soft-shell turtle, Nilssonia gangetica; Indian peacock soft-shell turtle, Nilssonia hurum; and Indian Flap-shell turtle, Lissemys punctata andersonii were Muhammad Zaheer Khan Wildlife and Fisheries, identified. Lissemys punctata (30.95%) and Nilssonia gangetica (27.39%) had abundant Department of Zoology, population status, whereas, Hardella thurjii (1.36%) and Pangshura tecta (3.01%) were rare. University of Karachi, 75270, Pakistan. Spotted Pond turtle (Geoclemys hamiltonii was not recorded during the present study, as this Species had been reported by various researchers in different areas of Pakistan. The current

study investigated the distribution and abundance of freshwater turtle Species inhabiting in different water bodies of Charsadda of Khyber Pakhtunkhwa Province. Capturing of turtles for

export is a major threat to these animals. Fishermen also kill them during fishing. Canal closure, de-silting and destruction of Ecological niches are also harmful to these animals. It is

concluded that it is necessary to provide effective and immediate legal protection/Coverage to all turtle species under the Khyber Pakhtunkhwa Wildlife (Protection, Preservation and

Management) Act, 1975, Pakistan; otherwise turtle species will become extinct.

Keywords: Turtles, Distribution, Population, Charsadda, Pakistan

1. Introduction

The Order Chelonia (Testudine) contains 13 recognized Families. These include land tortoises, Freshwater turtles and Marine turtles. There are about 289 living species of turtles and

tortoises, which are found in different habitat of the World [1]. Turtles of Pakistan are divided Correspondence author: into three main categories. Amtyaz Safi Dept. of Zoology, Sir Syed Govt. Girls College Nazimabad, Karachi- Marine turtles: Green sea turtle (Chelone mydas) and Olive Ridley turtle (Lepidochelys 74600, Pakistan olivacea) are the common species of marine turtles in Pakistan. Hawkes bill turtle Tel: 0092-3212374804 E-mail: [email protected] (Eretmochelys imbricate), Logger-headed turtle (Caretta caretta) and Leatherback sea turtle (Dermochelys coriacea) are also found occasionally.

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Tortoises (Land turtles): Two Species of tortoises are and the Sindh Wildlife Department for TRAFFIC found in Pakistan; Afghan tortoise (Agrionemys International in 1996, reported turtle trade in Sindh horsfieldii) and Sindh Star tortoise (Geochelone Province [5]. elegans). In Khyber Pakhtunkhwa, commercial exploitation of Freshwater turtles (Terrapins): Two families of turtles for their body parts was introduced in the year freshwater turtles are found in Pakistan, namely 2006 [6]. Illegal turtle trade, particularly in body parts Geoemydidae which consist of Hard-shell turtles; of soft-shell species was reported by Baig [7]. Spotted Pond turtle (Geoclemys hamiltonii), Crowned river turtle (Hardella thurjii), Brown roofed turtle The Ganges Soft-shell turtle, Peacock Soft-shell turtle, (Pangshura smithii), and Indian roofed turtle Spotted Pond turtle and the Indian saw-backed turtle (Pangshura tecta) and the 2nd Family Trionychidae are included in Appendix-I, whereas, Crowned river comprises of soft-shell turtles; Indian narrow-headed turtle, Indian narrow-headed soft-shell turtle and soft-shell turtle (Chitra indica), Indian soft-shell turtle Brown roofed turtle are listed in Appendix-II of the (Nilssonia gangetica), Indian peacock soft-shell turtle Convention on International Trade in Endangered (Nilssonia hurum) and Indian flap shell turtle Species (CITES) [7, 8]. The Indian Flap shell turtle is (Lissemys punctata andersonii). These are larger in Non CITES Species in Species data base of CITES of size as compared to Hard-shell turtles. Freshwater 2014 (Table 1). turtles that are consumed, soft shell turtles are considered the best due to their low bone to bone ratio The persistence of turtles is valuable not just socially and larger proportions of cartilage and gelatinous skin. and environmentally but also for the services they This demand has made soft shell turtles the most provide to the streams and rivers. Carrion eating important components of the freshwater turtle’s trade species may reduce eutrophication. Anthropogenic in Asia [2]. disturbance to freshwater systems can change ranging behavior with subsequent alteration of key Freshwater turtles play important role in the health of demographic processes. For example, stress in aquatic ecosystem, since they are scavengers, freshwater turtles suppresses ovulation and egg herbivores and carnivores, provide dispersal production [9]. To improve conservation of freshwater mechanism for plants, clean up water resources by turtles, we need to understand how turtles respond to scavenging on dead organic matter and help to anthropogenic activities including; which structures maintain healthy populations of fish [3], Soft-shell impede turtle movement and how turtles respond to turtles are source of Traditional Chinese Medicine, and wetland draining. their shells are highly effective for purifying blood and [10] stressed that accurate knowledge about spatial cure many diseases [4]. Turtle populations are being distribution is essential for effective management in the rapidly deleted as they were not protected or conserved natural habitat. seriously by any Government department previously in Pakistan. Consequently some species populations are No research work has been conducted on freshwater becoming threatened. Pakistan is signatory to the turtles of Khyber Pakhtunkhwa Province of Pakistan, Convention on international trade in Endangered so basic data on occurrence and population distribution Species of fauna and flora (CITES) in 1976. The of different Species is not available. The objective of Government of Pakistan approved the Federal CITES this study was to determine the population distribution Law in May 2012, for effective enforcement of CITES and status of Freshwater turtles in the water bodies of legislations in Pakistan. Wildlife being a provincial Charsadda (Pakistan). subject, Khyber Pakhtunkhwa Wildlife department revised the conservation status of freshwater turtles in Since these information are vital to identify areas of 2007. freshwater turtles and pin point their threats for proper management and conservation of the freshwater turtles. In Pakistan, freshwater turtle trade was first highlighted in 1990s. An investigative study by WWF-Pakistan

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Fig 1: Map of Khyber Pakhtunkhwa Showing District of Charsadda as Study Area.

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2. Materials & Methods flipper prints of turtles. Animals found above Total 7 sites, in which 3 Rivers (River Jindi, River ground in the dry canal were identified to Swat and River Kabul) 1 irrigating canal (Branch no. 6 species and counted, whereas the animals from main Canal/Lower Swat) and 3 drain systems hibernated/buried in dried canal bed were (Dub drain, Hisara drain and Kashmalo drain) were removed from the bed, identified and counted. surveyed in the district of charsadda as shown in Table  A third method used baited hooks to capture 2, Fig. 1 & 2. turtles and was particularly good for catching The study was conducted from November 2013 to soft-shell turtles. Steel hooks were baited with August 2014 using the following procedure for intestine of poultry. After species observation and census of turtles. identification and counting, turtles were  Basking turtles were observed, directly released back in their natural habitat. counted and different species were identified  Interviews were conducted from the with the help of Binocular Minolta (10 X 50 community to obtain information about status mm). of freshwater turtles. Special identification  No turtle was found basking during severe cards were shown during interviews to cold weather conditions so drag net was used identify the species. for capturing of turtles. Netted animals were However, the study was based mainly on direct counted; their Species identified and then observation; enumerations depended on basking, released back into the same water. captured and floating turtles.  Canals were surveyed, during canal closure season, by walking in dry canals following the

Table 1: IUCN and CITES status of freshwater turtles of Pakistan

Species IUCN Status CITES Status Geoclemys hamiltonii Vulnerable Appendix I Hardella thurjii Vulnerable Appendix II Pangshura smithii Low Risk Appendix II Pangshura tecta Vulnerable Appendix I Chitra indica Endangered Appendix II Nilssonia gangetica Vulnerable Appendix I Nilssonia hurum Vulnerable Appendix I Lissemys punctata Low Risk Non CITES

Table 2: Population status and Distribution of Freshwater turtles in District of Charsadda, Pakistan

Observed Turtles Species Name of Geographical S.no. locality (water L. N. P. Total % coordinates C. N. P. H. Body) puncta huru smithi indica gangetica tecta thurjii ta m i 34° 13' 13.30'' N 71° 44' Kashmalo 56.24''E 1. Drain 12 - - 05 - - 02 19 5.20 Elev. (TurangZai) 309.02m

34° 9' 38.35'' N 71° 47' Dub Drain 15.8 2. 26.71'' E 27 05 09 17 - - - 58 (Mardan road) 9 Elev. 302.15m

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34° 16' 54.49'' N Hisara Drain 71° 49' 13.6 3. (Near Kashmir 46.38''E 25 - 03 17 - 5 - 50 9 Kalay) Elev. 351.73m

34o 14’ 45.56” N Branch No. 6 71o 50’ from Main 4. 57.62” E 04 - - - 02 09 - 15 4.10 canal of Lower Elev. Swat (Behlola) 346.79m

34o 12’ River Swat 58.26” N 14.7 5. (Khyali) Near 71o 40’ 6.89” 13 07 07 11 05 11 0 54 9 Tarnab E Elev. 316 m 34o 12’ 19.42” N River jindi 26.3 6. 71o 43’ 18 09 29 33 - 05 02 96 (Nimouri) 0 35.76” E Elev. 310 m 34o 84’ 79” N 71o 41’ River Kabul 20.0 7. 11.16” E 14 09 21 17 04 07 01 73 (Sardaryab) 0 Elev. 294.82 m Total 113 30 69 100 11 37 05 365 % 30.95 8.21 18.90 27.39 3.01 10.13 1.36

Percentage of Different turtle Species

35 30 25 20 15 10 5 0 Percentage of Population of Percentage

P. tecta C. indica N. hurum P. smithii H. Thurjii L. punctata N. gangetica Name of Turtle

Fig 3: Population status of different Turtle Species in Charsadda District of Khyber Pakhtunkhwa.

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3. Results and Discussion Suwelo [13] reported that the tortoises, terrapins and A total of 365 Individual turtles belonging to two turtles of Southeast Asia have been harvested from the families viz., Geoemydidae (Brown roofed turtle, wild for a wide range of purposes, primarily for food Pangshura smithii; Indian roofed turtle, Pangshura and traditional Chinese medicines, but also for pets and tecta and Brahminy river turtle, Hardella thurjii) and to release in Buddhist sites in temples. Jetkins [14] Trionychidae (Indian soft-shell turtle, Nilssonia reported that in recent years the trade has escalated and gangetica; Peacock soft-shell turtle, Nilssonia hurum; changed dramatically. Once predominantly for local Narrow-headed soft-shell turtle, Chitra indica and consumption, the harvest is now motivated by Indian Flap-shell turtle, Lissemys punctata andersonii) international demand, primarily in East Asia and were identified (Table 2, Fig. 3). The most abundant particularly China, Hong Kong, South Korea and species found was Lissemys punctata (30.95%) Vietnam. followed by Nilssonia gangetica and Nilssonia hurum (27.39% and 18.90%) respectively. Whereas, Hardella The Plastron is used to extract medicine called thurjii (1.36%) and Pangshura tecta (3.01%) were rare, Guilinggao, which is commonly known as turtle jelly whereas the status of Pangshura smithii (10.13%) and and is thought to cure heart diseases. Recent studies Chitra indica (8.21%) were frequent. Lissemys can also be found which state that the extracts from punctata (30.95%) was common in all the sites turtles are also used in cosmetics. One needs to focus sampled. The greatest number and species diversity on the growing pharmaceutical industries that was recorded at River Jindi (26.30% of all captures) accelerated the rate of animal slaughter. belonging to six different species except Pangshura tecta. It is a river where most of the drains of district During our interviews in Charsadda, we clearly noticed Charsadda join it. Beside River Jindi, all the seven the lack of awareness about conservation, as well as species were recorded in River Kabul (Sardaryab) and illegal trading of endangered species including River Swat (Khyali) (20.00% and 14.79%, freshwater turtles. According to locals, Turtles of all respectively). And the reason was that, that these rivers kinds were hunted by some groups of local and outside have the greater water capacity. residents a few years ago to the point that they were almost wiped out all the turtles. But still we see today a The Indian flap-shell turtle (Lissemys punctata) was reasonable population here, which indicates that the most abundant species, probably because it loves population, has recovered from harvest with in a shallow streams, stagnant waters of rivers, marshes, relatively short period of time, perhaps because of ideal ponds, lakes and often extends in sewage system of conditions for growth. metropolitan cities. Minton [11] also reported the same behavior of the Indus mud turtle. Our data indicate During our study some threats to turtles population was collectively that Lissemys punctata has a healthy also recorded which are given below in order of their population and found in about all sites (Rivers, canal magnitude. and Drain systems) of charsadda. The second abundant 1. Freshwater turtles do not have any legal species was Nilssonia gangetica, which has a good protection coverage through any provincial population about in all surveyed sites. Mehmood et Act; therefore, they are being captured in al.,[8] investigated the Korang River of Islamabad- thousands for supply to foreigners living in Rawalpindi, and according to their study Lissemys Pakistan and to illegal export for supply to punctata was the most abundant species contributing abroad. Reports of capturing turtles on large up to 56% of the total numbers of turtles recorded. scale were received from these areas since Nilssonia gangetica contributed 30% while Pangshura 2006. smithii was least abundant (08%) during the study 2. Fishermen also capture turtles during fishing period. The present study showed about the same with nets and angling. Some turtles are result. accidentally killed with nets, whereas some fishermen considered them the enemies of Noureen [12] reported the distribution of Geoclemys fish, therefore, they kill the captured turtles to hamiltonii in the district of Dera Ismail Khan of save their fish. Khyber Pakhtunkhwa province, but during the present 3. Dogs were observed wondering extensively study this species was not recorded in Charsadda during canal closure in search of food. These district of Khyber Pakhtunkhwa province. According dogs eat dead fish, tapped fish and turtles in to local communities and some poachers the shallow water. Geoclemys hamiltonii is not found in the water bodies 4. During fish capturing operations by local of Charsadda by showing them the species peoples turtles are also captured and identification card. occasionally killed.

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5. Hibernated turtles are either killed or removed Miller). Pennsylvania Academy of Science, from their natural habitat and shifted with silt Easton PA. 1994; pp. 381-391. where their lives are on risk during de-silting 4. Zuberi B. Pakistani turtles in danger. All of canals. things Pakistan. www.solar-arid.org updated 6. Running water maintains body temperature of turtles. Turtles face severe cold condition due 25 Feb. 2007 and accessed at 30 June 2009. to unavailability of water and shortage of food 5. Baig KJ. Environmental baseline survey and which is harmful to turtles when canals are monitoring of Taunsa barrage: emergency closed. rehabilitation and Modernization Project: a 7. The maturity of turtles reaches late in their report submitted to Zoological science lives and they reproduce slowly. The species department. Pakistan Museum of Natural survival is possible if it survives for a long history.2006; pp. 22. period. 8. Nesting sites of freshwater turtles are not 6. Noureen U, Khan A and Arshad M. Exploring protected and the wild animals such as illegal trade in Freshwater turtles of Pakistan. monitor lizards, dogs and jackals eat their Rec. Zool. Surv. Pakistan.2012; 21: 19-24. eggs and even children break down these 7. Shah N. Wildlife trade in Sindh, A report eggs. published by WWF-P for TRAFFIC Fishermen also use various harmful and unsustainable International. 1996; pp. 57. techniques such as dynamite explosion, electric shocks and Pesticide for fishing. This is also a reason that the 8. Mehmood T, Siddiq MK, Rais M and Nadeem population of freshwater turtles are decreasing from the MS. Distribution and relative abundance of area. Freshwater turtles in korang river Islamabad- Rawalpindi, Pakistan. Pakistan J. Zool. 2012; 4. Conclusion 44(3): 889-893. The present study shows that seven species of 9. Thompson M. Hypothetical considerations of freshwater turtles are found in district Charsadda of the biomass of Chelid tortoises in the River Pakistan, in which Indian mud turtle (Lessymes punctata) is predominantly exists in the study areas Murray and the possible influences of while Hardella thurjii is very rare in Charsadda. The predation by introduced foxes. In d. Lunney population status of Nilssonia gangatica and Nilssonia and D. ayers, editors. Herpetology in hurum is also good in Charsadda. It is concluding that Australia: A diverse discipline. Transactions freshwater turtles are very important natural resource of the Royal Zoological Society of New South of the country, which are being ignored and wasted. To Wales, Chipping Norton. 1993. manage this situation and preserve turtle populations 10. Rubin ES, Boyee WM, Jorgenren MC, Torres into future, it is necessary to provide legal protection/coverage immediately under the NWFP SG, Hayes CL, “O”Bien CS and Jessup DA. Wildlife (Protection, Conservation, Reservation and Distribution and abundance of bighorn sheep Management) Act, 1975, otherwise this natural in the peninsular ranges. Calif. Wild. Soc. resource will be destroyed by the local peoples and Bull. 1998; 26: 539-551. Species will ultimately extent. 11. Minton SA. Jr. A contribution to the Herpetology of West Pakistan. Bull. Amer. 5. References Mus. Nat. Hist. 1966; 134: 29-184. 1. Azam MM and Saeed K. Abundance and 12. Noureen U. A preliminary visit to Dera Ismail distribution of freshwater turtles at Guddu and Khan to assess the status of freshwater turtles Taunsa barrages and Head Punjnad. Rec. of Pakistan (Unpublished report). Pakistan Zool. Surv. 2011; Pakistan. wetland Programme, Pakistan. 2007; pp. 1-23. 2. Walters O. (2000). A study of hunting and 13. Suwelo IS. The threatened species of trade of freshwater turtles and tortoises at Indonesian tortoises, terrapins and Turtles. Danau Sentarum. Borneo Research Bulletin. Tiperpaper. 2001; 28(2): 11-13. 3. Lovich JE. In Biological diversity: problem

14. Jetkins MD. Tortoises and Freshwater turtles: and challenges (eds. S. K. Majumdar; F. J. the trade in Southeast Asia. TRAFFIC Brenner; J. E. Lovich: J. F. Schalles and E. W.

International, UK. 1995.

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Safi A, Khan MZ. Distribution and current population status of freshwater turtles of District Charsadda of Khyber Pakhtunkhwa, Pakistan. Journal of Zoology Studies. 2014; 1(4):31-38.

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