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Cyclemys

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Asian leaf turtles
A young Cyclemys dentata from Java, Indonesia.
Scientific classification
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Genus:
Cyclemys

Bell, 1834
Type species
Cyclemys orbiculata
Bell, 1834
Species

7 sp., see text

Distribution of Cyclemys. The exact range of individual species is uncertain.[1]

Cyclemys, commonly referred to as Asian leaf turtles, is a genus of freshwater turtles from the family Geoemydidae. The genus occurs throughout Southeast and South Asia and currently contains seven species.

Asian leaf turtles average at 25 centimetres (9.8 in) in length. They are mostly brown to greenish in color, with round to rectangular shells. Their carapace bears a superficial resemblance to plant leaves, hence their common name. They can be found around shallow, slow-moving bodies of water in hilly forests. Adults are primarily terrestrial, though juveniles are more aquatic.

Asian leaf turtles have not been formally assessed by the IUCN in light of the discovery that the genus contained more species than was previously believed. Nevertheless, they are facing growing threats from illegal wildlife trade and habitat loss.

Taxonomy and nomenclature

Cyclemys turtles belong to the family Geoemydidae under the subfamily Geoemydinae. They were first described in 1834 by the English zoologist, Thomas Bell, in his work A Monograph of the Testudinata.[2][3] Cyclemys and closely related genera (Cuora, Pyxidea, and Notochelys), are believed to have diverged from a common Heosemys-like ancestor.[4][5][6]

The characteristic round carapace of the genus, shown here by an adult Cyclemys dentata.

Cyclemys taxonomy and phylogeny has been historically difficult to ascertain due to the morphological similarity between species, as well as changes in the color patterns during growth.[7] Until recently it was thought that the genus comprised only one or two morphologically variable species,C. dentata and C. oldhamii.[1][8] Subsequent investigation has now put the number of species under the genus to seven, though this remains controversial. The status of C. enigmatica as a valid species is contested, as is the recognition of C. atripons and C. pulchristiata, both of which are nearly impossible to tell apart morphologically.[9][10][1]

Previously recognized species, C. tcheponensis ( = C. tiannanensis) and C. shanensis, have been merged into C. oldhamii following mtDNA sequencing. The conclusions of which showed that the morphological differences between them (the presence of absence of neck/head stripes, and hatchling color patterns) were not enough to classify them as separate species.[1] C. ovata has been similarly subsumed into C. dentata.[11]

There are two distinct morphological differences between Cyclemys species based on the main color of their plastron - species with yellow bellies (C. atripons, C. dentata, and C. pulchristiata), and species with dark bellies (C. enigmatica, C. fusca, C. gemeli, and C. oldhamii).[1]

Synonyms of Cyclemys (ex errore) include: Cyclemus Li, Cyclemis Good, and Cyclemy Mao.[12]

The generic name Cyclemys comes from Greek κύκλος (meaning 'round' or 'circle', referring to the shape of the carapace) and εμύς ('freshwater turtle').[13] They are known under the common name Asian leaf turtles or simply leaf turtles, again because of the appearance of their carapace. They share the collective name 'leaf turtles' with turtles of the genus Geoemyda, as well as turtles with 'leaf' in their names like the Annam leaf turtle (Mauremys annamensis), among others.[13][14] 'Asian leaf turtle' is also the specific common name of C. dentata.

Description

The pattern of scutes on the carapace (upper left) and plastron (upper right) of the shell of Cyclemys. Shown in broken lines are the secondary divisions of the abdominal scutes, a distinguishing characteristic of the genus which only occurs in adults.

Cyclemys turtles are characterized by a more or less round carapace which is typically dark green, brownish, tan, or olive in color. The shell may have a prominent vertebral keel running from head to tail. Serrated marginal scutes are common in juveniles. In adults, only the posterior marginal scutes are serrated.[15]

Adult Cyclemys also develop a joint in the middle of their plastron (known as a plastral hinge), enabling it to articulate the front and rear halves to some extent. Unlike the closely related Cuora which can completely close its shell because of the hinge,[16] Cyclemys plastral hinges only close the shell partially.[6][17] The plastral hinge may also play a significant role in facilitating egg-laying in adult females.[14]

A distinguishing characteristic of the genus is the secondary division of the abdominal scutes (the middle pair of scutes in the plastron) due to the development of the plastral hinge as the turtle matures. It eventually leads to the formation of small triangular additional scutes between the abdominal and pectoral scutes.[18]

Cyclemys turtles are cryptodires, having the ability to pull their heads straight back and vertically into their shells instead of folding it sideways like pleurodires. The head varies between species from dull to striped with bright red or orange bands of color. The plastron can have a dark or light (tan to yellow) background which can be uniform or patterned with fine lines radiating from the center of each plastral scute.[15]

Feet are partially webbed and well developed for either aquatic or terrestrial mobility. They can grow to about 25 cm (9.8 in) in length.[13]

Cyclemys achieve sexual maturity after 7 to 12 years, earlier for males and later for females.[19][15] Sexual dimorphism is apparently mostly absent, though females are likely to outgrow males.[1][20] Females usually deposit ten to fifteen eggs per clutch.[14]

Lifespan

A C. dentata individual has been recorded living up to 14.7 years in captivity.[21] However, an adult specimen caught in the wild has also been recorded living up to another 14 years, making it likely that the maximum lifespan of Cyclemys species has been underestimated.[22]

Distribution and habitat

The ditribution ranges of individual species of Cyclemys remain unclear but the genus occurs in South Asia and Indochina (Vietnam, Myanmar, Laos, Cambodia, Burma, Thailand, central to southern China, Bangladesh, Nepal, and northeastern India), as well as the Southeast Asian countries of Malaysia, Indonesia, Brunei, and the Philippines.[1]

Adult Cyclemys spend most of their time on land. They can be found near ponds, streams, and other shallow, slow-moving bodies of water in hilly forests.[13][14] Although more common in lower elevations they have been found in higher elevations exceeding 1,000 m (3,300 ft) above sea level.[23]

They are omnivorous,[24] but juveniles tend to be more carnivorous. Because their prey is typically aquatic, the younger turtles are found in water more often than adults.[13]

Species

Listed alphabetically along with common names, identifying adult characteristics, and known geographical distribution.[12] They are divided into two morphologically distinct groups.[1]

The yellow plastron of a juvenile Cyclemys dentata.

Yellow-bellied species

  • Cyclemys atripons Iverson & McCold, 1997Western black-bridged leaf turtle or Striped leaf turtle. Carapace is reddish brown, ovoid to elongated, with or without fine radiating black patterns. Plastron is mostly yellow with or without fine radiating black lines. The head is speckled and the throat yellow. The neck is striped. Hatchlings have wide head and neck stripes and a yellow plastron with large dark spots. The common name of the species refers to the color of the bridge (the area where the plastron and the carapace meet) which is predominantly yellow with black stripes or entirely black.[1][25][14] Found in Cambodia, Southeast Thailand, and Vietnam (Annam).[10]
  • Cyclemys dentata (Gray, 1831)Brown stream terrapin or Asian leaf turtle. Carapace is dark brown, ovoid, with or without fine radiating black patterns. Plastron is mostly yellow with or without fine radiating black lines. The head is speckled with a dark yellow striped throat. The neck is striped. The bridge is yellow, with or without black radiating lines.[1] It is the most common species of Cyclemys in the pet trade. The carapace has a prominent keel. Hatchlings have narrow head and neck stripes and a brownish mottled plastron. Hatchlings also exhibit strongly serrated carapaces.[26] Found in Bangladesh,[27] Brunei, Indonesia (Java, Kalimantan, Sumatra, Borneo, Bali), Malaysia, the Philippines (Palawan, Sulu archipelago, Calamian),[28] Singapore, N. India, and peninsular Thailand.[29]
  • Cyclemys pulchristiata Fritz, Gaulke, and Lehr 1997 - Eastern black-bridged leaf turtle. Carapace is reddish brown, ovoid to elongated, with wide radiating black lines or large black specks. Plastron is mostly yellow and may have short fat lines, specks, or be uniformly colored. The head is speckled with a yellow throat. The neck is striped. Hatchlings have wide head and neck stripes and a yellow plastron. The bridge is predominantly yellow with black stripes or entirely black. It is mostly morphologically indistinguishable from C. atripons, requiring genetic sampling to confidently identify.[1][25] Some authorities consider this species to be a junior synonym to or a subspecies of C. atripons. Found in Cambodia and Vietnam.[1][25]
Cyclemys oldhamii carapace (top) and plastron (bottom). The female specimen (right) is larger than that of the male (left).[30]

Dark-bellied species

  • Cyclemys enigmatica Fritz, Guicking, Auer, Sommer, Wink & Hundsdörfer, 2008 - Enigmatic leaf turtle. Carapace is dark brown and slightly reddish, ovoid, and lacks patterns in adults. Plastron is dark brown to black with or without dense black radiating patterns. The head is tan to a light reddish-brown in color. The throat and neck is uniformly dark. The bridge is dark brown to black. Hatchlings lack head and neck stripes and have brownish mottled plastrons.[1] Geographic range overlaps with C. dentata.[31] Found in Brunei (?), Malaysia, and Indonesia (Java, Kalimantan, Sumatra).[32]
  • Cyclemys fusca Fritz, Guicking, Auer, Sommer, Wink & Hundsdörfer, 2008 - Myanmar brown leaf turtle. Carapace is dark brown, ovoid, and lacks patterns in adults. Plastron is Dark brown to black with or without dense black radiating lines. The head is greenish yellow. The throat and neck is uniformly dark. The bridge is dark brown to black.[1][18] Found in Myanmar (Kachin), perhaps adjacent India and Bangladesh.[33]
  • Cyclemys gemeli Fritz, Guicking, Auer, Sommer, Wink & Hundsdörfer, 2008 - Assam leaf turtle. Carapace lacks patterns in adults. It is elongated and relatively flat, with nearly parallel sides. Plastron is unpatterned and dark brown. The head is brown and the throat and neck uniformly dark. The bridge is also dark brown.[1][18] Found in Bangladesh and India (Arunachal Pradesh, Assam, Meghalaya, Mizoram, West Bengal).[34]
  • Cyclemys oldhamii Gray, 1863Oldham’s leaf turtle, Southeast Asian leaf turtle. Carapace is dark brown, rectangular, and unpatterned in adults. Plastron is dark brown to black with or without dense black radiating lines. The head is speckled with a dark throat. The neck varies from uniformly dark (western populations) to striped (eastern populations). The bridge is dark brown to black. Hatchlings have narrow head and neck stripes and brownish plastrons mottled along the edges with a large dark central region.[1] Found in Cambodia,[25] China (?), Indonesia (Kalimantan, Sumatra, Java), Laos, Myanmar, Malaysia (West Borneo), Thailand, Vietnam, India (Terai), and Nepal.[23][35]


Several species previously classified under CyclemysC. amboinensis, C. flavomarginata, C. mouhotti, and C. trifasciata — are now classified under the genus Cuora. C. annandalii is now classified under Heosemys, C. annamensis under Mauremys, and C. giebelii as Notochelys platynota.[11]

Conservation

Cyclemys are often caught and sold for the pet trade, food, or traditional medicine.[36] In August 25, 1998, Forest Protection authorities of Vietnam confiscated a shipment of about 700 turtles with an estimated 30 individuals of C. oldhamii.[37] In May 2007, more than 3000 individuals of Cyclemys, along with Asian box turtles, were confiscated in hundreds of crates in Yangjiang, China.[38]

The most commonly encountered species of Cyclemys in the pet trade, C. dentata, is now being captive bred. They are usually preferred as they are healthier, more acclimated to handling, and captive breeding minimizes the impact on wild populations.[13][26]

The confusion over their exact taxonomy and distribution led to an incomplete assessment of their conservation status by the International Union for Conservation of Nature and Natural Resources (IUCN).[8] In 1991, with only two species recognized, Cyclemys was given the Action Plan Rating (APR) of 3 - in need of some conservation action.[39] In the last assessment in 2000 by the Asian Turtle Trade Working Group of IUCN, the different species currently recognized under the genus Cyclemys were treated as all belonging to the species C. dentata. This resulted in the current incorrect classification of all of the species of Cyclemys as Lower Risk/Near Threatened.[8] Until now, the true conservation status as well as the actual effects of wildlife trade, deforestation, and habitat loss on individual Cyclemys species have yet to be studied.[23][15]

See also

References

  1. ^ a b c d e f g h i j k l m n o p Fritz, U., Guicking, D., Auer, M., Sommer, R. S., Wink, M. and Hundsdörfer, A. K. (2008), Diversity of the Southeast Asian leaf turtle genus Cyclemys: how many leaves on its tree of life?. Zoologica Scripta, 37: 367–390. doi: 10.1111/j.1463-6409.2008.00332.x
  2. ^ Gray, John Edward (1855). Catalogue of Shield Reptiles in the Collection of the British Museum. Order of the Trustees, British Museum (Natural History).
  3. ^ Fritz, Uwe; Nowak-Kemp, Malgosia (2010). "Chelonian type specimens at the Oxford University Museum" (PDF). Zootaxa. 1 (19). Magnolia Press. Retrieved March 27, 2011.
  4. ^ Honda, Masanao; Yasukawa, Yuichirou; Hirayama, Ren; Ota, Hidetoshi (2002). "Phylogenetic Relationships of the Asian Box Turtles of the Genus Cuora sensu lato (Reptilia: Bataguridae) inferred from Mitochondrial DNA Sequences" (PDF). Zoological Science. 19 (11). Zoological Society of Japan: 1305–1312. doi:10.2108/zsj.19.1305. PMID 12499674. Retrieved March 28, 2011.
  5. ^ Zhang, Yanyun; Nie, Liuwang; Huang, Yuqing; Pu, Youquang; Zhang, Li (2009). "The Mitochondrial DNA Control Region Comparison Studies of Four Hinged Turtles and its Phylogentic Significance of the Genus Cuora Sensu Lato (Testudinata: Geoemydidae)" (PDF). Genes and Genomics. 31 (5). The Genetics Society of Korea: 349–359. doi:10.1007/BF03191253. Retrieved March 29, 2011.
  6. ^ a b Bramble, Dennis M. (1974). "Emydid Shell Kinesis: Biomechanics and Evolution". Copeia. 1974 (3). American Society of Ichthyologists and Herpetologists. JSTOR 1442685. {{cite journal}}: |access-date= requires |url= (help)
  7. ^ Fritz, Uwe; Fritz, UWE (2008). "Historical DNA from museum type specimens clarifies diversity of Asian leaf turtles (Cyclemys)". Biological Journal of the Linnean Society. 94 (1). The Linnean Society of London: 131–141. doi:10.1111/j.1095-8312.2008.00966.x. {{cite journal}}: |access-date= requires |url= (help)
  8. ^ a b c Asian Turtle Trade Working Group 2000. Cyclemys dentata. In: IUCN 2010. IUCN Red List of Threatened Species. Version 2010.4. Retrieved March 25, 2011.
  9. ^ Artner, H. (2008). "The World's Extant Turtle Species" (PDF). Emys. 15 (3). Chelonia 2002 - Turtle Center. Retrieved March 27, 2011. {{cite journal}}: External link in |publisher= (help)
  10. ^ a b Uetz, Peter; Hallermann, Jakob; Hosek, Jiri. "Cyclemys atripons Iverson & McCord, 1997". The Reptile Database. Retrieved March 27, 2011.
  11. ^ a b Fritz, Uwe; Havaš, Peter (2007). "Checklist of Chelonians of the World" (Document). At the request of the CITES Nomenclature Committee and the German Agency for Nature Conservation and funded by the Museum für Tierkunde Dresden and the German Federal Ministry of EnvironmentTemplate:Inconsistent citations {{cite document}}: Unknown parameter |accessdate= ignored (help); Unknown parameter |issn= ignored (help); Unknown parameter |url= ignored (help)CS1 maint: postscript (link)
  12. ^ a b Turtle taxonomy Working Group (Rhodin, A.G.J., van Dijk, P.P, Iverson, J.B., and Shaffer, H.B.).2010. Turtles of the world, 2010 update: annotated checklist of taxonomy, synonymy, distribution, and conservation status. In: Rhodin, A.G.J., Pritchard, P.C.H., van Dijk, P.P., Saumure, R.A., Buhlmann, K.A., Iverson, J.B., and Mittermeier, R.A. (Eds.). Conservation Biology of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Monographs No. 5. pp. 000.85-000.164, doi:10.3854/crm.5.000.checklist.v3.2010
  13. ^ a b c d e f Tabaka, Chris; Senneke, Darrell (January 28, 2003). "Genus: Cyclemys (Asian Leaf Turtles)". World Chelonian Trust. Retrieved March 27, 2011.
  14. ^ a b c d e Franklin, Carl J. (2007). Turtles: An Extraordinary Natural History 245 Million Years in the Making. Voyageur Press. ISBN 978-0-7603-2981-8.
  15. ^ a b c d Melstrom, Keegan (November 17, 2009). Dr. Kenneth Angielczyk (ed.). Cyclemys dentata (Gray, 1831). Encyclopedia of Life. Retrieved March 27, 2011Template:Inconsistent citations{{cite book}}: CS1 maint: postscript (link)
  16. ^ Dodd, C. Kenneth (2002). North American Box Turtles: A Natural History. Animal Natural History. University of Oklahoma Press. p. 14. ISBN 978-0806135014.
  17. ^ "Asian Leaf, Yellow-headed Temple, Striped-necked Leaf, & Borneo Black Leaf Turtle". Free Pet Care Tips Newsletter. Retrieved March 29, 2011.
  18. ^ a b c Praschag, Peter; Hundsdörfer, Anna K.; Fritz, Uwe (2009). "Further specimens and phylogenetic position of the recently described leaf turtle species Cyclemys gemeli (Testudines: Geoemydidae)" (PDF). Zootaxa. 29 (37). Magnolia Press. ISSN 1175-5334. Retrieved March 29, 2011.
  19. ^ Paul Coleman (1995). "The Asian Leaf Turtle (Cyclemys dentata)". UKchelonia.info. Retrieved March 29, 2011.
  20. ^ Karen A., Jensen; Indraneil, Das (2006). "Biological Observations on the Asian Soft-Shell Turtle in Sarawak, Malaysian Borneo, with notes on the Biology and Conservation of other Non-marine Turtles". Testudo. 6 (3). British Chelonia Group. Retrieved March 30, 2011.
  21. ^ "AnAge entry for Cyclemys dentata". AnAge database at the Human Ageing Genomic Resources. Retrieved March 28, 2011.
  22. ^ Joao Pedro de Magalhaes (2010). "Cyclemys dentata Gray 1831, Lifespan, longevity, and ageing". Encyclopedia of Life. Retrieved March 28, 2011.
  23. ^ a b c Rui, Kalu Ram (2004). "Ecological Distribution Of Cyclemys Oldhamii(Gray 1863) From Nepal". Our Nature. 2 (7). Nature Conservation and Health Care Council, Nepal.
  24. ^ David T. Kirkpatrick (1996). "An Overview of Common Semi-Aquatic Turtles". University of North Carolina. Retrieved March 28, 2011. {{cite web}}: External link in |publisher= (help)
  25. ^ a b c d Durkin, Louise; Handschuh, Markus; Sovannak, Keo; Ward, Lizzy; Hulse, Nikki; Mould, Alistair (2010). "Discovery of a hitherto unknown breeding population of the Asian leaf turtle Cyclemys aff. atripons in Phnom Kulen National Park, northwestern Cambodia" (PDF). Cambodian Journal of Natural History (1). Centre for Biodiversity Conservation, Phnom Penh.
  26. ^ a b Hopson, Mary. "Asian Leaf Turtles". The Turtle Puddle. Retrieved March 27, 2011. {{cite journal}}: Cite journal requires |journal= (help); External link in |publisher= (help)
  27. ^ Ali Reza, A.H.M. (2004). "Natural Resources Management in Bangladesh: Linking National Priority to Global Perspective" (PDF). Tigerpaper. 31 (2). Retrieved March 27, 2011.
  28. ^ Diesmos, Arvin C.; Rogelio V., Sison; Alcala, Angel C.; Sison, Rogelio V. (2008). "Status and Distribution of Nonmarine Turtles of the Philippines". Chelonian Conservation and Biology. 7 (2). Chelonian Research Foundation: 157–177. doi:10.2744/CCB-0672.1.
  29. ^ Uetz, Peter; Hallermann, Jakob; Hosek, Jiri. "Cyclemys dentata (Gray, 1831)". The Reptile Database. Retrieved March 27, 2011.
  30. ^ Annandale, N. (1918). "Chelona and Batrachia of the Inle Lake" (PDF). Zoological Survey of India. Retrieved March 29, 2011. {{cite journal}}: Cite journal requires |journal= (help)
  31. ^ Hoogmoed, M.S.; Gassó Miracle, M.E.; van den Hoek Ostende, L.W. (2002). "Type specimens of recent and fossil Testudines and Crocodylia in the collections of the Netherlands Centre for Biodiversity Naturalis, Leiden, the Netherlands". Zool. Med. Leiden. 84 (8). Netherlands Centre for Biodiversity Naturalis. ISSN 0024-0672. Retrieved March 28, 2011.
  32. ^ Uetz, Peter; Hallermann, Jakob; Hosek, Jiri. "Cyclemys enigmatica Fritz, Guicking, Auer, Sommer, Wink & Hundsdörfer, 2009". The Reptile Database. Retrieved March 27, 2011.
  33. ^ Uetz, Peter; Hallermann, Jakob; Hosek, Jiri. "Cyclemys fusca Fritz, Guicking, Auer, Sommer, Wink & Hundsdörfer, 2009". The Reptile Database. Retrieved March 27, 2011.
  34. ^ Uetz, Peter; Hallermann, Jakob; Hosek, Jiri. "Cyclemys gemeli Fritz, Guicking, Auer, Sommer, Wink & Hundsdörfer, 2009". The Reptile Database. Retrieved March 27, 2011.
  35. ^ Uetz, Peter; Hallermann, Jakob; Hosek, Jiri. "Cyclemys oldhami Gray, 1863". The Reptile Database. Retrieved March 27, 2011.
  36. ^ "Leaf Turtle". Nam Kading Research & Training Centre. Retrieved March 27, 2011.
  37. ^ Hendrie, Douglas (November 1, 1998). "Protecting Vietnam's Turtles" (Document). Cuc Phuong Conservation ProjectTemplate:Inconsistent citations {{cite document}}: Unknown parameter |accessdate= ignored (help); Unknown parameter |url= ignored (help)CS1 maint: postscript (link)
  38. ^ United Nations Environment Programme (2007). Beijing 2008 Olympic games: an environmental review. UNEP Division of Communications and Public Information. ISBN 978-92-807-2888-0.
  39. ^ IUCN/SSC Tortoise and Freshwater Turtle Specialist Group (1989). Tortoises and freshwater turtles: an action plan for their conservation. IUCN/WWF. ISBN 2-88032-974-4.