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Diversity and conservation of freshwater turtles in Pakistan: a review Waqas Ali, Arshad Javid, Ali Hussain & Syed Mohsin Bukhari To cite this article: Waqas Ali, Arshad Javid, Ali Hussain & Syed Mohsin Bukhari (2018) Diversity and conservation of freshwater turtles in Pakistan: a review, Biodiversity, 19:1-2, 62-71, DOI: 10.1080/14888386.2018.1468820 To link to this article: https://doi.org/10.1080/14888386.2018.1468820
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Biodiversity 2018, Vol . 19, Nos . 1–2, 62–71 https://doi.org/10.1080/14888386.2018.1468820
Diversity and conservation of freshwater turtles in Pakistan: a review Waqas Ali, Arshad Javid, Ali Hussain and Syed Mohsin Bukhari Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore, Pakistan
ABSTRACT
Broadly speaking, turtles are represented by five families, 13 genera and 15 species in Pakistan, with freshwater turtles belonging to two families, six genera and eight species. Hardshell species include black pond turtle (Geoclemys hamiltonii), crowned river turtle (Hardella thurjii), brown roofed turtle (Pangshura smithii) and Indian roofed turtle (Pangshura tectum), while softshell species include Indian narrow-headed softshell turtle (Chitra indica), Ganges softshell turtle (Nilssonia gangeticus), Indian peacock softshell turtle (Nilssonia hurum) and Indian flapshell turtle (Lissemys punctata andersonii). Major threats to turtle populations in Pakistan include weak law enforcement, illegal trade, lack of awareness about the ecological role of the taxa, fishing activities and environmental pollution. As a result, three species are particularly vulnerable, namely Geoclemys hamiltonii, Hardella thurjii and Aspideretes gangeticus whereas Chitra indica is endangered and Kachuga smithii is near threatened. For successful conservation of turtles in Pakistan, it is essential that databases on diversity, distribution and the current status of various species in the country are developed and updated. In addition, conservation campaigns must be launched to raise awareness within local communities and school children regarding the important role turtles play within ecosystems. Establishing rescue and information centres at specific sites is also an absolute must for the protection of these environmentally friendly creatures.
Introduction In area, Pakistan is the 33rd-largest country in the world, spanning 881,913 square kilometres (340,509 square miles). The climate is continental with extreme variations during winter and summer and the monsoon season ranges from July to October. Rainfall varies throughout the year and floods and drought are common in various seasons of the year (Khan 1999). Pakistan, along with India, China and Nepal, is dependent on the Western Himalayas for freshwater resources (Pomeranz 2009) and it requires large volumes of water to meet its demanding agricultural, industrial and domestic needs (Figure 1). Due to increasing human population growth, with a population exceeding 209,970,000 people along with anthropogenic-caused impacts, such as agriculture and climate change, this has had direct effects on freshwater resources and their fauna (Khalid 2010). Pakistan is known as ‘the land of many lands’ as two of the six zoogeographic regions of the world are within the country. The fauna of Pakistan is represented by 198 freshwater and 1100 marine fish species, 24 amphibians, 195 reptiles, 668 birds and 174 mammalian species (Roberts 1991; Khan 2006). Freshwater turtles in Pakistan include black CONTACT Waqas Ali
[email protected]
© 2018 Biodiversity Conservancy International
ARTICLE HISTORY
Received 18 May 2017 Accepted 20 April 2018 KEYWORDS
Chitra indica; Kachuga smithii; habitat fragmentation; illegal trade; harmful chemicals
pond turtle (Geoclemys hamiltonii), crowned river turtle (Hardella thurjii), brown roofed turtle (Pangshura smithii) and Indian roofed turtle (Pangshura tectum), while softshell turtle species include Indian narrow-headed softshell turtle (Chitra indica), Ganges softshell turtle (Nilssonia gangeticus), Indian peacock softshell turtle (Nilssonia hurum) and Indian flapshell turtle (Lissemys punctata andersonii). Turtles have developed several adaptations including late maturity, high reproductive potential, less natural mortality and long life span. Turtles and tortoises are keystone species, playing major roles in the environment and food web as co-dependent species, whilst freshwater turtles play a significant role in the health of aquatic ecosystem due to their scavenger nature, being herbivores and carnivores, transferring nutrients from aquatic to terrestrial ecosystems, maintaining food webs and feeding on dead animals and purifying water. Turtles and tortoises play an invaluable role in balancing ecosystems and providing ecosystem services, which are also critically important for human-welfare (Ali et al. 2017). Many softshell turtle species are used to purify blood and are thus used in traditional Chinese medicine to cure many diseases (Beatty et al. 2001): a phenomenon which is increasingly endangering turtle populations. Adding to this is capturing turtles for food, leather, shell and other
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Figure 1. Riverine tracts of Pakistan.
body parts. As a result, three-quarters of Asia’s freshwater turtles and tortoises are threatened on the verge of extinction. Since 2737 BC turtles and tortoises have been used in medicines to cure many diseases with body parts such as the plastron and carapace of turtles used in Chinese medicines (see Table 1). Unani, the Greco-Arabic system of medicine, used to make turtle jelly from body parts of softshell turtles for the treatment of many human diseases (Zhao 1998). Due to increasing demand in medicine and food, China is the biggest importer of freshwater turtles from Pakistan, Nepal, Bangladesh and India as their own local wild stock is depleting and is protected by legislation (Moll and Moll 2004). As a result, illegal trade is insidiously catastrophic for most freshwater turtle species in Asia, with recent studies showing that 68 turtle species were recorded at Chinese food markets and out of these, 42 species were not native to China but were imported from Pakistan, Bangladesh and India (Gong et al. 2006). During the past few years, dramatic worldwide decline in amphibian and reptile species – 28% (470 out of 1678) reptiles and 30% (1895 out of 6285) amphibians of the world now classified as ‘threatened’ has caught the interest of conservationists, both locally
Table 1. Turtles species used in the traditional Chinese medicine and their status in a Taiwan market. Species Cuora amboinensis Siebenrockiella crassicollis Chinemys reevesii Indotestudo elongate Cuora flavoinarginata Geochelone elegans Geoeinvda spengleri Hardella thurjii Heosemvs grandis Hiereins annandalii Kachuga tecta Malayemys subtrijuga Manouria emys Manouria Impressa Maruemys mutica Moremzia ocellata Pyxicleci mnoithotii Cyclemys clentata Ocadia sinensis Platysternon megacephalum
Market status Abundant Abundant Common Common Occasional Occasional Occasional Occasional Occasional Occasional Occasional Occasional Occasional Occasional Occasional Occasional Occasional Rare Rare Rare
CITES status – – – II – II – – – – I II II – – I – – – –
and globally. Out of 335 total species of turtles and tortoises, 107 are classified as critically endangered, 167 are threatened and 175 are extinct or near extinction (Van Dijk et al. 2014). In Pakistan, due to lack of awareness and law enforcement, freshwater turtle species, such as
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Table 2. The taxonomic classification of freshwater turtles in Pakistan. Class Reptilia
Order Testudines
Super-family Testudinoidea
Trionychoidea
Family Bataguridae Bataguridae Bataguridae Bataguridae Trionychidae Trionychidae Trionychidae Trionychidae
Geoclemys hamiltonii, Hardella thurjii and Aspideretes gangeticus are facing severe problems, whilst Chitra indica is endangered and Kachuga smithii is near threatened (IUCN 2010).
Herpetofaunal diversity Boulenger (1890) recorded amphibians and reptiles in the Sub-continent, later updated by Smith (1943). Two authentic sources of information are available as data compiled by Mertens (1969), Minton (1966) and Khan (2006). The amphibians and reptiles of Pakistan are represented by 219 including nine and 13 species of amphibians and reptiles, respectively. The reptilian fauna of Pakistan belonging to 23 families, viz. Cheloniidae, Dermochelyidae, Emydidae, Testudinidae, Trionychidae, Crocodylidae, Gavialidae, Agamidae, Chameleonidae, Eublepharidae, Gekkonidae, Lacertidae, Scincidae, Uromastycidae, Varanidae, Leptotyphlopidae, Typhlopidae, Boidae, Colubridae, Elapidae, Hydrophiidae, Viperidae and Crotalidae (Khan 2004; Smith 1943). The freshwater turtle fauna of Pakistan is oriental at both the generic and species levels. Turtles are represented by five families, 13 genera and 15 species in Pakistan. Freshwater turtles belong to two families, six genera and eight species (Table 2). Hardshell species are
Genus Kachuga Kachuga Hardella Geoclemys Aspideretes Aspideretes Chitra Lissemys
Species Kachuga smithii Kachuga tecta Hardella thurjii Geoclemys hamiltonii Aspideretes gangeticus Aspideretes hurum Chitra indica Lissemys punctata andersonii
Geoclemys hamiltonii, Hardella thurjii, Pangshura smithii and Pangshura tectum while softshell turtles species are Chitra indica, Nilssonia gangeticus, Nilssonia hurum and Lissemys punctata andersonii. Descriptions of various freshwater turtle’s species are given in Table 3 (Azam and Saeed 2011; Khan 1991; Noureen, Khan, and Arshad 2012; Safi and Khan 2014). Diversity of freshwater turtles in different provinces of Pakistan Ali et al. (2016) conducted a survey in the Kasur district and reported three amphibian and 15 reptiles’ species including two freshwater turtle species, Lissemys punctata andersonii and Kachuga smithii. Azam, Fakhri, and Saifullah (2005) conducted a survey along the river Indus and reported the distribution and abundance of freshwater turtle’s species. Another survey conducted by Akbar, Mushtaq-ul-Hussan, and Zaib-u-Nisa (2006) at five rivers of Punjab reported 8 freshwater turtles species represented by four softshell and four hardshell species. The abundant species was Pangshura smithii and the status of Chitra indica was rare. Rais et al. (2012) conducted a survey on north Punjab’s districts Rawalpindi, Islamabad and Chakwal and reported 35 species of amphibians and reptiles representing 29 genera, 16 families. Out of these,
Table 3. Description of freshwater turtle species found in Pakistan. Species Geoclemys hamiltonii Hardella Thurjii
IUCN/CITES status II –
Pangshura smithii
LR/II
Pangshura tectum
LR/I
Chitra indica
VU/II
Nilssonia gangeticus
VU/II
Nilssonia hurum
VU/II
Lissemys punctata andersonii
II
Habitat Shallow ponds, pools, lakes and rivers Pools, ponds, canals, salt water Lakes, ponds puddles, canals Standing and slow moving Water Sandy shallow river Margins Rivers, lakes, permanent ponds Rivers, lakes, permanent ponds Lakes, rivers, shallow pools,
Food Snails, insects, larvae, crayfish
Clutch size 5–15
Incubation period 169–213
Behaviour Shy
Herbivore
8–13
200–273
Shy
Herbivore / carnivore
7–8
75–112
Shy
Herbivore / carnivore
8–12
125–144
Non-aggressive
Fish, crustaceans, snails Omnivore: birds, fish, carrion, cannibal Omnivore: birds, fish, carrion, cannibal Omnivore
60–120
22–40
25–40
25–35
Aggressive and ambushes predator Very aggressive
20–30
25–35
Aggressive
6–14
30–40
Shy and aggressive predator
IUCN Red List: VU = Vulnerable; LR = Lower Risk. CITES Appendices: I = species most in danger of going extinct, ban all commercial international trade; II = species that don’t qualify for Appendix I, but might in the near future if trade isn’t strictly controlled.
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30 species of reptile’s including seven hardshell and softshell species of freshwater turtle’s species were reported. Mahmood (2012) investigated the distribution and abundance of freshwater turtle species inhabiting the Korang River, near Islamabad and reported three species from the study area including Indus mud turtle (Lissemys punctata), Indian softshell turtle (Aspideretes gangeticus) brown river turtle (Kachuga smithii). The Indus mud turtle (Lissemys punctata) was found to be the most abundant species contributing up to 56%, the Indian softshell turtle (Aspideretes gangeticus) 30% and the brown river turtle (Kachuga smithii) constituted 8% of the total number of turtles recorded. Begum et al. (2013) conducted a survey at Hub Dam in Sindh and Baluchistan provinces and reported 25 reptile species represented by three orders and 12 families including three freshwater turtle species with the most abundant species being Hardella thurjii. Khan (2015) reported eight freshwater turtle species from four districts of the Khyber Pakhtun Khwa (KPK) Province, namely Charsadda, Peshawar, Nowshera and Dera Ismail Khan and four districts in the Sindh Province, namely Thatta, Badin, Sanghar and Sukkur. The most abundant species in both provinces was Lissemys punctata.
Habitats of freshwater turtles in Pakistan The geographic position of Pakistan is unique and the country harbors two out of six zoogeographic regions. Topographic features of Pakistan include three ecological regions viz., mountains, foothills and plains. Based on soil, vegetation and climatic condition these regions consist of 15 habitats: 1. dry and cold alpine deserts, 2. dry coniferous forests of Himalaya, 3. moist temperate forests of Himalaya, 4. Baluchistan hill ranges, 5. Baluchistan higher ranges, 6. tropical dry deciduous forests, 7. dry temperate semi-evergreen scrub forests and subtropical pine forests, 8. tropical dry mixed deciduous forests, 9. riverine tracts, 10. seasonal inundation zones, seepage areas, 11. lakes and swamps, 12. tropical thorn forests, 13. sand dunes in Thal and Cholistan Deserts, 14. littoral and intertidal zone and 15. offshore islands (Ali et al. 2018). Freshwater turtle species of genus Nilssonia and Chitra are mostly found in rivers and lakes. Nineteen Ramsar sites (Table 4) and other wetlands linked with dams are present along the Indus River in addition to many saline lakes which are present in the upper and lower Indus Valley. Mangrove swamps and intertidal mudflats are rich in grasses and floating vegetation found in the Indus Delta is the permanent habitat for amphibian and turtles fauna of Pakistan (Khan 2015). Ali et al. (2016) collected amphibian and reptiles from different habitat types in District Kasur; Lissemys punctata andersonii and Kachuga smithii were captured from water bodies.
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Table 4. List of Ramsar sites and their locality in Pakistan. Name Astola (Haft Talar) Island Chashma Barrage Deh Akro-II Desert Wetland Complex Drigh Lake Haleji Lake Hub Dam Indus Delta Indus Dolphin Reserve Jiwani Coastal Wetland Jubho Lagoon Kinjhar (Kalri) Lake Miani Hor Nurri Lagoon Ormara Turtle Beaches Runn of Kutch Tanda Dam Taunsa Barrage Thanedar Wala Uchhali Complex
Province Baluchistan Punjab Sindh Sindh Sindh Sindh and Baluchistan Sindh Sindh Baluchistan Sindh Sindh Baluchistan Sindh Baluchistan Sindh North-West Frontier Province Punjab North-West Frontier Province Punjab
Threats Illegal trade The greatest present-day threats to freshwater turtles are the Chinese food markets due to their medicinal and nutritional values. As China’s native freshwater turtle populations is declining to over exploitation, illegal traders from Indian subcontinent capture and illegally exporting turtles to China and Taiwan (Lau et al. 1997). Data related to the trade of freshwater turtles is lacking in Pakistan and illegal freshwater turtle trade was first highlighted in the 1990s. During 1996, a study was conducted by WWF-Pakistan and the Sindh Wildlife Department for TRAFFIC International, which reported turtle trade in the Sindh Province. Shah (1996) investigates that during engineering projects this province, Chinese consumed Indian softshell turtles as they can purchase one specimen at only 50 rupees (less than a US dollar) from the local fish market at Larkana and Manchar. The Board of Foreign Trade reported that from 1992 to 1998 more than 900 tons of hardshell turtle shells were exported to Taiwan from China other Southeast Asian countries (Yen 1992). Table 5 shows statistics from the Board of Foreign Trade from 1992 to 1998. In 2000, Lau and Shi reported illegal trading of live freshwater turtles was 13,000 metric tons from Southeast Asian countries, with the maximum number coming from Pakistan. During 2000, trade in freshwater turtles increased as fish populations reduced in the Indus River. In 2002, live capturing of freshwater turtles began in Punjab, in Sindh 2003 and in the KPK Province it started in 2006. In Taunsa Barrage, in the Dera Ghazi Khan District, nomads residing nearby were recorded to be exploiting Chitra indica and Nilssonia gangeticus for their body parts with average
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Table 5. Hardshell turtle’s shells (weight in kg) were exported to Taiwan from China and other Southeast Asian countries from 1992 to 1998. Year 1992 1993 1994 1995 1996 1997 1998 Total
Bangladesh 0 0 1,790 4.92 2700 0 0 9,410
Cambodia 0 0 0 0 7,659 8,050 14,740 30,449
China 33,731 154,594 50,626 7,460 14,137 8,366 93,764 362,678
Indonesia 13,740 51.920 56,511 65.253 90,566 88,278 37,315 403,583
laos 0 0 446 0 0 0 0 446
Malaysia 1,830 0 2850 0 0 0 1100 5,780
Pakistan 2,500 4750 0 0 0 0 0 7,250
Singapore 59,947 34,580 900 6.331 1,400 0 0 103,158
Thailand 804 3,480 413 0 0 0 0 4,697
Vietnam 0 0 735 0 210 19,942 9,605 30,492
Total 112,552 249,324 114,271 83,964 116,672 124,636 156,524 957,943
Note: Bold values represents country-wise trade of hardshell turtle species in kilograms from year 1992 to 1998.
catches of 200 turtle specimens per week and trading in dried shells in Karachi were also reported at 100–200 rupees per kg (Noureen 2009). The Pakistan Wetlands Programme (PWP) team conducted a survey from 17 April to 22 April 2007 to Dera Ismail Khan, KPK and reported that local fishermen (Kehals) dependent upon the Indus River were involved in capturing softshell turtle species, viz. Nilssonia gangeticus, Chitra indica and Nilssonia hurum, since December 2006. The average capture was about 37 softshell turtles per day by the local communities. The shells and live turtles were captured and delivered to international markets through illegal routes, earning 250 rupees (just under 4 US dollars) for one haul (Noureen and Khan 2007). The PWP team conducted freshwater turtle surveys from 24 June to 30 June 2007 to report trade in freshwater turtles at the Taunsa and Guddu Barrage, Indus River. Live turtles and their body parts of Chitra indica, Nilssonia gangeticus and Nilssonia hurum were exported to China through Lahore earning approximately 8000–10,000 rupees/40 kg of turtle depending upon its size (Noureen and Khan 2007). The PWP team conducted another survey at different barrages and dam works in the Punjab Province during 2007 at four principal river sites. Local communities, namely Mohana and Jabhel, were involved in the capture of turtles with a single person catching between 5 and 10 turtles/day. However, during more commercial fishing operations they catch approximately 200 turtles in a single day (Noureen et al. 2008). Karachi is one of the mega cities of Pakistan where markets exclusively for pet animals exist. Empress Market in Karachi Saddar and a fish market on Burns Road were found to be the largest animal market where turtles are also traded as pet animals in aquarium shops. During fishing these turtles were accidently captured in nets and were sold on in markets by local fishermen. The species seen most was Lissemys punctata andersonii which sold at 400–450 rupees (around 600 US dollars) per specimen (Noureen 2009). Mahmood et al. (2011) conducted a survey uncovering the trade of animal species at Goodri market, Multan and College Road market in Rawalpindi from
December 2009 to June 2010 and reported that 760 birds, 78 mammals, 114 fish and 45 reptiles were found in the Multan market whereas 901 birds, 55 mammals, 61 fishes and 43 reptiles were found being sold in the Rawalpindi market. The most common reptile species in both markets were spiny-tailed lizards (Uromastix hardwicikii), Indian softshell turtles (Aspideretes gangeticus) and brown river turtles (Kachuga smithii). In 2005, a shipment of 3650 kg of frozen turtles was held at Karachi Seaport going to Vietnam. In 2007, the Wildlife and Pakistan Customs Department at Jinnah International Airport, Karachi, captured illegal trade of 700 kg of turtle parts on its way to China. In Peshawar in 2007, the KPK wildlife department seized 300 kg of turtle parts also going to China. Similarly, in 2008 the Punjab Wildlife Department captured the illegal trade of 300 kg of turtles in Lahore. The market value of turtle eggs in Lahore was 5–10 rupees/egg and live turtles at 2500–4500 rupees /kg. Hardshell species of freshwater turtles were also used for ornamental purposes and sold at 400 and 500 rupees/ specimen with mostly hatchlings of Pangshura smithii seen in ornamental fish markets. Local communities in KPK, Punjab and Sindh residing along Indus River are dependent upon the Indus river water as they were involved in capturing of turtles and fishes. Based on information received by TRAFFIC from anonymous sources, trade in freshwater turtles appeared to start in Bangladesh, India and Pakistan in 2014, where turtles were captured and transported to wholesale markets in Thailand from where they sent to retail centres in Hong Kong (Serene 2014). Safi (2014) reported that local peoples in KPK, hunted turtles of all kinds up to a point that they almost wiped out all the turtles from the area but thankfully due to ideal conditions for growth, reasonable populations have recovered. Between January 2013 and March 2014, illegal international trade of the black spotted turtle (Geoclemys hamiltonii) has increased. During this time, more than 1960 turtles were captured in 22 incidents. Out of these, 1865 were seized in 2014. The main market hub is in Bangkok, Thailand and Hong Kong from all of the Asian countries.
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In 2013 a Pakistani national was arrested with 470 Black Spotted Turtles in four suitcases in Bangkok, Thailand, by the Thai Royal Customs. In another case in 2013, the Customs Department in Islamabad, Pakistan, captured a bag with 320 black spotted turtles hidden in clothes going to Bangkok, Thailand (Serene 2014). Trade routes Punjab and KPK Lahore is a hub for the export of turtles and their body parts and locally collected turtles are generally transported to Lahore through Peshawar. In Sindh province, the Karachi Seaport is a main route for illegal trade. The biggest importers of freshwater turtles from Pakistan are China, Hong Kong, Korea, Vietnam and Iran (Noureen 2012). Fishing operations Reptiles are less appreciated creatures in Pakistan and due to lack of information regarding the role of turtles in the environment, many were killed by fisherman who considered them as their enemy. Moreover, damaged fishing nets discarded in water bodies act as traps and capture many turtles, which ultimately leads to the death of these animals. During fishing activities, traps and nets set to capture fish also incidentally catch and drown turtles. Turtles were also killed by baits used to capture fishes (Khan 1998; Fratto, Barko, and Scheibe 2008). Fishermen also use various harmful and unsustainable techniques such as dynamite explosion, electric shocks and pesticide for fishing which also kills turtles (Noureen 2009). Closure of canals Vast mortalities of turtles occur during their hibernation period as de-siltation and closure of canals either killed or shifted turtles to new locations where their lives are at risk. Scarcity of water in rivers and canals negatively affect turtle population due to unavailability of food (Wahab et al. 2012). Killing Turtles migrate for many reasons but nesting is most common as turtles prefer road shoulders for nesting sites and while crossing roads vast mortalities occur (Aresco 2005; Marchand and Litvaitis 2004; Steen and Gibbs 2004; Wahab et al. 2012). Mostly turtles were killed due to accidents with heavy traffic while crossing highways in search of their nesting sites (Noureen 2009). Moreover, wandering turtles mostly get injured or killed by local peoples just for fun (Khan 2006).
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Floods Severe population decline of freshwater turtles is common due to change in environmental conditions which leads to rivers alteration. As a result, microhabitat and demographic changes occur in population distribution and abundance (Travis et al. 2008). Chemical poisoning Currently, fishermen use dynamite explosion to capture maximum numbers of fish which also affects freshwater turtle species adversely, resulting in high mortality (Ewing 1999). Wahab et al. (2012) reported that Sukkar Barrage has been the victim of chemical poisoning and as a result hundreds of turtles died and were washed ashore. The Guddu Barrage also suffered from such an incident in 2010, where mass mortality of freshwater turtles along with other aquatic fauna occurred due to toxic chemicals. Pollution Surface runoff, industrial and sewage wastewater are the ultimate sources for increasing aquatic pollution. Pollutants negatively affect aquatic fauna especially turtles as they are directly depend upon water for many activities. Being at the top of the trophic level, toxins and heavy metals accumulate in high amounts and have lethal effects on both taxa. The effect of pollution and non-biodegradable pollutants are poorly studied and have never been documented (Carol 2009). Climate change Pakistan is included within the high-risk countries affected by climate change and among the top ten countries most vulnerable to climate change. During the last two decades, Pakistan has faced extreme climatic events, experiencing changes in monsoon patterns which have caused flooding, such as in 2010 and also cyclones in 1997 and 2007 (Arnell 1999; Khan 2013). In Pakistan, from the high Himalayas to the Indus Delta, all wetlands are badly affected by climate change (floods, drought, and unusual rains) and human management. These wetlands are highly productive ecosystems and are the economic lifelines for many of the local people. Such landscapes become fragile due to degradation, invasion of exotic species and imbalance of nutrients. Clearing of aquatic vegetation along watersheds leads to siltation, turbidity, decreased productivity and increased flooding (Heino, Virkkala, and Toivonen 2008). Climate change has the potential to affect turtle populations significantly as their sex determination is based on temperature. At a
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particular site, turtle population structures may change as a consequence of a warmer climate. Eggs incubated at relatively warm temperatures develop into females as compared to cool eggs which produce male turtles (Van Dijk 2010). Habitat destruction Anthropogenic activities, viz. the uses of riparian areas, overgrazing, urbanisation, deforestation, habitat fragmentation and degradation, have exerted negative effects on turtle populations worldwide. Furthermore, direct and indirect effects of water channelling have led to habitat loss of many species (Bodie 2001). Seventy per cent of the total population of Pakistan lives in rural areas with cultivation along river banks being the most common practice. This directly affects turtles by destroying their nesting sites whilst the increasing salinity in freshwater rivers and wetlands causes a decrease in aquatic flora and fauna, especially turtles (Brock, Nielsen, and Crossle 2005). Khan (2015) reported that mass mortalities of turtles were seen due to drought conditions in Thatta and Badin of Sindh province and dogs were the most common predator of turtles. By clearing vegetation around river edges, hibernating turtles are either killed or removed from their natural habitat. Nesting sites of freshwater turtles are not protected and wild animals such as monitor lizards, dogs and jackals eat their eggs and even human children break these eggs (Ali et al. 2018).
Protection Act was amended by the Punjab Wildlife and Parks Department and turtles and tortoises were listed in Schedule III. That said, strict law enforcement is still required against illegal capturing and trading of turtles. The 1972 Sindh Wildlife Protection Ordinance does not make any amendments and no freshwater turtles of the province are protected by law.
Conservation measures Development of database The first step for conservation is to assess the distribution and status of turtle species throughout the country. Provincial wildlife departments in collaboration with private agencies such as ZSP, WWF Pakistan and PMNH should take note of the findings within these surveys. International organisations and agencies can also play a major role by providing training and equipment to maintain a communication network and awareness-raising. Wildlife trade monitoring There is dire need to monitor turtle trade routes and information on species and volumes of turtles shipped through various sources (Wahab et al. 2012). Habitat conservation
The IUCN Red List (2009) reported seven species as vulnerable and endangered, mostly affected by illegal hunting of turtles in Pakistan.
Mass turtle mortalities have been reported during fishing, canal auctions and general desolation as hibernating turtles are either killed or transported to other places resulting in death with no food or water resources available. Turtles should be released into rivers before the auction of canals and strict legislation is required to ban the chemical poisoning and dynamiting explosion of fishing activities (Khan 2006).
CITES
Commercial farming
Pakistan became a signatory to CITES in July 1976. Out of eight freshwater turtle species, only Hardella thurjii is not listed in any CITES appendix, whereas Appendix I include four species of turtles and three species were added to Appendix II of CITES.
There is a need to start commercial farming of freshwater turtles, which is a substantial and reliable form of income. As a result, farmed turtles would keep market prices stable and may decrease the pressure on wild populations.
Conservation status of freshwater turtles of Pakistan IUCN Red List
Conservation breeding and genetic implications Provincial Wildlife Protection Acts In 2007, the 1975 Wildlife Protection Act was revised and the NWFP Wildlife Department provided protection by including all freshwater turtle species of the province in Schedule III. Later on, the 1974 Punjab Wildlife
The present illegal trade scenario leads to many turtle species being threatened with extinction in their natural habitat. A nationwide assessment of the status of different turtle species, their ecology and genetics is required, whilst a species recovery plan is also needed. Habitat
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fragmentation plays a major role in the loss of genetic diversity but not enough data is currently available. Genetic approaches must be used to detect and monitor by making molecular markers (Engstrom et al. 2007; Fitzsimmons and Hart 2007). The current state of legislation and enforcement It is crucial that strict legislation and law enforcement is implemented in order to protect freshwater turtle species in Pakistan. Illegal trade should be addressed through CITES, IUCN and TRAFFIC International to conserve endangered species. The situation regarding the capturing of turtles is better in the capital city Islamabad, but strict implementation is required in the Punjab and Sindh province. Public awareness-raising within the local community regarding the values of different turtle species is crucial in order to reduce the killing and hunting of turtles. Wildlife corridors should be built during highway construction projects in order to reduce migrating turtle mortality due to road accidents (Rais, 2012). According to Sarwar (2015) there is a need to study turtle natural history, breeding and farming research studies which may stabilise decreasing populations. Raising awareness The significance and ecological role of turtles is still unknown in Pakistan at the community level. It will be impossible to recover population of turtles if they disappeared from the wild. Turtles serve as keystone species and should be added as a focal point in conservation awareness campaigns. Collaboration with media, grant donors agencies and non-governmental organisations is urgently needed for addressing the conservation issue of freshwater turtles (Noureen 2009; Wahab et al. 2012).
Conclusion and recommendations • The development of a database recording diversity, distribution and the current status of various freshwater turtle species in Pakistan. • At the national level, preparation of field guides is necessary for identification and turtle survey techniques. • At the community level, conservation education is necessary through workshops, trainings and seminars to raise awareness. • Conservation education should start at the local school level. • The establishment of rescue and information centres as potential sites is necessary for local community guidance.
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Disclosure statement No potential conflict of interest was reported by the authors.
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