Abstract
Almost all Asian turtle species are considered threatened by the World Conservation Union (IUCN). We investigated the turtle fauna and their distribution in hilly forests in northern Vietnam (TamThanh commune, Quan Son district) during two consecutive periods (12th–23th May, 12th–24th August 2019). These forests are of Subtropical Moist Forest type according to WWF, and dominated by evergreen and semi-evergreen forests. We used a combination of (1) field surveys; (2) hunter interviews; (3) examination of hunter quarry, and (4) monitoring of hunting activity. We performed field surveys in bamboo and hilly secondary forests (500–1350 m), applied 103 hunter interviews, and examined the same number of hunter bags. We found a total of 124 different individuals of as many as 9 turtle species (representing 18% of the currently known total chelonian fauna in the Indo-Burma region). Two species were the most dominant, the Impressed tortoise (Manouria impressa), found mostly as shells in villages, and the Indochinese box turtle (Cuora galbinifrons) sighted inside bamboo forests at different elevations. C. galbinifrons is one of the most critically endangered turtle species in the world. Given that there are still large expanses of unexplored bamboo forests and mixed bamboo—evergreen forest (over 5 million hectares) remaining throughout northern Vietnam, if our results are typical of other similar habitats, it is likely that C. galbinifrons may be more common than currently assessed. We suggest that field surveys should be conducted as soon as possible to confirm whether these turtles are as seriously threatened as presently considered by the IUCN.
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References
Akani GC, Barieenee IF, Capizzi D, Luiselli L (1999a) Snake communities of moist rainforest and derived savanna sites of Nigeria: biodiversity patterns and conservation priorities. Biodivers Conserv 8:629–642
Akani GC, Luiselli L, Politano E (1999b) Ecological and conservation considerations on the reptile fauna of the eastern Niger Delta (Nigeria). Herpetozoa 11:141–153
Ben A, John BI (2012) Mauremys nigricans (Grey 1834)—Red-necked pond turtle, Chinese Red-necked turtle, Kwangtung river turtle, Black-necked pond turtle. Conservation Biology of Freshwater Turtles and Tortoises. A compilation project of the IUCN/SSC tortoise and freshwater turtle specialist group, pp 1–9
Ben-Zhi Z, Mao-Yi F, **-Zhong X, **ao-Sheng Y, Zheng-Cai L (2005) Ecological functions of bamboo forest: research and application. J For Res 16:143–147
Blanck T (2013) Zu Besuch bei Cuora galbinifrons auf Hainan, China. Reptilia) 18(99):100–109
Bouret R (1941) Les tortues de l'Indochine avec une note sur la pêche et l'élevage des tortues de mer par F. Le Poulain. Saigon, Gouvernement Général de l'Indochine, 235pp. (Institut Océanographique de l'Indochine. Station Maritime de Cauda, Nha Trang, Viet Nam, Note, 38)
Cheung SM, Dudgeon D (2006) Quantifying the Asian turtle crisis: market surveys in southern China, 2000–2003. Aquat Conserv 16:751–770
Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:2717–2727
Das I, McCormack T, van Dijk PP, Hoang HV, Struijk R (2016) Cuora mouhotii (Gray 1862)—Keeled Box Turtle. In: Rhodin AGJ, Pritchard PCH, van Dijk PP, Saumure RA, Buhlmann KA, Iverson JB, Mittermeier RA (eds) Conservation biology of freshwater turtles and tortoises: a compilation project of the IUCN/SSC Tortoises and Freshwater Turtles Specialist Group. Chelonian Research Monographs 5(9): 099.1–12
Douglas H, Bui DP, Timothy EM, Hoang HV, Van Dijk PP (2011) Vietnam’s tortoises and freshwater turtles—identification book (Vietnamese)
Fritz U, Ziegler T, Herrmann H, Lehr E (2002) Intergradation between subspecies of Cuora galbinifrons (Bourret, 1939) and Pyxidea mouhotii (Gray, 1862) in southern North Vietnam (Reptilia: Testudines: Geoemydidae). Faunistische Abhandlungen. Staatliches Museum für Tierkunde in Dresden 23:59–74
Hendrie DB (2000) Status and conservation of tortoises and freshwater turtles in Vietnam. In: Presented at the Asian turtle trade: proceedings of a workshop on conservation and trade of freshwater turtles and tortoises in Asia. Chelonian Research Monographs, pp 63–73
Hendrie D (2001) FFI progress reports—turtle conservation and ecology project. Indochina
Hendrie DB, Trang N (2000) Compiled notes on the wildlife trade in Vietnam
Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJ (2001) Counting the uncountable: statistical approaches to estimating microbial diversity. Apply Environ Microbiol 67:4399–4406
IUCN (2016) Cuora galbinifrons: McCormack T, Shi H, Stuart B: The IUCN Red List of Threatened Species 2016: e.T97357437A3078734. https://doi.org/10.2305/IUCN.UK.2016-1.RLTS.T97357437A3078734.en
IUCN Standards and Petitions Committe (2019) Guideline for Using the IUCN Red List Categories and Criteria. Version 14. Prepared by the Standards and Petitions Committee. http://www.iucnredlist.org/documents/RedListGuidelines.pdf
Le M (2007) Conservation of turtles in Vietnam: a survey of Cat Tien National Park. Oryx 41:544–547
Le DD, Broad S (1995) Investigations into tortoise and freshwater turtle trade in Vietnam. IUCN, Gland
Le M, Hoang T, Le D (2004) Trade data and some comments on the distribution of Mauremys annamensis (Siebenrock, 1903). Asiat Herpetol Res 10:110–113
Luiselli L (2003) Comparative abundance and population structure of sympatric Afrotropical tortoises in sex rainforest areas: the differential effects of “traditional veneration” and of “subsistence hunting” by local people. Acta Oecol 24:157–163
Ly T, Hoang HD, Stuart BL (2011) Market turtle mystery solved in Vietnam. Biol Conserv 144:1767–1771
MARD (2016) QĐ 3158/QĐ-BNN-TCLN: inform the status of Vietnam’s forest type updated to 2015 (in Vietnamese)
McCormack TEM, Dawson JE, Hendrie DB, Ewert MA, Iverson JB, Hatcher RE, Goode JM (2014) Mauremys annamensis (Siebenrock 1903)—Vietnamese Pond Turtle, Annam Pond Turtle, Rùa Trung Bộ. Conservation Biology of Freshwater Turtles and Tortoises
Mittermeier RA, van Dijk PP, Rhodin AG, Nash S (2015) Turtle hotspots: an analysis of the occurrence of tortoises and freshwater turtles in biodiversity hotspots, high-biodiversity wilderness areas, and turtle priority areas. Chelonian Conserv Biol 14:2–10
Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Nguyen VS, Ho TC (1996) A checklist of amphibians and reptiles of Vietnam. Science Technology Publishing House, Hanoi
Nguyen VS, Ho TC, Nguyen Q (2009) Herpetofauna of Vietnam. Edition Chimaira, Frankfurt am Main
Pham Van T (2018) Distribution, threats and ecology of Black Breasted 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 Tropical Forestry). Vietnam National University of Forestry, p 80
Pham Van T, Blanck T, Thao AT, Tran VD (2017) A Computer modeling and interview survey combination to find the existence of the turtle from “nowhere”—Zhou’s box turtle (Cuora zhoui Zhao, Zhou & Ye, 1990)
Pham Van T, Vu TT, Dowson JE, Bui TT, Leprince B (2018) Natural history observations on the Endangered turtle Geoemyda spengleri in Tay Yen Tu Nature Reserve (Vietnam), with notes on other sympatric species. Herpetol Bull 146:1–7
Pham Van T, Leprince B, Luong Xuan H, Nguy Thu Q, Le Duc O, Bordes C, Vuong Tien M, Luiselli L (2019a) Observations of threatened Asian box turtles (Cuora spp.) on trade in Vietnam. Herpetol J 29:178–183. https://doi.org/10.33256/hj29.3.178183
Pham Van T, Luu VQ, Tien TV, Leprince B, Khanh LTT, Luiselli L (2019b) Longitudinal monitoring of turtle trade through Facebook in Vietnam. Herpetol J 29:48–56
Pham Van et al. (under review) Characteristics of relatively undisturbed snake communities in hilly forests in northern Vietnam
Regulation no.17/2015/QĐ-TTg (2015) Vietnam national regulation: Issuing the regulation on management of protection forests
Rhodin AG, Stanford CB, Van Dijk PP, Eisemberg C, Luiselli L, Mittermeier RA, Hudson R, Horne BD, Goode EV, Kuchling G (2018) Global conservation status of turtles and tortoises (Order Testudines). Chelonian Conserv Biol 17:135–161
Stanford CB, Rhodin AGJ, van Dijk PP, Horne BD, Blanck T, Goode E, Hudson R, Mittermeier RA, Currylow A, Eisemberg C, Frankel M, Georges A, Gibbons PM, Juvik JO, Kuchling G, Luiselli L, Haitao S, Singh S, WaldeA (2018) Turtle in trouble—the world’s 25 + most endangered tortoise and freshwater turtle. Turtle Conservation Coalition
Sterling EJ, Hurley MM (2005) Conserving biodiversity in Vietnam: applying biogeography to conservation research. Proc Calif Acad Sci 56:98
Stuart BL, van Dijk PP, Hendrie DB (2001) Photographic guide to the turtle of Thailand, Laos, Vietnam and Cambodia. IUCN, Gland
Tam Thanh People Committee (2019) Report on social economic-security and defense for first six months 2019 of Tam Thanh commune, Quan Son district, Thanh Hoa Province
Thanh Hoa FPD (2019) Tam Thanh commune forest types. Exported from Thanh Hoa provincial Forest Protection Department (FPD) database, forest inventory 2018
Tran KL, Pham Van T, McCormack TEM, Hoang VH, Le M, Ngo MH (2016) Illegal turtle trade in Bac Kan, Quang Ninh, Tuyen Quang Provinces and online illegal turtle trade. VNU J Sci: Earth Environ Sci 32:291–299
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.). In: Rhodin AGJ, Iverson JB, van Dijk PP, Saumure RA, Buhlmann KA, Pritchard PCH, Mittermeier RA (Eds). Conservation biology of freshwater turtles and tortoises: a compilation project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Monographs 7:1–292. https://doi.org/10.3854/crm.7.checklist.atlas.v8.2017
Van Dijk PP, Stuart BL, Rhodin AGJ (2000) Asian turtle trade: proceedings of a workshop on conservation and trade of freshwater turtles and tortoises in Asia. Chelonian Research Monographs, pp. 1–164
WWF (2019) Tropical and subtropical moist broadleaf forests. Southeastern Asia: China, Laos, Myanmar, Thailand, and Vietnam. http://worldwildlife.org/ecoregions/im0137. Accessed 8 Sept 2019
Acknowledgements
The present study was funded by Wildlife Conservation Society’s John Thorbjarnarson Fellowship for Reptile Research and by Turtle Sanctuary and Conservation Center NGO, Paris (France). We would like to thank the Vietnam National University of Forestry, Hanoi, and the Thanh Hoa province authorities for providing the necessary permissions for the interview survey and for the field researches (request permissions code: 221, 243,244 ĐHLN-HTQT and respond permissions code 5550/UBND-THKH, 1660/SNN&PTNT-KL, 195/CCKL-BTTN). Two anonymous referees considerably improved the submitted draft.
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Pham Van, T., Le Duc, O., Leprince, B. et al. Unexpected high forest turtle diversity in hill forests in northern Vietnam. Biodivers Conserv 29, 4019–4033 (2020). https://doi.org/10.1007/s10531-020-02061-y
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DOI: https://doi.org/10.1007/s10531-020-02061-y