Journal of Threatened Taxa | www.threatenedtaxa.org | 26 April 2017 | 9(4): 10035–10046

 

 

275477.jpg

 

 

 

Conservation of the Southern River Terrapin Batagur affinis (Reptilia: Testudines: Geoemydidae) in Malaysia: a case study involving local community participation

 

Pelf Nyok Chen

Turtle Conservation Society of Malaysia, 6513, RAKR Kg. Fikri, 24000 Chukai, Kemaman, Terengganu, Malaysia.

pelf@turtleconservationsociety.org.my, chenpn@gmail.com

 

 

 

 

doi: http://doi.org/10.11609/jott.3267.9.4.10035-10046

Editor: Anders G.J. Rhodin, Chelonian Research Foundation, Lunenburg, USA. Date of publication: 26 April 2017 (online & print)

 

Manuscript details: Ms # 3267 | Received 04 January 2017 | Final received 23 February 2017 | Finally accepted 09 April 2017

 

Citation: Chen, P.N. (2017). Conservation of the Southern River Terrapin Batagur affinis (Reptilia: Testudines: Geoemydidae) in Malaysia: a case study involving local community participation. Journal of Threatened Taxa 9(4): 10035–10046; http://doi.org/10.11609/jott.3267.9.4.10035-10046

 

Copyright: © Chen 2017. Creative Commons Attribution 4.0 International License. JoTT allows unrestricted use of this article in any medium, reproduction and distribution by providing adequate credit to the authors and the source of publication.

 

Funding: (a) Mohamed Bin Zayed Species Conservation Fund (financial assistance); (b) Prof. Zubaid Akbar b. Mukhtar Ahmad from Universiti Kebangsaan Malaysia (research equipments); (c) CIMB Foundation (Malaysia) (research equipments).

 

Competing interests: The author declares no competing interests.

 

Author Details: Pelf-Nyok Chen has been involved in the field of turtle research and conservation since 2004. Her research focuses on the nesting, reproductive and hatchling ecology and conservation of the Southern River Terrapin Batagur affinis. In 2011, she co-founded Turtle Conservation Society of Malaysia, a non-profit and non-governmental organization dedicated to turtle conservation in Malaysia.

 

Acknowledgements: This study was part of a larger B. affinis research and conservation program, carried out under the Special Permits issued by the Malaysian Department of Wildlife and National Parks. I am grateful to the Mohamed bin Zayed Species Conservation Fund for providing the initial research grants for this project in 2012, 2013 and 2014; Prof. Zubaid Akbar b. Mukhtar Ahmad from Universiti Kebangsaan Malaysia for sponsoring research equipments; and CIMB Foundation (Malaysia) for sponsoring 300 microchips. I thank David Steen and Whitney Joanna Banning-Anthonysamy for reviewing the initial drafts of this manuscript and greatly improved it. I am indebted to Eng Heng Chan for her patience, guidance and for teaching me the ropes of turtle research. I thank the Village Development and Security Committee for their support towards this project. Finally, this project would not have been possible without the assistance provided from volunteers, student interns and the Terrapin Guardians, i.e., Wazel b. Mahad, Mohd. Zulkifli b. Mohd. Noor, Abdullah b. Awang, Mohd. Nasir b. Abdul Hamid, and Mohd. Azmi b. Wazel.

 

 

 

 

 

Abstract: It is evident that the participation of the local community plays a crucial role in the success of a conservation project. Despite initiating and leading the oldest Batagur affinis conservation project in Malaysia since 1967, which involved egg protection, head starting and reintroduction programs, the Department of Wildlife and National Parks did not involve the participation of the local community. This study provides the first account of the involvement of local villagers in B. affinis research and conservation project in the Kemaman River, Terengganu, Malaysia. As a result of involving this group of local villagers, the Village Development and Security Committee was recruited to be involved in the conservation project. From 2012 to 2016, we hand captured and processed 102 post-nesting females. The Schnabel mark-recapture method estimated at least 186 wild female B. affinis in the river. We collected 2,542 B. affinis eggs from 205 nests for incubation, and produced 1,723 hatchlings (mean hatching success 67.8%). Survivorship of head started B. affinis hatchlings in captivity ranged from 96.7−100 % among cohorts. Head started hatchlings recorded a 467% increase in body mass and 90% increase in straight carapace length. We reintroduced 1,690 B. affinis juveniles into the river. We also initiated a symbolic adoption program to raise funds and ensure the sustainability of the conservation project. This study proves that local communities are capable of managing their own resources, given sufficient training in conservation techniques.

 

Keywords: Batagur affinis, community, conservation, head starting, Kemaman, Malaysia, population, reintroduction, Southern River Terrapin, status.

 

Abbreviations: ANOVA - Analysis of Variance; BM - Body mass; DID - Department of Irrigation and Drainage; DWNP - Department of Wildlife and National Parks; LSD - Least Significant Difference; MANZA - Malaysia, Australia and New Zealand Association; MYR - Malaysian Ringgit; PE - Polyethylene; SCL - Straight carapace length; SCW - Straight carapace width; US$ - US Dollars.

 

 

Malay abstract: Ia adalah jelas bahawa penglibatan masyarakat setempat memainkan peranan yang penting dalam kejayaan sesuatu projek pemuliharaan. Walaupun Jabatan Perlindungan Hidupan Liar dan Taman Negara telah memulakan projek pemuliharaan Batagur affinis yang pertama di Malaysia sejak tahun 1967, dan melibatkan program pengeraman telur, pemeliharaan anak tuntung dalam kurungan dan program pelepasan semula anak tuntung ke dalam sungai, pihak Jabatan tidak melibatkan masyarakat setempat dalam projek-projek tersebut. Ini merupakan projek pertama yang melibatkan penduduk setempat dalam projek penyelidikan dan pemuliharaan B. affinis di Sungai Kemaman, Terengganu, Malaysia. Lanjutan daripada penglibatan penduduk setempat, Jawatankuasa Kemajuan dan Keselamatan Kampung juga telah terlibat dalam projek pemuliharaan ini. Dari 2012 hingga 2016, kami telah menangkap dan memproses sebanyak 102 ekor tuntung betina. Kaedah tangkap-tanda-lepas-dan-tangkap-semula Schnabel menganggarkan sekurang-kurangnya 186 ekor tuntung sungai betina yang liar di dalam sungai. Kami telah mengumpul sebanyak 2,542 butir telur B. affinis dari 205 sarang untuk pengeraman, dan menghasilkan sebanyak 1,723 ekor anak tuntung (purata kadar penetasan 67.8%). Kemandirian anak-anak B. affinis semasa dalam pemeliharaan di dalam kurungan direkodkan antara 96.7–100% antara kohort. Anak-anak tuntung mencatatkan peningkatan berat badan sebanyak 467% dan peningkatan panjang karapas sebanyak 90%. Kami telah melepaskan sebanyak 1,690 ekor B. affinis juvenil ke dalam sungai. Kami juga telah memulakan program anak angkat secara simbolik untuk menjana kewangan dan memastikan kemampanan projek pemuliharaan ini. Kajian ini membuktikan bahawa masyarakat setempat mampu menguruskan sumber-sumber mereka sendiri, sekiranya diberi latihan yang mencukupi dalam teknik-teknik pemuliharaan.

 

 

 

 

 

 

INTRODUCTION

 

 

The Southern River Terrapin Batagur affinis is a freshwater turtle that is listed as one of the top 25 most Critically Endangered tortoises and freshwater turtles in the world (Turtle Conservation Coalition 2011). The species is found only in southern Thailand, Cambodia and peninsular Malaysia (Praschag et al. 2007, 2008; Moll et al. 2015). Wild populations of B. affinis have been extirpated and are depleted in much of the species’ former range in southern and southeastern Asia, which extended into the Mekong delta in Vietnam and Tonle Sap in Cambodia (Moll 1980; Platt et al. 2003; Kalyar et al. 2007; Moll et al. 2015) and Malaysia currently seems to harbor the only viable wild populations of this species (Platt et al. 2006). In peninsular Malaysia, wild B. affinis populations have been documented in the Kedah and Perak Rivers on the west coast (B. affinis affinis), and in the Terengganu, Dungun (Edward Moll unpub.), and Setiu Rivers on the east coast (B. affinis edwardmolli) (Soh 2004; Chan & Chen 2011).

The decline of B. affinis populations in Malaysia is attributable to various forms of natural, accidental and deliberate destruction, overexploitation and alteration of habitat (Moll et al. 2015). Besides being hunted for its meat (Eng Heng Chan & Pelf Nyok Chen unpub.), B. affinis is also pursued for its eggs and juveniles (Moll 1980). Its distribution in the major rivers in the states of Kedah, Perak, and Terengganu has made it a good source of income and food for local villagers. Individuals are occasionally captured in fishing nets set across rivers to catch freshwater fish. Terrapins may drown in the nets or, if caught alive, are either released or consumed (Eng Heng Chan & Pelf Nyok Chen unpub.).

In Malaysia, B. affinis is listed as a ‘Totally Protected’ species, and according to Wildlife Conservation Act 2010, it is illegal to kill, destroy, possess, trade or harass B. affinis, regardless of whether it is mature adults, juveniles, hatchlings, or eggs (Image 1).

There is a growing body of evidence that community participation plays a crucial role in promoting conservation success (Campbell & Vainio-Mattila 2003; Ghimire et al. 2004; Strusaker et al. 2005) because these projects see the local rural people as the solution rather than the problem (Horwich & Lyon 2007). By combining the knowledge gained through scientific investigations, with the insights of the local population, we stand a much better chance of succeeding in recovery efforts (Bird et al. 2003). The inclusion of local people in resource management can provide many benefits. Stronger conservation alliances based on the mutual sharing of knowledge, along with the combination of local science and structured monitoring, may produce the greatest conservation benefits (Bird et al. 2003). Community-based conservation projects have been initiated in numerous wildlife conservation projects (Vieitas et al. 1999; Nichols et al. 2000; Bernstein & Christiansen 2011; Hamilton et al. 2011; Şekercioğlu 2012). In recent years, community-based conservation projects have been carried out across numerous disciplines, i.e., wildlife reintroductions, ecotourism, conservation of wildlife, mangrove forests and wetlands, creation of protected areas, and to varying degrees of success (Horwich & Lyon 2007).

The involvement of the local community is necessary in B. affinis conservation due to conflicts in resource utilization (i.e., consumption of B. affinis eggs for their alleged aphrodisiac properties, the use of indiscriminate fishing gear for their own convenience, etc.). It also ensures that the local community will protect their resources, and in the long term, ensures the sustainability of the project. While various B. affinis conservation efforts have been carried out by the Malaysian Department of Wildlife and National Parks (DWNP), including egg protection programs, head starting, captive breeding and reintroductions, none of these involved the participation of the local communities.

Despite B. affinis being listed as Critically Endangered and although Malaysia has been hypothesized to harbor the remaining viable wild populations of the species (Platt et al. 2006; Moll et al. 2015), there has been no systematic attempt to quantify the sizes of B. affinis populations in Malaysia. Previous capture-release surveys conducted in the Perak River in the late 1970s showed no consistent population estimates of wild B. affinis and too few collections were made in the Terengganu River to provide any population estimates (Moll 1980). Population sizes were estimated based on the number of eggs collected for incubation, rather than from a direct count of individuals (Moll 1980).

The DWNP recognized the critical roles played by B. affinis egg protection and head starting programs, which led to the establishment of three head starting facilities in Peninsular Malaysia since 1967 (Edward Moll unpub.). Other egg protection programs have also been initiated in the Dungun and Setiu River (Chan & Chen 2011) populations; however, in all these conservation programs, a continued decline in the populations has been recorded (Table 1), except in 2008, where 99 nests from 95 females were recorded, representing the highest nest numbers since monitoring in the Terengganu River began in 1977 (Chan & Chen 2011; Eng Heng Chan & Pelf Nyok Chen, unpub.). The DWNP has also been reintroducing head started B. affinis into the wild, but the success of these reintroduction programs have not been assessed.

The goal of this study was to document the participation of a local community in a B. affinis research and conservation project in the Kemaman River, Malaysia. It was demonstrated that the participation of the local community is not only a viable conservation strategy, but also ensures the sustainability of the B. affinis conservation project, and both the ecological and non-ecological achievements and milestones of the project were highlighted. Specific objectives were to document: (1) the population size of wild, female B. affinis; (2) the egg protection and head starting programs; and (3) the reintroductions of juvenile B. affinis into the Kemaman River.

 

316613.jpg

 

 

315652.jpg

 

 

MATERIALS AND METHODS

 

 

Study Area

Kemaman is the southern-most district in the east coast state of Terengganu in Peninsular Malaysia. The Kemaman River, measuring approximately 166.7km in length, is the third longest river in Terengganu (Fig. 1). This study was conducted in Pasir Pok Yok (4014’32.1936”N & 103017’1.9536”E), one of the major B. affinis nesting banks in the Kemaman River. Pasir Pok Yok measures approximately 250m in length, and approximately 30m at its widest. It is backed by a palm oil plantation and is not accessible by road. Outside of the B. affinis nesting season, this sand bank is largely unused by the local fishermen.

River depths range from three to seven meters. The Kemaman River merges with the Chukai River at the estuary and both flow into the South China Sea. There are approximately 15 sand banks along the Kemaman River, but Pasir Pok Yok, which is located near Kg. Pasir Gajah, is the major B. affinis nesting bank in the river (Chan & Chen 2010). It is located approximately 30km from the estuary. A dam was erected 5km downstream from Pasir Pok Yok for paddy irrigation as well as to provide freshwater supply to the residents in the nearby town of Chukai, with a population of more than 160,000 (Malaysia 2010).

 

Participation of local community

Five local villagers were recruited at the initiation of the B. affinis conservation project. For decades, these villagers have been collecting B. affinis eggs for their own consumption, which they considered a local delicacy (Mohd. Nasir b. Abdul Hamid pers. comm. October 2010). However, after learning about the proposed conservation efforts, they agreed to collaborate on this work and to give up their own consumption of B. affinis eggs in the future.

After oviposition, we hand-captured the females and brought them to the campsite. At the campsite, local villagers were trained to weigh and measure the straight carapace length (SCL) and straight carapace width (SCW) of the B. affinis (Image 2). They were taught how to microchip the females as a permanent method to identify the individuals. As we measured and microchipped the female, two other local villagers retrieved the eggs and placed them into a bucket lined with sand. This was to prevent the eggs from moving around during transportation to the hatchery the next morning.

There has been much debate over the effect of moving nests from their original location to modified environments (Mrosovsky 2008). Such nests may experience differences in hatching success (Garcia et al. 2003) and sex ratios (Dutton et al. 1985) compared with those left in situ. We transferred all B. affinis eggs to the hatchery because the eggs cannot be left in situ on the nesting bank due to the presence of predators such as wild boars and monitor lizards (Wazel b. Mahad pers. comm. October 2010). Furthermore, it was likely that other local villagers would poach the eggs that were left on the nesting bank due to the high demand for the eggs (Mohd. Zulkifli b. Mohd. Noor pers. comm. October 2010). It was more practical to incubate the eggs in a hatchery in the village.

The next morning we transferred all the B. affinis eggs from the buckets into the hatchery and marked and labeled all the nests accordingly. We hired the same villager to monitor the incubation process by checking the nests at least twice daily. When the B. affinis hatchlings emerged, the villager was trained to mark, weigh and measure all the hatchlings before placing them into polyethylene (PE) water tanks for head starting.

 

 

316618.jpg

 

Population studies

Population studies were conducted during the B. affinis nesting season, from February to March 2012 to 2016. Beginning on 1 February, a group of five local villagers and the author proceeded to the B. affinis nesting bank every evening. Upon arrival at the nesting bank, we began to patrol the nesting bank for nesting females. Once a nesting female was detected, we observed the nesting process at the edge of the vegetation, and sometimes behind makeshift blinds; females were allowed to nest undisturbed.

After the nesting process was completed, we hand-captured and brought the female to the camp site, where we checked her for injuries and abnormalities, recorded her body mass with a 50kg spring balance, and measured her SCL and SCW with a pair of 80cm stainless steel calipers. Then, we scanned her for the presence of a microchip. In the absence of a microchip, we assigned a new microchip (ProID). We cleaned the point of insertion, sanitized it with alcohol and implanted a passive integrated transponder (AVID, Avid Identification Systems, Inc., Norco, CA, USA) subcutaneously with a disposable syringe into the left inguinal region of the female. Then, we disinfected the point of insertion with alcohol and iodine. Microchips have been used for the identification and monitoring of various wildlife, e.g., in tortoises (Hellebuyck et al. 2013), snakes (Webb & Shine 1998), penguins (Renner & Lloyd 2000), and birds (Granzow 2008).

Processed females were marked for visual identification with a running alphabet letter (A, B, C, etc.) on the fourth vertebral scute using a non-permanent correction pen. In the event that any microchipped females returned to nest on a subsequent night we could eliminate the repetitive processing.

 

Head starting techniques

We maintained the head started B. affinis in 800L polyethylene (PE) water tanks, in groups of approximately 100 hatchlings. A local villager was trained to feed the hatchlings twice a day, i.e., once in the morning at about 0900, and once in the evening at about 2100. Water was changed twice daily, i.e., once before the first feeding, and once before the second feeding. We placed pieces of bricks into the tanks to serve as “platforms” for the hatchlings. As the hatchlings grew bigger, we increased the water level in the tanks to provide them more space to move about.

Hatchlings were fed with commercially available fish pellets daily. We supplemented the diet with water spinach (Ipomoea aquatica), water hyacinth (Eichhornia crassipes) and Chinese mustard or Kai Choi (Brassica juncea) thrice a week. A month before the hatchlings were released, we fed them all with only I. aquatica, E. crassipes and B. juncea. We weighed and measured all hatchlings before they were reintroduced into the Kemaman River.

 

Annual reintroductions events

We co-organized the annual reintroduction events every September with the local community. All head started B. affinis juveniles of the current cohort were released into the Kemaman River. Symbolic adoptions were introduced and members of the public were encouraged to financially support the conservation project to ensure its sustainability.

 

Data analyses

The population size of wild, female B. affinis in the Kemaman River was estimated using the Schnabel mark-recapture method because it allows for more than two capture-recapture encounters (Krebs 1989). For the calculation of growth of B. affinis in captivity, the measurements of some hatchlings were not considered due to their deformed or under-developed carapace (e.g., carapace that was not fully opened, and was still constricted to the shape of the terrapin egg). One-way ANOVA and Fisher’s Least Significant Difference (LSD) test were used to compare the differences in the morphometric measurements of the females among years. All statistical analyses were run using StatPlus:mac PRO with alpha set at 0.05 for all statistical procedures.

 

RESULTS

 

 

Participation of the local community

For their participation during the B. affinis nesting season, the project compensated the local villagers with a one-month allowance. Four of these local villagers have asserted, on separate occasions, that they have stopped poaching B. affinis eggs. After one B. affinis nesting season, the local villagers called themselves the ‘Terrapin Guardians’.

As a result of recruiting the “Terrapin Guardians,” we had the opportunity to invite the Village Development and Security Committee to be involved in the B. affinis project. Our initial cooperation was in the form of co-organizing our first B. affinis reintroduction event in 2012. Subsequently, the Village Committee became gradually invested in the project. For example, the Committee members assisted in the construction of our new hatchery in 2014, as the old hatchery—which was built on a low budget prior to the initiation of the project in 2011—was beginning to give way.

In 2016, the Village Committee had offered us the use of a utility room adjacent to the Community Hall, which we could convert into a Mini Terrapin Museum. This was evidence that the Village Committee was taking the collaboration seriously, and wanted to contribute to the B. affinis conservation project.

 

Population estimates

We captured and processed a total of 102 post-nesting female B. affinis from 2012 to 2016 (Table 3). Using the Schnabel mark-recapture method, a total of 186 wild female B. affinis in the Kemaman River was estimated (95% CI; 127–273).

Average body mass of the female B. affinis was 25.0kg (SD = ±3.0) (range 18.8−33.5 kg). The females averaged 54.6cm (SD = ±2.8) (range 47.5−60.2cm) in SCL and 42.4cm (SD = ±2.7) (range 29.0−48.3 cm) in SCW. There was no significant difference in body mass, SCL and SCW of the female B. affinis among years.

 

Egg protection program

In 2012, we collected 97 B. affinis nests for incubation. The following year, we recorded a drop of approximately 70% and only managed to collect 29 nests. Subsequently, we collected a consistent number of nests from 2013 to 2016 (Table 3). Throughout the study, we have collected a total of 2,542 B. affinis eggs from a total of 205 nests for incubation from 2012 to 2016. Of these, a total of 1,723 hatchlings have been produced, head started and subsequently reintroduced into the Kemaman River. Without the participation of the local community, this project would not have been possible because the fieldwork required at least one researcher to spend the night on the riverbank throughout the B. affinis nesting season.

 

316616.jpg

 

316617.jpg

 

Head starting and reintroductions

Survivorship of head started B. affinis hatchlings in captivity ranged from 96.7−100 % among cohorts. Nine hatchlings of the 2012 cohort escaped (Table 4). Ten from the 2012 cohort, eight from the 2014 cohort and six from the 2016 cohort died of unknown causes.

Body mass, SCL and SCW of B. affinis increased over time while in captivity. Head started B. affinis averaged 53.8g (SD = ±7.5) and 6.7cm (SD = ±0.3) SCL at hatching (N = 554) and 305.0g (SD = ±84.2) and 12.7cm (SD = ±1.2) SCL at the time of release (N = 737). This translates to a 467% increase in weight and 90% increase in SCL. The largest head started hatchling produced to date (#1236, 591g, 15.8cm SCL at release) was from the 2013 cohort.

Between 2012 and 2016, we reintroduced a total of 1,690 B. affinis hatchlings into the Kemaman River. Two hundred hatchlings that were less than four weeks old were reintroduced in 2012 in conjunction with “World Turtle Day” that was celebrated worldwide on 23 May. Subsequently, all head started juveniles were reintroduced at the end of the year. While we did not perform a health screen on all the head started juveniles prior to reintroductions, we did not observe any individuals exhibiting clinical signs of disease. Reintroductions typically took place in September, prior to the arrival of the annual Northeast monsoon that influences the east coast states in peninsular Malaysia, including Terengganu.

The annual reintroduction events were public events, with the aim of increasing public awareness on the status of B. affinis as well as the research and conservation projects carried out in the village. Every year, between 150 and 250 participants attended the release events, and these were school students, members of the public, donors who symbolically adopted terrapins, and the local communities. We put up mini exhibitions during the reintroduction events that aimed to educate the public on turtle diversity in Malaysia, our conservation efforts, and how the public could help save our terrapins.

One of the innovative fundraising programs that we initiated was the symbolic adoption program. Members of the public could help support our conservation activities by symbolically adopting a B. affinis at MYR 30 each. This amount was raised to MYR 35 in 2016. Every year, we invited all sponsors to participate in our reintroduction events and to release their adopted terrapins. The number of B. affinis symbolically adopted each year translated into a substantial amount of funds (Table 5). These funds were channeled back into the conservation project, which in turn, sustained the project.

All previous B. affinis reintroduction events had been reported in numerous national and international newspapers and magazines, such as the local Utusan Malaysia, Berita Harian, Sinar Harian, The Star, the New Straits Times, a few Chinese-medium newspapers, the Malaysia, Australia and New Zealand Association (MANZA) magazine, Turtle Survival Alliance magazine, etc. (Chen & Chan 2014; Anonymous 2015; Yaacob 2015; Husin 2016; Yusof 2016). The annual reintroductions have also been mentioned in various social media sites such as websites, Facebook, Instagram, and Twitter. The project also appeared in a 30-minute segment in a local TV program (https://www.youtube.com/watch?v=ouW6BuPbh14), as well as news clips in a few Astro (cable TV) stations (https://www.youtube.com/watch?v=Z3oulRfptXI). In 2015, the project was chosen as one of the three winners of a ‘Good Story Pitch’ by the Our Better World Foundation based in Singapore, and a team of videographers documented our B. affinis project in an 8-minute documentary (Our Better World 2015).

 

DISCUSSION

Community based conservation

The overarching goal of this study sought to provide the first account of the active participation of a local community in a B. affinis research and conservation project in the Kemaman River, Malaysia.

This study has shown that for conservation projects to be sustainable, the local communities must be involved and they must be trained to be stewards of their natural resources (Horwich & Lyon 2007). While participation does not predict behavioral and ecological outcomes (Waylen et al. 2010), this strategy was also proposed in the B. affinis review by Moll et al. (2015) in lieu of immediate solutions to poaching, habitat loss and sand mining that directly caused the decline of the wild populations. In fact, Horwich & Lyon (2007) documented numerous successful conservation projects that involved the participation of local communities.

One of the most important outcomes of this B. affinis conservation project was the formation of a group of “Terrapin Guardians” who prided themselves much with the work that they were involved with. Surprisingly, these “Terrapin Guardians,” who were not very highly educated, were able to follow instructions and perform scientific tasks in the absence of a researcher. This supports the assumption that the local community can be trained to be responsible over their own natural resources. Moreover, Waylen et al. (2010) also found that greater community participation is associated with intervention success. There are several possible explanations for this. Firstly, these local villagers had been poachers of B. affinis eggs for decades, and they could be more knowledgeable about the terrapins than any new researcher or conservationist; however, they may not be familiar with the science behind the conservation actions. Secondly, they felt empowered by being involved in a conservation project that helped to conserve a Critically Endangered species (Horwich & Lyon 2007).

The participation of the local community also brought about increased infrastructure to the village, such as improved roads, and a new hatchery for the conservation project; and civic pride among local villagers (Badrulhisyam B. Jusoh pers. comm. May 2015). This has led to more collaboration between the Village Development and Security Committee and project proponents in organizing community events such as “World Turtle Day” celebrations and reintroduction events. Additionally, this project has also garnered increased media attention to the local village, to the extent that the Village Committee has now adopted the B. affinis conservation project and has begun making plans to expand the conservation project. In May 2016, the Village Committee built a new hatchery for the project. Finally, the Village Committee also offered the project a utility room adjacent to the Community Hall, which we could turn into a Mini Terrapin Museum.

This project represents a vital partnership between the author and the Village Committee, local villagers, school students, and numerous volunteers, who share the same goal of conserving B. affinis, and we recognize that all involved must be a part of the solution (Bird et al. 2003). Presentations to government agencies and the public, as well as published newspaper and magazine articles have garnered support for the conservation project, ensuring the project’s long-term viability (see also Buhlmann et al. 2015). The above outcomes demonstrated that while the participation of the local community is not a simple prescription for guaranteed success (Adams & Hulme 2001), they suggest that community participation promotes conservation success (Campbell & Vainio-Mattila 2003). Despite these promising findings, further work is required to ensure the sustainability of the B. affinis conservation project. The analysis of ethnoecological knowledge and local management practices gives precise information on how local practices interact with the population ecology of the species considered (Ghimire et al. 2004). This is important because ultimately, for any conservation project to be successful and sustainable, it has to be internally driven and motivated, and the local communities are the best people to assume the responsibilities of taking charge of their own natural resources (Horwich & Lyon 2007). This case study could serve as a reference for future B. affinis conservation projects that involve the local communities in Malaysia.

 

Population size of B. affinis in Malaysia

This was the first study that attempted to systematically quantify the wild, female population of Batagur affinis through a mark-recapture study in the Kemaman River. By microchipping the nesting females, and recapturing them in subsequent years, we found that there are at least 186 wild, female B. affinis in the Kemaman River. Comparatively, there were approximately 30 females in the Setiu River; between 33 and 100 females in the Terengganu River, the longest river in the state; between 10 and 30 females in the Dungun River; and between 8 and 25 females in the Perak River, the most studied population. These estimates were, however, calculated from the number of wild-laid eggs or nests collected for incubation and by taking into consideration that B. affinis would deposit between one and three nest holes during each nesting event (see Loch 1950; Khan 1964; Moll 1978, 1980, 1985; Chan & Chen 2011), rather than a direct count of females captured. Despite the inconsistencies in the reporting units used, these reports revealed a drastic decline of wild B. affinis populations throughout its range (Kalyar et al. 2007; Moll et al. 2015). For example, Platt et al. (2008) reported that according to local villagers, small numbers of B. affinis (then called B. baska) were present in Tonle Sap in Cambodia during the early 1900s, but they were now locally extirpated. Hence, the findings from this study confirms the assumption that the Kemaman River harbors one of the largest B. affinis populations in Malaysia and throughout its global range (Platt et al. 2006).

Very little was found in the literature on the size and age of sexual maturity for female B. affinis. In the first record of the natural history of B. affinis, Moll (1980) suggested that females appeared to mature at around 45cm. Additionally, using the von Bertalanffy Growth Model, it was estimated that B. affinis took approximately 22 years to reach first maturity at 51cm (Eng Heng Chan et al. unpub.). The results from this study concur with both previous studies as the smallest post-nesting female B. affinis measured in the Kemaman River was 47.5cm SCL.

The present results are significant as they suggest that the Kemaman River harbors one of the largest populations of B. affinis in the country, and possibly throughout its range. This is important for conservation because knowledge of the status of this population provides the basis for more behavioral and ecological studies on B. affinis, and future conservation efforts. Further research should be undertaken to investigate the population size and demography of B. affinis in all the river systems in Malaysia.

 

Egg protection program

Prior to the initiation of this B. affinis egg protection program, local villagers collected all wild-laid B. affinis eggs for consumption. The eggs were considered a local delicacy and if sold in the market, could fetch a high price of approximately RM 5 each (US$ 1.60 in 2012). Hence, one of the initial objectives of this project was to document the B. affinis egg protection effort in the Kemaman River. One of the principal results of this study was that more than 2,542 B. affinis eggs were collected for incubation from 2012 to 2016 and this is interesting because it shows the willingness of the local community to give up consuming B. affinis eggs and instead incubate them for conservation purposes.

A few previous studies have documented B. affinis egg protection programs in various river systems in Malaysia (see Chan & Chen 2011) but this study provides the first report of such a program in the Kemaman River. We found a 70% drop in the number of nests and eggs collected from 2012 to 2013 (Table 3). There are several possible explanations for this. Firstly, it could be due to the major floods that occurred in December 2012, which was recognized as one of the worst floods in the area in recent years (Anon. 2012). In fact, 90% of the population of the village was evacuated to higher grounds (Mat Zaik b. Mohd. Yusof pers. comm. January 2013). The abnormal rise in the flood waters may have facilitated the movements of B. affinis from the Kemaman River over land and into unknown areas. Secondly, it could be a result of the removal of a fallen concrete bridge in the river, approximately 1.7km upstream from the B. affinis nesting bank. This fallen bridge had, in the past, constrained the upriver movements when female B. affinis migrate moderate to long distances upstream from feeding areas in the estuaries to the sand banks used for nesting (Moll 1980; Moll et al. 2015). Discussions with the “Terrapin Guardians” revealed that the fallen concrete bridge and concrete debris used to block the entire width of the river (approximately 60m), and because female B. affinis could not move upstream to nest on other potential nesting banks, they returned to our nesting bank throughout the nesting season (Mohd. Zulkifli b. Mohd. Noor pers. comm. May 2013). The concrete debris were removed by the authorities in 2012, and as such, in the subsequent nesting seasons, the terrapins were free to move along and nest in the other nesting banks further upriver.

Despite the drastic decrease in the number of nests and eggs, we recorded a consistent hatching success that ranged from 62.7–76.6% from 2012–2016. A possible explanation for the gradually increasing hatching success could be improved incubation techniques. In 2016, however, the hatching success dropped to 66.1% due to serious ant infestation at the hatchery. In fact, all nests undergoing incubation had to be relocated into individual buckets for the remaining incubation duration.

Nevertheless, the egg protection program has produced 1,723 B. affinis hatchlings in five years, which would not have been possible without intervention. Comparatively, only 1,477 B. affinis hatchlings have been produced from the Setiu River from 2004 to 2014 (Eng Heng Chan & Pelf Nyok Chen unpub.). This finding, while preliminary, again suggests that the Kemaman River possibly harbors the largest wild population of B. affinis in Malaysia. Despite these promising results, the egg protection program should be intensified, possibly to adjacent nesting banks, to increase recruitment into the Kemaman River.

 

Head starting and reintroductions

One of the primary objectives of this study was to head start B. affinis hatchlings in captivity until they outgrew the period of greatest vulnerability to predators, and then release them into the river in order to increase their survival in the wild (Heppell et al. 1996).

In this study, B. affinis eggs were collected and incubated in captivity, and the resulting hatchlings were released after a period of husbandry, that ranged from 18–21 weeks. My results showed that at the end of the head starting duration, B. affinis hatchlings showed a 467% increase in BM and 90% increase in SCL. The mean increase in BM recorded in this study (range 11.13–15.88 g/week) was consistent with that recorded by Chen (2008). The commercially available tilapia pellets that we used provided a nutritious diet and all hatchlings fed on it readily. In addition to tilapia pellets, various vegetables were introduced to the head started hatchlings to help provide a more balanced diet (Chen 2008). None of the head started hatchlings exhibited “pyramiding” or any visible clinical diseases before they were released.

Unlike most head starting programs where animals were raised between 9 and 12 months (Heppell et al. 1996; Herlands et al. 2004; Chen 2008; Buhlmann et al. 2015), B. affinis hatchlings in this study were only head started for four to five months before they were reintroduced. In spite of the relatively short head start duration, B. affinis hatchlings were raised to a size where they would only be predated upon by apex predators in the wild. These hatchlings could not be head started any longer due to the annual northeast monsoon that affects the entire village and project site from October/November to January/February. In fact, the project site was so badly flooded in December 2012 that the entire village was at least 2.5 m under water (Anon. 2012).

Conservation efforts that emphasized ex situ techniques such as hatcheries, head starting and captive breeding require decades to ascertain whether these strategies are effective (Moll et al. 2015). Conservationists have argued that unless the underlying causes of population decline such as poaching of large adults, habitat loss, etc. are addressed, head starting and releasing large numbers of juvenile terrapins into the environment is unlikely to reverse the downward population trends (Moll & Moll 2004; Burke 2015; Moll et al. 2015).

While this study does not offer a conclusive answer to the question of whether head starting is an effective conservation tool, it does allow conservationists to reintroduce larger individuals into the river, which in turn increases their chances of survival (Pritchard 1981). It would be fruitful to pursue further research which focuses on recapturing the head started B. affinis in order to determine their post-release adaptability, growth and survival. However, in the setting of a community-based conservation, we demonstrated that local villagers could be trained to manage head starting programs provided they are given sufficient training.

Survivorship during captivity ranged from 96.7−100 % among cohorts. However, there were no published reports on this or a closely related species that could be used as a basis for comparison. The mortality in this project did not result from accidents or negligence (Table 4). As annual survivorship in juvenile turtles appears to increase with age due to a reduced risk of predation of larger individuals (Frazer 1992), recovery programs such as head starting attempt to ameliorate low survivorship during early life history stages by raising hatchlings in captivity and releasing them only after they reach a larger size (Haskell et al. 1996). Despite the on-going debate on the efficacy of head starting as a conservation tool, I believe that it remains an important recruitment strategy in the absence of immediate solutions to causes of population declines.

Approximately 1,690 B. affinis hatchlings have been reintroduced into the Kemaman River from 2012–2016. Contrary to common practices where individuals were repatriated or relocated to a site where populations have been extirpated (Seigel & Dodd 2000), these hatchlings were released into the same locality where their eggs were laid. However, the efficiency of the head starting and reintroduction programs will not become apparent until the survivors breed as adults over 22 years later (Horwich & Lyon 2007; Eng Heng Chan et al. unpub.). Similar reintroduction programs that were successful were previously reported (Bell & Parsons 2002; Herlands et al. 2004; Buhlmann et al. 2015).

Our annual reintroductions involved mostly the local communities and included activities that spread conservation awareness as well as raised funds. The reintroduction events were heavily publicized and school children and members of the public were encouraged to participate. We also demonstrated to the local community the numerous benefits of conserving B. affinis. An example of another such program was reported by Wood & Herlands (1997) and Herlands et al. (2004) for Diamondback Terrapins in New Jersey, USA. These reintroductions provide an important avenue for promoting conservation, raising public awareness, educating the public (Stuart 1991; Lindburg 1992; Rahbek 1993; Wiese et al. 1996) and raising funds (Snyder et al. 1996; Wiese et al. 1996). Our symbolic Terrapin Adoption Program provided the public a platform to support our B. affinis conservation project by making a small donation, and funds generated were sufficient to ensure the sustainability of the project. Considering numerous conservation projects were terminated due to the lack of funds, the ability to sustain a long-term conservation project is extremely important to ensure the survival of a critically endangered species.

Wildlife reintroduction is a common conservation strategy (Anthony et al. 2015), in which individuals are moved from one locality to another (Seigel & Dodd 2000). Researchers have reintroduced numerous marine and freshwater turtles into the wild, either as a result of captive breeding, rehabilitation of diseased individuals and/or in an attempt in population recovery (Williams 1993; Wood & Wood 1993; Haskell et al. 1996). Common indicators of successful reintroductions includes positive survival and reproduction rates, establishment of viable wild and captive populations, increased population sizes, developed protocols, etc. Non-biological indicators include increased public and local stakeholder awareness and establishment of legal protection for the wildlife (Ewen et al. 2014). The only way to carry out a real evaluation of the reintroduction project is by long-term monitoring (Bertolero & Oro 2009).

Given the long maturation period for most chelonians, including B. affinis, Dodd & Seigel (1991) recommended that reintroduced turtles be monitored for at last 20 years. To determine the success of our head starting and reintroductions, further work is required to monitor the adaptation, survival, growth and movements of the post-release individuals. Without monitoring and an evaluation of the reintroduction programs, it is impossible to assess whether this is a successful strategy for the conservation of B. affinis. Additionally, future research should focus on the assessment and protection of the critical habitats in the river and address the underlying causes of population decline such habitat loss, the use of indiscriminate fishing gear, and the continued tradition of consuming B. affinis eggs among the older generation of local villagers.

 

 

REFERENCES

Adams, W.M. & D. Hulme (2001). If community conservation is the answer in Africa, what is the question? Oryx 35: 193–200; http://doi.org/10.1046/j.1365-3008.2001.00183.x

Anonymous (2012). Floods in Terengganu claims six lives. The Star.

Anonymous (2015). Populasi tuntung di Kemaman diancam kepupusan - NGO.

http://www.bharian.com.my/node/79946. Electronic version accessed 1 November 2016.

Anthony, T., J.D. Riedle, M.B. East, B. Fillmore & D.B. Ligon (2015). Monitoring of a reintroduced population of juvenile alligator snapping turtles. Chelonian Conservation and Biology 14: 43–48; http://doi.org/10.2744/1071-8443-14.1.43

Bell, C.D.L. & J. Parsons (2002). Cayman turtle farm head-starting project yields tangible success. Marine turtle newsletter 98: 5–6.

Bernstein, N.P. & J.L. Christiansen (2011). Response of a Yellow Mud Turtle (Kinosternon flavescens Agassiz) community to habitat change: management implications for a nature preserve. Natural Areas Journal 31: 414–419; http://doi.org/10.3375/043.031.0412

Bertolero, A. & D. Oro (2009). Conservation diagnosis of reintroducing Mediterranean pond turtles: what is wrong? Animal Conservation 12: 581–591.

Bird, K.E., W.J. Nichols & C. Tambiah (2003). The value of local knowledge in sea turtle conservation: a case from Baja California, Mexico. University of British Columbia Fisheries Centre Research Reports 11: 178–183.

Buhlmann, K.A., S.L. Koch, B.O. Butler, T.D. Tuberville, V.J. Palermo, B.A. Bastarache & Z.A. Cava (2015). Reintroduction and head-starting: tools for Blanding’s Turtle (Emydoidea blandingii) conservation. Herpetological Conservation and Biology 10: 436–454.

Burke, R.L. (2015). Head-starting turtles: learning from experience. Herpetological Conservation and Biology 10(Symposium): 299–308.

Campbell, L.M. & A. Vainio-Mattila (2003). Participatory development and community-based conservation: opportunities missed for lessons learned? Human Ecology 31: 417–437.

Chan, E.H. & P.N. Chen (2010). Elevating survival prospects for critically endangered river terrapins of Terengganu through research, conservation, community participation, outreach and education. A Final Report submitted to the United States Fish and Wildlife Services, USA.

Chan, E.H. & P.N. Chen (2011). Nesting activity and clutch size of Batagur affinis edwardmolli from the Setiu River, Terengganu, Malaysia. Chelonian Conservation and Biology 10: 129–137.

Chen, P.N. (2008). Head-starting of river terrapins (Batagur baska): Feeding trials of hatchlings and juveniles. Master’s Thesis. Institute of Oceanography, Universiti Malaysia Terengganu, 158pp.

Chen, P.N. & E.H. Chan (2014). High hatch rates in Malaysian river terrapin program are cause for optimism. Turtle Survival, USA.

Dodd, C.K.J. & R.A. Seigel (1991). Relocation, repatriation, and translocation of amphibians and reptiles: are they conservation strategies that work? Herpetologica 47: 336–350.

Dutton, P.H., C.P. Whitmore & N. Mrosovsky (1985). Masculinisation of leatherback turtle Dermochelys coriacea hatchlings from eggs incubated in styrofoam boxes. Biological Conservation 31: 249–264.

Ewen, J.G., P.S. Soorae & S. Canessa (2014). Reintroduction objectives, decisions and outcomes: global perspectives from the herpetofauna. Animal Conservation 17: 74­–81; http://doi.org/10.1111/acv.12146

Frazer, N.B. (1992). Sea turtle conservation and halfway technology. Conservation Biology 6:179-184.

Garcia, A., G. Ceballos & R. Adaya (2003). Intensive beach management as an improved sea turtle conservation strategy in Mexico. Biological Conservation 111: 253–261.

Ghimire, S.K., D. McKey & Y. Aumeeruddy-Thomas (2004). Heterogeneity in ethnoecological knowledge and management of medicinal plants in the Himalayas of Nepal: implications for conservation. Ecology and Society 9: 6.

Granzow, E. (2008). Microchip placement for identification of birds. Lab animal 37: 21.

Hamilton, R.J., T. Potuku & J.R. Montambault (2011). Community-based conservation results in the recovery of reef fish spawning aggregations in the Coral Triangle. Biological Conservation 144: 1850–1858; http://doi.org/10.1016/j.biocon.2011.03.024

Haskell, A., T.E. Graham, C.R. Griffin & J.B. Hestbeck (1996). Size related survival of headstarted redbelly turtles (Pseudemys rubriventris) in Massachusetts. Journal of Herpetology 30: 524–527.

Hellebuyck, T., F. Pasmans, A. Van Caelenberg, M. van Looy & A. Martel (2013). Assessing the use of microchip transponders as a marking method in juvenile Hermann’s Tortoises (Testudo hermanni). Journal of Herpetological Medicine and Surgery 23: 32–36; http://doi.org/10.5818/1529-9651-23.1.32

Heppell, S.S., L.B. Crowder & D.T. Crouse (1996). Models to evaluate headstarting as a management tool for long-lived turtles. Ecological Applications 5: 556–565. Proceedings of the Diamondback terrapin (Malaclemys terrapin) head-starting project in Southern New Jersey: 2004.

Horwich, R.H. & J. Lyon (2007). Community conservation: practitioners’ answer to critics. Oryx 41: 376–385.

Husin, S. (2016). Aktiviti korek pasir sungai ancam tuntung. Berita Harian 29.

Kalyar, J. Thorbjarnarson & K. Thirakhupt (2007). An overview of the current population and conservation status of the Critically Endangered River Terrapin, Batagur baska (Gray, 1831) in Myanmar, Thailand and Malaysia. The Natural History Journal of Chulalongkorn University 7: 51–65.

Khan, M.K.M. (1964). A note on Batagur baska (the river terrapin or tuntung). Malayan Nature Journal 18: 184–186.

Krebs, C.J. (1989). Ecological methodology. Harper & Row, New York,

Lindburg, D.G. (1992). Are wildlife reintroductions worth the cost? Zoo Biology 11: 1–2.

Loch, J.H. (1950). Notes on the Perak River turtle. Malayan Nature Journal 5: 157–160.

Malaysia (2010). Profil Daerah Kemaman.

Mitrus, S. (2005). Headstarting in European Pond Turtles (Emys orbicularis): Does it work? Amphibia-Reptilia 26: 333–341.

Moll, D. & E.O. Moll (2004). The Ecology, Exploitation and Conservation of River Turtles. Oxford University Press, Inc., New York, USA, 393.

Moll, E.O. (1978). Drumming along the Perak. Natural History 87: 36–43.

Moll, E.O. (1980). Natural history of the River Terrapin, Batagur baska (Gray) in Malaysia (Testudines: Emydidae). Malaysian Journal of Science 6: 23–62.

Moll, E.O., S.G. Platt, E.H. Chan, B.D. Horne, K. Platt, P. Praschag, P.N. Chen & P.P. van Dijk (2015). Batagur affinis (Cantor 1847) - Southern River Terrapin, Tuntong. Conservation Biology of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Monographs 5(8): 090.1–17; http://www.iucn-tftsg.org/batagur-affinis-090/ Electronic version accessed 4 January 2017.

Mrosovsky, N. (2008). Against oversimplifying the issues on relocating turtle eggs. Environmental management 41: 465–467.

Nichols, W.J., K.E. Bird & S. Garcia (2000). Community-based research and its application to sea turtle conservation in Bahia Magdalena, BCS, Mexico. Marine turtle newsletter 89: 4–7.

Our Better World. (2015). Have you ever seen a terrapin smile? http://www.ourbetterworld.org/en/story/have-you-ever-seen-terrapin-smile. Electronic version accessed 1 November 2016.

Platt, K., S.G. Platt, K. Thirakhupt & T.R. Rainwater (2008). Recent Records and Conservation Status of the Critically Endangered Mangrove Terrapin, Batagur baska, in Myanmar. Chelonian Conservation and Biology 7: 261–265; http://doi.org/10.2744/CCB-0701.1

Platt, S.G., D. Hendrie, E.H. Chan, B. Poynter, K. Platt, H. Sovannara, R. Holloway, M.M. Khin, P.N. Chen & C.L. Soh (2006). Batagur baska: A Status Review and Conservation Action Plan.

Platt, S.G., B.L. Stuart, H. Sovannara, L. Kheng & H. Kimchhay (2003). Rediscovery of the critically endangered river terrapin, Batagur baska, in Cambodia, with notes on occurrence, reproduction, and conservation status. Chelonian Conservation and Biology 4: 691–694.

Praschag, P., A.K.Hundsdörfer & U. Fritz (2007). Phylogeny and taxonomy of endangered South and Southeast Asian freshwater turtles elucidated by mtDNA sequence variation (Testudines: Geoemydidae: Batagur, Callagur, Hardella, Kachuga, Pangshura). Zoologica Scripta 36: 429–442; http://doi.org/10.1111/j.1463-6409.2007.00293.x

Praschag, P., R.S. Sommer, C. McCarthy, R. Gemel & U. Fritz (2008). Naming one of the world’s rarest chelonians, the southern Batagur. Zootaxa 1758: 61–68.

Pritchard, P.C.H. (1981). Criteria for scientific evaluation of head-starting. Marine turtle newsletter 19: 3–4.

Rahbek, C. (1993). Captive breeding - a useful tool in the preservation of biodiversity? Biodiversity and Conservation 2: 426–437.

Renner, M. & S. Lloyd (2000). Marking penguins with implanted transponders. Notornis 47: 163–165.

Seigel, R.A. & C.K.J. Dodd (2000). Manipulation of turtle populations of conservation: halfway technologies or viable options? pp. 218–238. In: Klemens, M.W. (eds.). Turtle Conservation. Smithsonian Institution Press, Washington, D.C.

Şekercioğlu, C.H. (2012). Promoting community-based bird monitoring in the tropics: Conservation, research, environmental education, capacity-building, and local incomes. Biological Conservation 151: 69–73; http://doi.org/10.1016/j.biocon.2011.10.024

Snyder, N.F.R., S.R. Derrickson, S.R. Beissinger, J.W. Wiley, T.B. Smith & W.D. Toone (1996). Limitations of captive breeding in endangered species recovery. Conservation Biology 10: 338–348.

Soh, C.L. (2004). A study on distribution, movement and growth of captive-raised River Terrapin (Batagur baska) and Wild Painted Terrapin (Callagur borneoensis) in Setiu River. Bachelor of Science in Marine Biology. Faculty of Science and Technology, Kolej Universiti Sains dan Teknologi Malaysia, 70pp.

Strusaker, T.T., P.J. Strusaker & K.S. Siex (2005). Conserving Africa’s rain forests: problems in protected areas and possible solutions. Biological Conservation 123: 45–54.

Stuart, S.N. (1991). Reintroductions: to what extent are they needed? Symposia of the Zoological Society London 62: 27–37.

Turtle Conservation Coalition (2011). Turtles in Trouble: The World’s 25+ Most Endangered Tortoises and Freshwater Turtles - 2011. Lunenburg, MA: IUCN/SSC Tortoise and Freshwater Turtle Specialist Group, Turtle Conservation Fund, Turtle Survival Alliance, Turtle Conservancy, Chelonian Research Foundation, Conservation International, Wildlife Conservation Society, and San Diego Zoo Global, 54pp.

Vieitas, C.F., G.G. Lopez & M.A. Marcovaldi (1999). Local community involvement in conservation - the use of mini guides in a programme for sea turtles in Brazil. Oryx 33: 127–131.

Waylen, K.A., A. Fischer, P.J.K. McGowan, S.J. Thirgood & E.J. Milner-Gulland (2010). Effect of local cultural context on the success of community‐based conservation interventions. Conservation Biology 24: 1119–1129; http://doi.org/10.1111/j.1523-1739.2010.01446.x

Webb, J.K. & R. Shine (1998). Using thermal ecology to predict retreat-site selection by an endangered snake species. Biological Conservation 86: 233–242.

Wiese, R.J., K. Willis & M. Hutchins (1996). Conservation breeding in 1995: an update. Trends in Ecological Evolution 10: 218–219.

Williams, P. (1993). NMFS to concentrate on measuring survivorship, fecundity of head-started Kemp’s ridleys in the wild. Marine turtle newsletter 63: 3–4.

Wood, F. & J. Wood (1993). Release and recapture of captive-reared green sea turtles, Chelonia mydas, in the waters surrounding the Cayman Islands. Herpetological journal 3: 84–89.

Wood, R.C. & R. Herlands (1997). Turtles and tires: The impact of roadkills on northern Diamondback Terrapin, Malaclemys terrapin terrapin, populations on the Cape May Peninsula, Southern New Jersey, USA. In: Abbema, V. (ed.). Proceedings of the Turtles and Tires: The Impact of Roadkills on Northern Conservation, Restoration and Management of Tortoises and Turtles - An International Conference. New York Turtle and Tortoise Society, New York, USA.

Yaacob, W.Z.W. (2015). Tuntung Makin Pupus. Utusan Malaysia, Timur, 26pp.

Yusof, S.A.M. (2016). Tuntung Sungai Kemaman: Disenarai 25 hidupan terancam di dunia. Kosmo! K2: 21–23.