Distribution, threats and ecology of black breasted leaf turtle (geoemyda spengleri gmelin, 1789) in tay yen tu nature reserve, bac giang province, viet nam with notes on other sympatric species

MINSTRY OF EDUCATION AND TRAINING MINISTRY OF AGRICULTURE AND RURAL DEVELOPMENT VIETNAM NATIONAL UNIVERSITY OF FORESTRY PHAM VAN THONG DISTRIBUTION, THREATS AND ECOLOGY OF BLACKBREASTED LEAF TURTLE (Geoemyda spengleri GMELIN, 1789) IN TAY YEN TU NATURE RESERVE, BAC GIANG PROVINCE, VIETNAM, WITH NOTES ON OTHER SYMPATRIC SPECIES MASTER THESIS IN FOREST SCIENCE Hanoi, October 2018 MINISTRY OF EDUCATION AND TRAINING MINISTRY OF AGRICULTURE AND RURAL DEVELOPMENT VIETNAM NATIONAL UNIVERSITY OF FORESTRY  PHAM VAN THONG DISTRIBUTION, THREATS AND ECOLOGY OF BLACKBREASTED LEAF TURTLE (Geoemyda spengleri GMELIN, 1789) IN TAY YEN TU NATURE RESERVE, BAC GIANG PROVINCE, VIETNAM, WITH NOTES ON OTHER SYMPATRIC SPECIES Major: Forest Science Code: 8620201 MASTER THESIS IN FOREST SCIENCE Academic advisor: Dr Luu Quang Vinh Prof Dr Thomas Ziegler Signature: Hanoi, October 2018 ABSTRACT Ranking as number 9th in the top of the world, Vietnam is one the most biodiverse countries in terms of turtle species richness, with 27 species being tortoise and freshwater turtle However, the natural history of all of these species is very little known, but it is thought that the great majority of them are heavily threatened by habitat loss and overhunting Here, this study provides the primarily information from research (based on both interviews local people and field survey through the forest) in the Tay Yen Tu Nature Reserve, Bac Giang Province, Vietnam in order to collect natural history information (distribution, ecology and threats) on Geoemyda spengleri There were at least 10% (n=72) of the interviewees recognized 12 species It includes G spengleri, C mouhotii, C cyclornata, C galbinifrons, I elongata, P steindachneri, P sinensis, P megacephalum, S quadriocellata, M mutica, C zhoui, C oldhamii G spengleri and C mouhotii were by far the most frequently cited species by interviewees, and were also dominant in a sample of 40 turtle individuals that were observed on local trade These two species were also observed during field transects (seven G spengleri and one C mouhotii) It is the first record of the G spengleri population and its co-occurrence in Tay Yen Tu NR Individuals of G spengleri were observed from 10:47-13:45 hour, in all cases in sunny weather after rains, at 25-300C temperature range G spengleri was seen in montane bamboo forests at elevation range from 651m-725m, often inside or nearby rocky caves, and in sites with forest cover being 70%-90%, at slope angles varying from to 45 degrees While C mouhotii was recorded at 607m a.s.l during the sunny with forest cover is 50% This study is also estimated the population size of G spengleri in Tay Yen Tu NP range from 620-1849 individuals Key words: Tay Yen Tu Nature Reserve, Geoemyda spengleri, first record, cooccurrence i CONTENTS ABSTRACT i CONTENTS ii ABBREVIATIONS iii LIST OF FIGURES iv LIST OF TABLES v I INTRODUCTION II LITERATURE REVIEW 2.1 Chelonian research in the world 2.2 Chelonian research in Vietnam 2.3 Study species 16 III METHODOLOGY 17 3.1 Study sites 17 3.2 Data collection 19 3.2.1 Interview surveys 19 3.2.2 Field surveys 21 3.2.3 Species distribution and population status 23 3.2.4 Threats 24 3.2.5 Statistical analyses 25 IV RESULTS 26 4.1 Tay Yen Tu NR‟s species composition and status 26 4.2 Field surveys 29 4.2.1 General findings 29 4.2.2 Species ecology 30 4.3 Threats 36 4.3.1 Online trade 36 4.3.2 Threats to G spengleri population and sympatric species in Tay Yen Tu NR 37 V DISCUSSION 39 5.1 Chelonian co-occurrence species status in trade in Tay Yen Tu NR 39 5.2 The wild G spengleri population status 40 5.3 Species ecology 40 5.4 Threats 42 5.5 Recommendations 43 VI CONCLUSIONS 45 ACKNOWLEDGEMENTS 47 REFERENCES 49 ii ABBREVIATIONS a.s.l Above sea level ArcGIS ATP Geographic information system Asian Turtle Program BBLT BHS CITES Black-breasted leaf turtle Biodiversity hotspots Convention on International Trade in Endangered Species of Wild Fauna and Flora Carapace length Critically Endangered Critically Endangered (Possibly Extinct) Critically Endangered (Possibly Extinct in the Wild) Carapace width Data deficient Digital elevation model Degree of freedom Endangered Education for Nature of Vietnam Extinct Global Positioning System High-biodiversity wilderness areas Identify International Union for Conservation of Nature Least Concern Non-Government organization Nature reserve Near threatened Probability Turtle conservation center Traditional Chinese medicine Tortoise and freshwater turtle Tortoise and freshwater turtle specialist group Turtle priority areas United State American Vietnam National University of Forestry Vulnerable CL CR CR(PE) CR(PEW) CW DD DEM Df EN ENV EX GPS HBWA ID IUCN LC NGO NR NT P TCC TCM TFT TFTSG TPA USA VNUF VU iii LIST OF FIGURES Figures Contents Page number Figure Map of turtle diversity countries in the world Source: Mittermeier et al., 2015 Figure Distribution of G spengleri in Vietnam and China and Laos 16 Source: Turtle Taxonomy Working Group et al.,2017 Figure Map of Tay Yen Tu Nature Reserve 17 Figure Forest in Tay Yen Tu Nature Reserve 19 Figure Map of Vietnam, showing the position of the interview 29 points and of the presence sites of turtles at the Tay Yen Tu NR The field survey tracks are also indicated Figure Bamboo forest (Arundinaria sp.) where is the „favorite‟ 30 habitat for G spengleri in Tay Yen Tu NR Figure Black-breasted leaf turtle (Geoemyda spengleri) in the wild 31 (male at above, and female at below) Figure A single C mouhotii found in forest by hunting dog 32 Figure G spengleri population structure in Tay Yen Tu NR 33 Figure 10 Predicting potential distribution map of G spengleri in Tay 35 Yen Tu NR region Figure 11 73 individuals of G.spengleri were offered for sell by Facebook in Quang Ninh province in October 2017 iv 36 LIST OF TABLES Tables Table Table Table Contents Top countries in term of tortoise and freshwater turtle taxon richness Source: Mittermeier et al., 2015 Number of TFT trade from farm in China Source: Haitao et al., 2008 List of TFT species within Vietnam Source: Turtle Page number 14 Taxonomy Working Group et al., 2017 Table Synopsis of the places where turtle individuals were observed 28 during the interview surveys Table Synopsis of body measurements (mean ± Standard Deviation) taken from both wild-caught and traded turtle individuals at the study area v 33 I INTRODUCTION The Socialist Republic of Vietnam is ranked 9th among the most biodiverse countries of the world in terms of turtle species richness with a total of 32 species, 27 being freshwater and terrestrial and being marine (Dijk et al., 2014) Unfortunately, the conservation status of the Vietnamese turtle fauna is uncertain as 85.1% of the native freshwater and terrestrial taxa are currently listed as Threatened in the IUCN Red List (IUCN, 2018) For most species, habitat loss and overhunting (for consumption as human food, traditional medicine, religious merit) have been the main threats (Stanford et al., 2018) Indeed, the forest cover in Vietnam has decreased from 43% to 36% from 1945-1990 (De Jong & Hung, 2006) Although the country‟s forest cover has been recently increased due to the national-scale reforestation of Vietnam since 1992 that is assumed to contribute to this recovery, the forest quality still remains poor (Meyfroidt & Lambin, 2009) Indeed, the recovery of forest coverage was due in part to the ban of industrial logging from natural areas and the displacement of wood extraction to neighboring countries, but mainly to extensive programs of homogenous tree plantations (Meyfroidt & Lambin, 2009) These plantation habitats are clearly unsuitable for turtles, whereas the suitable remnant natural forest is still heavily fragmented and isolated (Fox et al., 2004) The second main threat to Vietnamese turtles is trade for domestic consumption, with massive numbers of individuals being exploited in the 1980s2000s (Van Dijk et al., 2000; Nijman, 2010) also to supply the food and traditional medicine markets of China (Cheung and Dudgeon, 2006; Turtle Conservation Fund, 2002) According to IUCN (2018) assessments, the populations of most Vietnamese turtle species have declined by about 50-90% The Black-breasted leaf turtle (Geoemyda spengleri), that is the main target of this study, is not an exception (however, we also present some remarks on the other sympatric turtle species) The Black-breasted leaf turtle (Geoemyda spengleri) (Figure 1) is among the smallest Geoemydidae species worldwide It is native to southern China, Northern Vietnam and Laos (Yasukawa and Ota, 2010; Turtle Taxonomy Working Group et al., 2017), and is classified as Endangered by IUCN (2018) due to habitat loss and trade (Gong et al., 2005, 2009) However, the species‟ population size in the wild and the distribution are poorly known (for instance, G spengleri has recently been also recorded in Laos (Stuart et al., 2011), with no ecological study published so far (Yasukawa & Ota, 2010) and with behavioral data being recorded only in ex-situ research (Henze et al., 2004) In Vietnam, the presence of G spengleri has been documented in Tam Dao National Park, (Bourret, 1934; Nguyen & Ho 1996; Yasukawa et al., 2001), Tuyen Quang, Son La, Yen Bai, Vinh Phuc, Bac Giang, Quang Ninh, Thanh Hoa, Nghe An, and Ha Tinh provinces (Bourret, 1934; Le, 2001; Nguyen et al., 2010) The southernmost boundary of its distribution range lies in Da Nang and Quang Nam Provinces (Le, 2000; Le & Nguyen, 2003) However, the coastal city of Da Nang may serve as a collection center rather than a field locality (Yasukawa and Ota, 2010) Few conservation actions have been implemented to manage the remnant free-ranging populations of this species Our aim in this study is to present some natural history data on G spengleri in a protected area of Vietnam (Tay Yen Tu Nature Reserve) in the hope to contribute to a better understanding of the field ecology and conservation of this threatened turtle species, and also to give some additional notes on the turtle fauna of the study area In detail the thesis goal aim to provide scientific information on species distribution, population status, threats, ecology and distribution of G spengleri within Tay Yen Tu Nature Reserve To archive the goal there are several objectives that the study needs to reach: (1) provide basic scientific data on the animal ecology and habitat condition to improve captive management of the ex-situ populations; (2) better understand the threats to the species to enhance enforcement; (3) determine the population status in the protected area to provide the scientific information in order to give recommendation the conservation actions II LITERATURE REVIEW 2.1 Chelonian research in the world Turtle is unique group of Reptile class with special body design to against the predators and survival for million years Oldest turtle fossil sample has recognized to live in Upper Triassic from approximate 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Clark, E.E., Buhlmann, K.A., Gibbons, J.W., 2005 Translocation as a conservation tool: site fidelity and movement of repatriated gopher tortoises (Gopherus polyphemus) Animal Conservation 8, 349–358 Turtle Taxonomy Working Group, Rhodin AGJ, Iverson JB, Bour R, Fritz U, Georges A, Shaffer HB, van Dijk PP, 2017 Turtles of the World: Annotated Checklist and Atlas of Taxonomy, Synonymy, Distribution, and Conservation Status (8th Ed.) 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spp.) on Hainan Island, China Chelonian Conservation Biology 16, 236–238 Yasukawa, Y., Hirayama, R., Hikida, T., 2001 Phylogenetic relationships of geoemydine turtles (Reptilia: Bataguridae) Current Herpetological 20, 105– 133 57 Yasukawa, Y., Ota, H., 2010 Geoemyda spengleri (Gmelin 1789) – Black-Breasted Leaf Turtle Chelonian Research Monograph No 5, 047.1-047.6 Yiming, L., Dianmo, L., 1998 The dynamics of trade in live wildlife across the Guangxi border between China and Vietnam during 1993–1996 and its control strategies Biodiversity Conservation 7, 895–914 58 APPENDIX Appendix Synopsis of the results of the interview surveys at Tay Yen Tu Nature Reserve, by species and by type of usage as declared by the hunters/traders, including the turtle price No Individuals = Number of turtle individuals observed during the interview surveys; Pet = number of individuals used as pet; For sale = number of individuals that will be sold in China; Food = number of individuals used as food; Medicine = number of individuals used for traditional medicine; No People confirming presence = number of interviewees (and their relative percentage, %; total n = 72) claiming the presence of the various turtle species at the study area The price of C cyclornata and C zhoui claimed to be 1990s, the rest are current price Species No Individuals Geoemyda spengleri 10 Cuora mouhotii 14 Cuora cyclornata Cuora galbinifrons Indotestudo elongata Palea steindachneri Pelodiscus sinensis Platysternon megacephalum Sacalia quadriocellata Mauremys mutica Cuora zhoui Cyclemys oldhamii Total 40 Pet Sell to China Food Medicine No People confirming presence 0 30 12 0 32 0 1 18 0 20 0 15 0 0 10 0 0 11 0 0 0 0 0 0 23 59 % Price range ($) 41.7 4.55-9.09 44.4 27.27-40.92 9.7 3076.90- 3846.12 25.0 68.13-150.00 1.4 unknown 27.8 29.50-31.82 20.8 22.72-27.27 13.9 181.81-227.22 15.3 90.90-136.31 6.9 unknown 2.8 307.61-1538.42 2.8 90.91 Appendix Synopsis of the number of interviewees, divided by their commune of residence and by declared profession Communes Thanh Son Town Tuan Mau Tuan Dao An Chau town An Lac Thanh Luan An Lap Long Son Truong Son Nghia Phuong Vo Tranh District Son Dong Son Dong Son Dong Son Dong Son Dong Son Dong Son Dong Son Dong Lục Nam Lục Nam Lục Nam Total n Hunt ers Trad ers Traditional medicine collectors Oth er Tot al 2 16 2 11 1 0 3 1 0 0 0 0 12 16 38 72 60 Appendix Synopsis of the raw data concerning the wild turtle individuals that were observed during the present study Precise geographic coordinates are not reported for conservation reasons, but are available on request from the authors T = ground temperature, Alt = elevation (m a.s.l.), CL = carapace length, CW = carapace width Date Time T (°C) Species name 25-Jul-18 12:35 Cuora mouhotii 29,00 mouhotii 24-Jul-18 13:45 Geoemyda 26,00 spengleri 24-Jul-18 11:20 Geoemyda 25,00 spengleri 24-Jul-18 11:44 Geoemyda 25,00 spengleri 24-Jul-18 11:07 Geoemyda 26,00 spengleri 24-Jul-18 13:20 Geoemyda 26,00 spengleri 22-Jul-18 10:47 Geoemyda 27,00 spengleri 22-Jul-18 12:30 Geoemyda 30,00 spengleri Location Ong Van slope, Tay Yen Tu Nature reserve, Tuan Mau commune, Son Dong district, Bac Giang province Đá Chồng Forest, Tay Yen Tu NR, Tuấn Mậu commune, Sơn Động district, Bắc Giang province Đá Chồng Forest, Tay Yen Tu NR, Tuấn Mậu commune, Sơn Động district, Bắc Giang province Đá Chồng Forest, Tay Yen Tu NR, Tuấn Mậu commune, Sơn Động district, Bắc Giang province Đá Chồng Forest, Tay Yen Tu NR, Tuấn Mậu commune, Sơn Động district, Bắc Giang province Đá Chồng Forest, Tay Yen Tu NR, Tuấn Mậu commune, Sơn Động district, Bắc Giang province Núp Vung Forest, Thanh Luận commune, Sơn động district, Bắc Giang Province Núp Vung Forest, Thanh Luận commune, Sơn động district, Bắc Giang Province Alt (m) CL (mm) CW (mm) Shell height (mm) weight Age (g) Gender classify Habitat type Forest Slope cover 607 171 109 56 538 M Adult Herb bush 50 725 43 36 1,6 11 unk hatching Bamboo forest 45 90 724 89 68 35 98 F Adult Rocky cave 10 70 724 78 56 28 49 M Sub-adult Rocky cave 70 710 96 6,9 36 107 F Adult Bamboo forest 75 705 55 43 23 26 F Juvenile Rocky cave 45 80 651 100 65 42 94 M Adult Bamboo forest 25 80 659 86 59 38 96 F Adult Bamboo forest 35 70 61 Appendix 4: Different type of habitat that found G spengleri Above: found on the ground, below: found on rocky cave 62 Appendix 5: Searching effort by dog hunting (left) and by human (right) 63 Appendix 6: Interview survey found 01 C mouhotii, 04 C galbinifrons, 01 P sinensis (above photo) and 01 C cyclornata (below photo) were eaten by local hunter in Dong Ri town, Son Dong district, Bac Giang Province 64 Appendix 7: Some other findings from interview surveys Top left: G spengleri found in local house with big broken on real of carapace due to dog hunting bitten Top right: one of P steindachneri found in local house for food consumption Middle left: two of C mouhotii found in local trader house Middle right: A P sinensis found in local house for food consumption Last: of G spengleri found in local trader house in Thanh Son town, Son Dong district, Bac Giang province 65 Appendix 8: The author Pham Van Thong who is principal investigator for this study Top: Thong is collecting the data of a dead C galbinifrons at local house Below: Thong is conducting interview a local people at Tuan Mau commune, Thanh Son district, Bac Giang province Photo: Bui Thanh Tung 66 Appendix 9: Field record form Source: Asian Turtle Program Tortoise and Freshwater Turtle Field Record Report Species Local name Date of observation: Record Number (please leave blank) Location and Reporting Information (required) Name of Location (site name) District Province Country Reported by (name and organization/institution) 10 Identified by (include name and organization/affiliations) Record Type and Classification (required) 11 Observation Type (circle one): Unknown 12 Voucher type (circle): sample A Live specimen B Dead specimen Photograph attached C Shell, skull, remains Specimen/remains None D blood/tissue 13 Classification of Report       A1 Observed in the Wild A2 Observed in possession of hunter/fisherman/other person(s) within the source area B1 Observed in captivity within a community in close proximity to the source area B2 Observed in local trade C1 Reported in interview C2 Site-specific record from report or other source without further reference Other information (if available/optional) 14 Age class: Adult Sub-adult 16 Length (carapace mm) Juvenile Hatchling Unknown 17 Width (carapace mm) 19 Additional locality information (forest, wetland, village, commune, ethnic group, etc.) Address: Name: Age: Ethnicity: Profession: 15 Sex: Unknown Male Female 18 Weight (g) 20 GPS Coordinates (if known) UTM – WGS84 Geogra phic WGS8 Altitude: Altitude : 21 Describe circumstances of observation/report (provide more details about the situation of turtle observation, source of turtle, price, quantity,…) 22 Wild observation (Air temperature 0C, water temperature 0C, relative humidity %, slope, forest cover,….) Photograph (if available) 23 Insert digital photograph here Report by: _ 67 Date: Appendix 10: Measurement variable of turtle Dimension measurements Length of carapace (L.ca) Height of carapace (H.ca) Middle Width of carapace (MidW.ca) Width of gular (P.G) Width of humeral (P.H) Width of pectoral (P.P) Width of abdominal (P.AB) Width of femoral (P.F) Width of anal (P.AN) Plastron’s length (PL) Length of gular (L.G) Length of humeral (L.H) Length of pectoral (L.P) Length of abdominal (L.AB) Length of femoral (L.F) Length of anal (L.AN) Length of tail (L.cd) Max Width of Carapace (MaxW.Ca) 68 Appendix 11: Percentage of turtle use purpose among villagers Percentage of turtle use purpose 15% 12% Pet 17% Sell to China 56% Eat Medicine 69