Herpetology Notes, volume 7: 737-744 (2014) (published online on 21 December 2014)
New records of turtles from Binh Dinh Province, Vietnam
Loi Duc Duong1, Chung Dac Ngo1 and Truong Quang Nguyen2,*
Abstract. Nine species of turtles are recorded for the first time from Binh Dinh Province, namely Platysternon megacephalum, Cuora amboiensis, C. picturata, C. trifasciata, Heosemys grandis, Malayemys subtrijuga, Mauremys sinensis, Sacalia quadriocellata, and Manouria impressa. Our findings bring the total number of turtle species to 17 in Binh Dinh Province.
Key words: Distribution, morphology, new records, taxonomy, Binh Dinh.
Introduction Based on the results of our recent field work between 2012 and 2014, we herein document the occurrence of In the most recent checklist of reptiles and amphibians nine additional species of freshwater turtles in Binh of Vietnam, Nguyen, Ho and Nguyen (2009) reported Dinh Province. three species of turtles from Binh Dinh Province, namely Mauremys annamensis (Siebenrock), Materials and Methods Eretmochelys imbricata (Linnaeus), and Lepidochelys olivacea (Eschscholtz). Hendrie et al. (2011) recorded Seven field surveys, seven to ten days each, were seven species of freshwater turtles from this province, conducted in July, September and November 2012; viz. Cuora bourreti Obst and Reimann, Cuora mouhotii February, March and May 2013; and January 2014 in (Gray), Cyclemys pulchristriata Fritz, Gaulke and 11 districts of Binh Dinh Province: An Lao, An Nhon, Lehr, Cyclemys tcheponensis (Bourret), Indotestudo Hoai An, Hoai Nhon, Phu Cat, Phu My, Quy Nhon, Tay elongata (Blyth), Pelodiscus sinensis (Wiegmann), and Son, Tuy Phuoc, Van Canh, and Vinh Thanh (Fig. 1). Pelochelys cantorii Gray. However, the presence of P. Species records were based on the direct observation or cantorii in Binh Dinh Province needs to be confirmed by remains (e.g., carapaces and skulls) of turtle specimens further studies because we have not found any evidence in villager’s houses. of the presence of this species during our field trips. Morphological characters: Photographs and In addition, Guicking et al. (2002) regarded Cyclemys morphological measurements were taken with a tape tcheponensis as a subspecies of C. shanensis Annandale in the wild and individuals were released immediately but Stuart and Fritz (2008) subsequently considered at the site of capture. Morphometric variables are both C. shanensis and C. tcheponensis as synonyms of abbreviated as follows: SCL: carapace length (minimum C. oldhamii. At present, a total of nine species of turtles straight line carapace length), CW: maximum carapace have been recorgnized from Binh Dinh Province. width, CH: maximum carapace height, PL: plastron length (from anterior-most end to posterior-most end of the plastron), TaL: tail length (from posterior margin of cloaca to the tip of tail). Species identification follows Ernst and Babour (1989), Lehr et al. (1998), Stuart and
1 College of Education, Hue University, 34 Le Loi Road, Fritz (2008), Stuart et al. (2001), Hendrie et al. (2011), Hue City, Vietnam; E-mails: [email protected], and Ly et al. (2011). [email protected] 2 Institute of Ecology and Biological Resources, Vietnam Results Academy of Science and Technology, 18 Hoang Quoc Viet, Hanoi, Vietnam; E-mail: [email protected] Results of our field surveys confirmed the occurrence * Corresponding author of the six species of freshwater turtles which were 738 Loi Duc Duong et al.
was found on 27 March 2013 by L. D. Duong in the forest of An Lao mountain, An Hung Commune, An Lao District (14o39.033’N, 108o54.588’E, elevation 57 m above sea level (a.s.l.)). Another individual, sex unknown, was seen in a trader’s house on 7 March 2013 in Vinh Kim Commune of Vinh Thanh District. Morphological characters. Weight 163 g; head very large; carapace flat (SCL: 96 mm, CW: 72.7 mm, CH: 39 mm); plastron notched posteriorly (PL: 75 mm); tail very long (TaL: 99 mm), covered with large scales; toes webbed. Coloration in presevative: head and carapace yellowish brown; neck grayish brown dorsally, yellow ventrally; plastron light brown; forelimbs light brown, covered with large scales; hind limbs brown with a row of large scales along the inner and outer borders and on the heel. Distribution. In Vietnam, Platysternon megacephalum has been recorded from Lai Chau and Lao Cai provinces in the North southwards to Kon Tum and Gia Lai provinces (Nguyen, Ho and Nguyen, 2009). Elsewhere,
Figure 1. Map showing the survey site (black square) in Binh Dinh Province, Vietnam.
previously reported in Binh Dinh Province: Cuora bourreti, Cuora mouhotii, Mauremys annamensis, Cyclemys pulchristriata, Indotestudo elongata, and Pelodiscus sinensis. Two species of sea turtles, Eretmochelys imbricata and Lepidochelys olivacea were reported from Binh Dinh Province based on interviews with local people. In addition, we recorded nine species of freshwater turtles for the first time from Binh Dinh Province.
Taxonomic accounts Family Platysternidae Platysternon megacephalum Gray, 1831 Big-headed Turtle / Rua dau to (Fig. 2) Figure 2. A juvenile of Platysternon megacephalum from An Hung Commune, An Lao District, Binh Dinh Province: A) Specimen examined. A dead juvenile (CLBH.13118) dorsal view and B) ventral view. New records of turtles from Binh Dinh Province, Vietnam 739
stripe, bordered in yellow, present on each side, from tip of snout, above the nostril and the orbit to the neck; two other yellow stripes present on each side of the head; carapace dark olive; plastron light brown with black spot toward the outside of each scute; marginals yellowish brown, each with black spot along outer border. Distribution. In Vietnam, C. amboinensis has been recorded from some central and southern provinces: Dak Lak, Dong Nai, Tay Ninh, Long An, Kien Giang, and Ca Mau (Nguyen, Ho and Nguyen, 2009). Elsewhere, this species is known from India, Bangladesh, Myanmar, Laos, Thailand, Cambodia, Malaysia, Singapore, Indonesia, Timor Leste, Brunei, and the Philippines (Nguyen, Ho and Nguyen, 2009; Uetz and Hošek, 2014).
Figure 3. An adult female of Cuora amboiensis from Nhon Khanh Commune, An Nhon District, Binh Dinh Province: A) dorsolateral view and B) ventral view.
this species is known from China, Myanmar, Laos, Thailand, and Cambodia (Nguyen, Ho and Nguyen, 2009; Uetz and Hošek, 2014).
Family Geoemydidae Cuora amboinensis (Daudin, 1802) Malayan Box Turtle / Rua hop lung den (Fig. 3). Specimen examined. One adult female was captured on 28 March 2013 by L. D. Duong near a lake in Nhon Khanh Commune, An Nhon Township (13o37.120’N, 108o59.587’E, elevation 15 m a.s.l.). Morphological characters. Weight 850 g; carapace high-arched (SCL: 181 mm, CW: 127.5 mm, CH: 83.5 mm), vertebral keel present, posterior notch absent; marginals not serrated; plastron large (PL: 175.2 mm), Figure 4. An adult male of Cuora picturata from Canh completely covered carapacial openings, without medial Lien Commune, Van Canh District, Binh Dinh Province: A) anal notch. Coloration in life: head dark olive; a black dorsolateral view and B) ventral view. 740 Loi Duc Duong et al.
Cuora picturata Lehr, Fritz & Obst, 1998 Vietnamese Box Turtle/ Rua hop tran vang mien nam (Fig. 4). Specimens examined. One adult male was captured on 27 May 2013 by L. D. Duong in forest of Canh Lien Commune, Van Canh District (13o37.120’N, 108o59.587’E, elevation 60 m a.s.l.). Three other individuals were observed in Canh Thuan Commune, Van Canh District in the house of a local trader. Morphological characters. Weight 820 g; carapace high-domed (SCL: 152 mm, CW: 120 mm, CH: 93 mm), vertebral keel indistinct; marginals not serrated; plastron large (PL: 152 mm), posteriorly round, Figure 5. A subadult of Cuora trifasciata from Vinh Son completely covered capapacial openings. Coloration in Commune, Vinh Thanh District, Binh Dinh Province: A) life: head yellowish brown with dark speckles; carapace dorsal view and B) ventral view. bright brown; a vertebral light stripe present, edged in black; a dark stripe present along upper part of pleurals; lower part of pleurals whitish yellow or light brown, sometimes with small dark spots; marginals yellowish brown with black spots; plastron light yellow with a large black blotch on each scute. Distribution. In Vietnam, C. picturata has been known from Khanh Hoa and Phu Yen provinces (Nguyen, Ho and Nguyen, 2009; Hendrie et al., 2011). Elsewhere, this species is known from Cambodia (Nguyen, Ho and Nguyen, 2009; Uetz and Hošek, 2014).
Cuora trifasciata (Bell, 1825) Three-striped Box Turtle/ Rua hop ba vach (Fig. 5) Specimens examined. One subadult individual was photographed on 6 May 2013 by L. D. Duong in the house of a wildlife trader in Vinh Thanh Township, Vinh Thanh District (14o05.867’N, 108047.183’E, elevation 42 m asl.). The trader reported that this animal was collected on 15 April 2013 from K2 Village, Vinh Son Commune, Vinh Thanh District. We were not allowed to take measurements of this individual, the following morphological description is based on the photograph. Coloration in life: carapace yellowish brown with a long black vertebral stripe and two shorter lateral stripes, extending along the first three pleurals; head light brown above, darker laterally, with a dark stripe from nostril to orbit; neck and limb sockets orange; platron notched posteriorly, black with orange pattern in anterior part and lateral border. Distribution. In Vietnam, C. trifasciata has been recorded from Cao Bang and Lang Son provinces southwards to Quang Nam, Kon Tum, and Gia Lai Figure 6. An adult female of Heosemys grandis from Canh provinces (Nguyen, Ho and Nguyen, 2009). Elsewhere, Lien Commune, Van Canh District, Binh Dinh Province: A) dorsal view and B) ventral view. New records of turtles from Binh Dinh Province, Vietnam 741 this species is known from China and Laos (Nguyen, Ho and Nguyen, 2009; Uetz and Hošek, 2014).
Heosemys grandis (Gray, 1860) Giant Asian Pond Turtle/ Rua dat lon (Fig. 6) Specimen examined. One adult female was captured on 17 March 2013 by L. D. Duong in Canh Lien Commune, Van Canh District (13o37.200’N, 108o59.587’E, elevation 65 m a.s.l.). Morphological characters. Weight 4100 g; carapace highly arched, depressed dorsally, serrated posteriorly (SCL: 300 mm, CW: 193.2 mm, CH: 125.3 mm); vertebral keel well-defined, blunt; plastron large, notched posteriorly (PL: 280 mm); upper jaw with a shallow medial notch; toes webbed. Coloration in life: head gray with numerous orange spots; carapace grayish brown, medial keel yellow; plastron yellow, each scute with dark lines radiating outward from a large dark central blotch. Distribution. In Vietnam, Heosemys grandis has been recorded from Quang Binh southwards to Dong Nai and Kien Giang province (Nguyen, Ho and Nguyen, 2009). Elsewhere, this species is known from Myanmar, Laos, Thailand, Cambodia, and Malaysia (Nguyen, Ho and Nguyen, 2009; Uetz and Hošek, 2014).
Malayemys subtrijuga (Schweigger, 1812) Figure 7. An adult male of Malayemys subtrijuga from Phu Malayan Snail-eating Turtle/ Rua ba go (Fig. 7) An Commune, Tay Son District, Binh Dinh Province: A) Specimen examined. One adult male was captured dorsolateral view and B) ventral view. on 10 February 2013 by L. D. Duong in a stream in Tay Son forest, Phu An Commune, Tay Son District (13o51.850’N, 108o56.083’E, elevation 52 m a.s.l.). Morphological characters. Weight 162.8 g; carapace moderately arched (SCL: 99.5 mm, CW: 76 mm, CH: Mauremys sinensis (Gray, 1834) 44.5 mm), with three discontinuous keels consisting Chinese Striped-necked Turtle / Rua co soc (Fig. 8). of knobs situated at the posterior border of the scutes; marginals serrated but notched posteriorly; plastron Specimen examined. One adult male was captured notched posteriorly (PL: 80.1 mm). Coloration in life: on 5 May 2013 by L. D. Duong in a marsh area near head black with some yellow stripes: the first from Bong Son Township, Hoai Nhon District (14o25.533’N, snout running above the nostrils and orbits to the neck 109o00.833E, elevation 7 m a.s.l.). and the second from each side of snout backwards to the Morphological characters. Weight 610 g; carapace neck; carapace light brown with black spot in posterior slightly depressed (SCL: 192 mm, CW: 123 mm, CH: of each scute; plastron cream with black blotch on each 74 mm), with a discontinuous vertebral keel, more scute; outer edge of marginals yellow; limbs dark gray. distinct anteriorly; marginals not serrated; plastron Distribution. In Vietnam, Malayemys subtrijuga has notched posteriorly (PL: 156 mm); upper jaw notched been recorded from Quang Binh southwards to Dong medially; toes webbed. Coloration in life: head and Nai, Kien Giang and Ca Mau provinces (Nguyen, Ho neck olive dorsally and yellow ventrally, containing and Nguyen 2009). Elsewhere, this species is known numerous greenish yellow stripes; carapace dark brown from Laos, Thailand, and Cambodia (Nguyen, Ho and with yellow seams; plastron yellow with large dark Nguyen, 2009; Uetz and Hošek, 2014). blotch on each scute; limbs dark brown. 742 Loi Duc Duong et al.
and two females were kept in the house of a local trader in Vinh Son Commune. They were collected by local people in January 2014 in the forest near Village K8, Vinh Son Commune, Vinh Thanh Dictrist. Morphological characters. Weight 215 g; carapace elongate, slightly depressed (SCL: 128.5 mm, CW: 86.5 mm, CH: 40.1 mm), with a low vertebral keel; marginals not serrated; plastron notched posteriorly (PL: 106.5 mm); upper jaw not notched; toes webbed. Coloration in life: head yellowish brown with four bright dark-centered ocelli; neck dark brown dorsally and red ventrally; three longitudinal orange stripes extending from the head backward to the neck; carapace yellowish brown with dark vermiculations; plastron yellowish cream with dark vermiculations; limbs dark brown. Distribution. In Vietnam, Sacalia quadriocellata has been recorded from Lao Cai and Ha Giang provinces in the North southward to Thua Thien - Hue and Quang
Figure 8. An adult male of Mauremys sinensis from Bong Son Township, Hoai Nhon District Binh Dinh Province: A) dorsolateral view and B) ventral view.
Distribution. In Vietnam, Mauremys sinensis has been recorded from Son La and Phu Tho provinces in the North to Quang Nam Province in the South (Nguyen, Ho and Nguyen, 2009). Elsewhere, this species is known from southern China and Taiwan (Nguyen, Ho and Nguyen, 2009; Uetz and Hošek, 2014).
Sacalia quadriocellata (Sibenrock, 1903) Four-eyed Turtle/ Rua bon mat (Fig. 9). Specimens examined. One adult female was captured on 17 November 2013 by L. D. Duong in a stream of Figure 9. An adult female of Sacalia quadriocellata from o Canh Lien Commune, Van Canh District (13 36.503’N, Canh Lien Commune, Van Canh District, Binh Dinh Province: 108o51.070’E, elevation 548 m a.s.l.). Another male A) dorsal view and B) ventral view. New records of turtles from Binh Dinh Province, Vietnam 743
Nam provinces (Nguyen, Ho and Nguyen, 2009). Elsewhere, this species is known from China and Laos (Nguyen, Ho and Nguyen, 2009; Uetz and Hošek, 2014).
Family Testudinidae Manouria impressa (Günther, 1882) Impressed Tortoise/ Rua nui vien (Fig. 10). Specimen examined. One adult female was captured on 15 May 2013 by L. D. Duong in the forest of Canh Lien Commune, Van Canh District (13o37.200’N, 108o59.978’E, elevation 60 m a.s.l.). Morphological characters. Weight 1550 g; carapace oval, flattened dorsally, strongly serrated (SCL: 250 mm, CW: 139.5 mm, CH: 130 mm), posterior marginals upturned, pleurals concave, well-defined growth annuli present on the vertebrals and marginals; plastron large with a deep cloacal notch (PL: 220 mm); head large, upper jaw without hook. Coloration in life: head yellow with some pink pigment; neck yellow; carapace yellowish brown with dark radiations along the outer border of each scute; marginals with large dark blotches; plastron yellowish brown with dark seams and streaks; forelimbs black, hind limbs and tail dark brown. Figure 10. An adult male of Manouria impressa from Canh Distribution. In Vietnam, Manouria impressa has Lien Commune, Van Canh District, Binh Dinh Province: A) been recorded from Lai Chau, Lao Cai, and Yen Bai dorsal view and B) ventral view. provinces in the North to Kon Tum, Lam Dong, and Dong Nai provinces in the South (Nguyen, Ho and Nguyen, 2009). Elsewhere, this species is known from Southern China, Myanmar, Laos, Thailand, Cambodia, and Malaysia (Nguyen, Ho and Nguyen, 2009; Uetz and Hošek, 2014). traders in Van Canh, Tay Son, Vinh Thanh, An Lao and Bong Son communes: Platysternon megacephalum, Discussion Cuora bourreti, C. mouhotii, C. picturata, C. trifasciata, Cyclemys pulchristriata, Heosemys grandis, Mauremys Our findings bring the species number of turtles to annamensis, M. sinensis, Sacalia quadriocellata, 17 in Binh Dinh Province, comprising 15 species of Indotestudo elongata, and Manouria impressa. In freshwater turtles and two species of marine turtles (see addition, turtle species in Binh Dinh Province are also at Appendix). Among them, Mauremys annamensis and risk from habitat loss and degradation, particularly the Cuora picturata are endemic to Vietnam. It is noted conversion of forest land into plantation of eucalyptus that all recorded turtles from Binh Dinh Province are for paper industry. Therefore, habitat protection and threatened species: 12 of them listed in the Vietnam Red improvement of law enforcement to control wildlife Data Book (Tran et al., 2007), comprising two critically trade are conservation priorities for the turtle fauna in endangered, six engdangered and four vulnerabale Binh Dinh Province. species and 16 species listed in the IUCN Red List (2014), consisting of five critically endangered, four Acknowledgements. We thank the directorate of the Forest engdangered, six vulnerabale, and one near threatened Protection Department of Binh Dinh Province and the Department species (see Appendix). A major threat to the turtle fauna of Agriculture and Rural Development of Van Canh District for of Binh Dinh Province is illegal wildlife trade. The support of our field work and issuing relevant permits. Many following species were observed in the houses of wildlife thanks to E. Sterling (New York) and K. Koy (Berkeley) for 744 Loi Duc Duong et al. providing the map, T. Ziegler (Cologne) and Tim McCormack Ly, T., Hoang, H.D., Stuart, B.L. (2011): Market turtle mystery (Hanoi) for valuable comments on our manuscript. solved in Vietnam. Biological Conservation 144: 1767-1771. Nguyen, S.V., Ho, C.T., Nguyen, T.Q. (2009): Herpetofauna References of Vietnam. Edition Chimaira, Frankfurt am Main. Stuart, L.B., Fritz, U. (2008): Historical DNA from type museum Ernst, C.H., Barbour, R.W. (1989): Turtles of the World. specimens clarifies diversity of Asian leaf turtles (Cyclemys). Smithsonian Institution Press. Washington, D. C., and London. Biological Journal of the Linnean Society 94: 131-141. Hendrie, D.B., Bui D.P., McCormack, T., Hoang, V.H., Van Stuart, L.B., Van Dijk, P.P., Hendrie, D.B (2001): Photographic Dijk, P.P. (2011). Handbook identification law enforcement guide to the the turtles of Thailand, Laos, Vietnam and freshwater turtles in Vietnam. Giao Thong Van Tai Publishing Cambodia. Design Group, Phnompenh, Cambodia. House, Hanoi (in Vietnamese). Tran, K., Ho, C.T., Nguyen, S.V., Pham, T. (2007): Reptiles Guicking, D., Fritz, U., Wink, M., Lehr, E. (2002): New data on the and Amphibians. In: Dang, N. T., Tran, K., Dang, H.H., diversity of the Southeast Asian leaf turtle genus Cyclemys (Bell, Nguyen, C., Nguyen, T.N., Nguyen, Y.H., Dang, D.T. (eds.). 1834), molecular results. (Reptilia: Testudines: Geoemydidae). Vietnam Red Data Book, Part1 Animals, p. 219-276 + 8 Pls. Faunistische Abhandlungen, 23: 75-86. Natural Science and Technology Publishing House (in IUCN (2014): The IUCN Red List of Threatened Species. Available Vietnamese). at:
1 Appendix. Updated list of turtle species recorded for Binh Dinh Province. The list include Appendix. Updated2 listconfirmed of turtle literature species records recorded (Nguyen, for Binh Ho and Dinh Nguyen Province. 2009; Hendrie The list et al.,include 2011) confirmedand results of literature records (Nguyen, Ho and Nguyen 3 2009;this Hendrie work (marked et al., with 2011) *). Conservation and results status: of CR: this Critically work (marked Endangered, with EN: *). Endangered, Conservation status: CR: Critically Endangered, EN: 4Endangered,VU: Vulnerabale, VU: Vulnerabale, NT: Lower Risk/Near NT: Lower Threatened. Risk/Near Threatened. 5 6 Vietnam Red Data Book IUCN Red List Species (2007) (2014) Platysternidae Platysternon megacephalum Gray, 1831 * EN Geoemydidae Cuora amboinensis (Daudin, 1802)* VU VU Cuora bourreti Obst & Reimann, 1994 EN CR Cuora mouhotii (Gray, 1862) EN Cuora picturata Lehr, Fritz & Obst, 1998* EN CR Cuora trifasciata (Bell, 1825)* CR CR Cyclemys pulchristriata Fritz, Gaulke & Lehr, 1997 NT Heosemys grandis (Gray, 1860)* VU VU Malayemys subtrijuga (Schweigger, 1812)* VU VU Mauremys annamensis (Siebenrock, 1903) CR CR Mauremys sinensis (Gray, 1834)* EN Sacalia quadriocellata (Siebenrock, 1903) * EN Testudinidae Indotestudo elongata (Blyth, 1853) EN EN Manouria impressa (Günther, 1882)* VU VU Trionychidae Pelodiscus sinensis (Wiegmann, 1834) VU Cheloniidae Eretmochelys imbricata (Linnaeus, 1766) EN CR Lepidochelys olivacea (Eschscholtz, 1829) EN VU 7
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