Organisms Diversity & Evolution

, Volume 10, Issue 3, pp 227–242 | Cite as

The world’s economically most important chelonians represent a diverse species complex (Testudines: Trionychidae: Pelodiscus)

  • Uwe FritzEmail author
  • Shiping Gong
  • Markus Auer
  • Gerald Kuchling
  • Norbert Schneeweiß
  • Anna K. Hundsdörfer
Original Article


Pelodiscus is one of the most widely distributed genera of softshell turtles, ranging from south-eastern Siberia and Korea over central and southern China to Vietnam. Economically, Pelodiscus are the most important chelonians of the world and have been bred and traded in high numbers for centuries, resulting in many populations established outside their native range. Currently, more than 300 million turtles per year are sold in China alone, and the bulk of this figure comprises farmed Pelodiscus. Due to easy availability, Pelodiscus also constitutes a model organism for physiological and embryological investigations. Yet, diversity and taxonomy of Pelodiscus are poorly understood and a comprehensive investigation using molecular tools has never been published. Traditionally, all populations were assigned to the species P. sinensis (Wiegmann, 1834); in recent years up to three additional species have been recognized by a few authors, while others have continued to accept only P. sinensis. In the present study, we use trade specimens and known-locality samples from Siberia, China, and Vietnam, analyze 2,419 bp of mtDNA and a 565-bp-long fragment of the nuclear C-mos gene to elucidate genetic diversity, and compare our data with sequences available from GenBank. Our findings provide evidence for the existence of at least seven distinct genetic lineages and suggest interbreeding in commercial turtle farms. GenBank sequences assigned to P. axenaria (Zhou, Zhang & Fang, 1991) are highly distinct. The validity of P. maackii (Brandt, 1857) from the northernmost part of the genus’ range is confirmed, whereas it is unclear which names should be applied to several taxa occurring in the central and southern parts of the range. The diversity of Pelodiscus calls for caution when such turtles are used as model organisms, because the respective involvement of more than a single taxon could lead to irreproducible and contradictory results. Moreover, our findings reveal the need for a new assessment of the conservation status of Pelodiscus. While currently all taxa are subsumed under ‘P. sinensis’ and listed as ‘vulnerable’ by the IUCN Red List of Threatened Species, some could actually be endangered or even critically endangered.


Asia Conservation Diversity Phylogeography Phylogeny 



Lab work was done by Anke Müller. Markus Auer’s work in China benefited from a grant of the EAZA Shellshock Campaign. Bing He, Zunliang Li, Guofang Zhong, and Jianping Zou helped to collect samples in Guangdong. Christian Schmidt (Dresden) translated Chinese papers for us. Thomas Ziegler (Köln) provided photos of Vietnamese Pelodiscus.


  1. Castelloe, J., & Templeton, A. R. (1994). Root probabilities for intraspecific gene trees under neutral coalescent theory. Molecular Phylogenetics and Evolution, 3, 102–113.CrossRefPubMedGoogle Scholar
  2. Chen, H.-G., Liu, W.-B., & Zhang, X.-J. (2005). Comparative analysis of mitochondrial DNA 12S rRNA region between Pelodiscus sinensis and Pelodiscus axenaria and their molecular marker for identification. Journal of Fisheries of China, 29, 318–322 [in Chinese, with English abstract].Google Scholar
  3. Chen, H.-G., Liu, W.-B., Li, J.-Z., & Zhang, X.-J. (2006). Comparative analysis of mitochondrial DNA cytb gene and their molecular identification markers in three species of soft-turtles. Acta Hydrobiologica Sinica, 30, 380–385 [in Chinese, with English abstract].Google Scholar
  4. Chkhikvadze, V. M. (1987). O sistematicheskom polozhenii dal’nevostochnogo trioniksa. Bulletin of the Academy of Sciences of the Georgian SSR, 128, 609–611.Google Scholar
  5. Choo, B. L., & Chou, L. M. (1992). Does incubation temperature influence the sex of embryos in Trionyx sinensis? Journal of Herpetology, 26, 341–342.CrossRefGoogle Scholar
  6. Clement, M., Posada, D., & Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1660.CrossRefPubMedGoogle Scholar
  7. Diesmos, A. C., Brown, R. M., Alcala, A. C., & Sison, R. V. (2008). Status and distribution of nonmarine turtles of the Philippines. Chelonian Conservation and Biology, 7, 157–177.CrossRefGoogle Scholar
  8. Donnelly, P., & Tavaré, S. (1986). The ages of alleles and a coalescent. Advances in Applied Probability, 18, 1–19.CrossRefGoogle Scholar
  9. Engstrom, T. N., Shaffer, H. B., & McCord, W. P. (2002). Phylogenetic diversity of endangered and critically endangered Asian softshell turtles (Trionychidae: Chitra). Biological Conservation, 104, 173–179.CrossRefGoogle Scholar
  10. Engstrom, T. N., Shaffer, H. B., & McCord, W. P. (2004). Multiple data sets, high homoplasy, and phylogeny of softshell turtles (Testudines: Trionychidae). Systematic Biology, 53, 693–710.CrossRefPubMedGoogle Scholar
  11. Ernst, C. H., & Barbour, R. W. (1989). Turtles of the world. Washington: Smithsonian Institution.Google Scholar
  12. Ernst, C. H., Altenburg, R. G. M., & Barbour, R. W. (2000). Turtles of the world, ver. 1.2. CD-ROM. Amsterdam: ETI BioInformatics.Google Scholar
  13. Fritz, U., & Bininda-Emonds, O. R. P. (2007). When genes meet nomenclature: tortoise phylogeny and the shifting generic concepts of Testudo and Geochelone. Zoology, 110, 298–307.CrossRefPubMedGoogle Scholar
  14. Fritz, U., & Havaš, P. (2007). Checklist of chelonians of the world. Vertebrate Zoology, 57, 149–368.Google Scholar
  15. Fritz, U., & Obst, F. J. (1999). Neue Schildkröten aus Südostasien. Teil II. Bataguridae (Cyclemys, Heosemys, Mauremys, Ocadia, Pyxidea, Sacalia) und Trionychidae. Sauria, 21, 11–26.Google Scholar
  16. Fritz, U., Auer, M., Bertolero, A., Cheylan, M., Fattizzo, T., Hundsdörfer, A. K., et al. (2006). A rangewide phylogeography of Hermann’s tortoise, Testudo hermanni (Reptilia: Testudines: Testudinidae): implications for taxonomy. Zoologica Scripta, 35, 531–543.CrossRefGoogle Scholar
  17. Fritz, U., Ayaz, D., Buschbom, J., Kami, H. G., Mazanaeva, L. F., Aloufi, A. A., et al. (2008a). Go east: phylogeographies of Mauremys caspica and M. rivulata—discordance of morphology, mitochondrial and nuclear genomic markers and rare hybridization. Journal of Evolutionary Biology, 21, 527–540.CrossRefGoogle Scholar
  18. Fritz, U., Guicking, D., Auer, M., Sommer, R. S., Wink, M., & Hundsdörfer, A. K. (2008b). Diversity of the Southeast Asian leaf turtle genus Cyclemys: how many leaves on its tree of life? Zoologica Scripta, 37, 367–390.CrossRefGoogle Scholar
  19. Gustincich, S., Manfioletti, G., del Sal, G., Schneider, C., & Carninci, C. (1991). A fast method for high-quality genomic DNA extraction from whole human blood. BioTechniques, 11, 298–302.PubMedGoogle Scholar
  20. Hall, T. A. (1999). BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.Google Scholar
  21. Huelsenbeck, J. P., & Ronquist, F. (2001). MrBAYES. Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.CrossRefPubMedGoogle Scholar
  22. IUCN = International Union for the Conservation of Nature and Natural Resources. (2009). IUCN red list of threatened species. Version 2009.1. Accessed 23 May 2009.
  23. Iverson, J. B. (1992). A revised checklist with distribution maps of the turtles of the world. Richmond: Privately printed.Google Scholar
  24. Jensen, K. A., & Das, I. (2008). Cultural exploitation of freshwater turtles in Sarawak, Malaysian Borneo. Chelonian Conservation and Biology, 7, 281–285.CrossRefGoogle Scholar
  25. Ji, X., Chen, F., Du, W.-G., & Chen, H.-L. (2003). Incubation temperature affects hatchling growth but not sexual phenotype in the Chinese soft-shelled turtle, Pelodiscus sinensis (Trionychidae). Journal of Zoology, 261, 409–416.CrossRefGoogle Scholar
  26. Jung, S.-O., Lee, Y.-M., Kartavtsev, Y., Park, I.-S., Kim, D. S., & Lee, J.-S. (2006). The complete mitochondrial genome of the Korean soft-shelled turtle Pelodiscus sinensis. DNA Sequence, 17, 471–483.Google Scholar
  27. Kawai, A., Nishida-Umehara, C., Ishijima, J., Tsuda, Y., Ota, H., & Matsuda, Y. (2007). Different origins of bird and reptile sex chromosomes inferred from comparative mapping of chicken Z-linked genes. Cytogenetic and Genome Research, 117, 92–102.CrossRefPubMedGoogle Scholar
  28. Kocher, T. D., Thomas, W. K., Meyer, A., Edwards, S. V., Pääbo, S., Villablanca, F. X., et al. (1989). Dynamics of mitochondrial DNA evolution in mammals: amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences of the United States of America, 86, 6196–6200.CrossRefPubMedGoogle Scholar
  29. Le, M., Raxworthy, C. J., McCord, W. P., & Mertz, L. (2006). A molecular phylogeny of tortoises (Testudines: Testudinidae) based on mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 40, 517–531.CrossRefPubMedGoogle Scholar
  30. Maran, J. (2003). Visite d’une ferme à tortues au Vietnam. Manouria, 6, 8–12.Google Scholar
  31. McGaugh, S. E., Eckerman, C. M., & Janzen, F. J. (2008). Molecular phylogeography of Apalone spinifera. Zoologica Scripta, 37, 289–304.CrossRefGoogle Scholar
  32. Mertens, R., & Wermuth, H. (1955). Die rezenten Schildkröten, Krokodile und Brückenechsen. Zoologische Jahrbücher / Abteilung für Systematik, Ökologie und Geographie der Tiere, 83, 323–440.Google Scholar
  33. Meylan, P. A. (1987). The phylogenetic relationships of soft-shelled turtles (family Trionychidae). Bulletin of the American Museum of Natural History, 186, 1–101.Google Scholar
  34. Meylan, P. A., & Gaffney, E. S. (1992). Sinaspideretes is not the oldest trionychid turtle. Journal of Vertebrate Paleontology, 12, 257–259.Google Scholar
  35. Naro-Maciel, E., Le, M., FitzSimmons, N. N., & Amato, G. (2008). Evolutionary relationships of marine turtles: a molecular phylogeny based on nuclear and mitochondrial genes. Molecular Phylogenetics and Evolution, 49, 659–662.CrossRefPubMedGoogle Scholar
  36. Nessov, L. A. (1995). On some Mesozoic turtles of the Fergana Depression (Kyrgyzstan) and Dzhungar Alatau Ridge (Kazakhstan). Russian Journal of Herpetology, 2, 134–141.Google Scholar
  37. Nie, L.-W., Guo, C.-W., & Wang, Q. (2001). Sex determination mechanism of Trionyx sinensis. Chinese Journal of Applied and Environmental Biology, 7, 258–261.Google Scholar
  38. Nurizan, A., & Ong, B. L. (1997). Some problems of cultured soft-shell turtle (Pelodiscus sinensis) in Peninsular Malaysia. Jurnal Veterinar Malaysia, 9, 27–28.Google Scholar
  39. Posada, D., & Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817–818.CrossRefPubMedGoogle Scholar
  40. Posada, D., & Crandall, K. A. (2001). Intraspecific gene genealogies: trees grafting into networks. TREE, 16, 37–45.PubMedGoogle Scholar
  41. Praschag, P., Hundsdörfer, A. K., Reza, A. H. M. A., & Fritz, U. (2007). Genetic evidence for wild-living Aspideretes nigricans and a molecular phylogeny of South Asian softshell turtles (Reptilia: Trionychidae: Aspideretes, Nilssonia). Zoologica Scripta, 36, 301–310.CrossRefGoogle Scholar
  42. Ran, C.-X., & Yuan, C.-G. (2004). The incubation temperature and the sex determination of Trionyx sinensis. Journal of Fujian Fisheries, 25, 51–53.Google Scholar
  43. Ronquist, F., & Huelsenbeck, J. P. (2003). MrBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.CrossRefPubMedGoogle Scholar
  44. Sato, H., & Ota, H. (1999). False biogeographical pattern derived from artificial animal transportations: a case of the soft-shelled turtle, Pelodiscus sinensis, from the Ryukyu Archipelago, Japan. Developments in Animal and Veterinary Sciences, 29, 317–334.Google Scholar
  45. Shi, H. T., Parham, J. F., Fan, Z. Y., Hong, M. L., & Yin, F. (2008). Evidence for the massive scale of turtle farming in China. Oryx, 42, 147–150.Google Scholar
  46. Spinks, P. Q., & Shaffer, H. B. (2005). Range-wide molecular analysis of the western pond turtle (Emys marmorata): cryptic variation, isolation by distance, and their conservation implications. Molecular Ecology, 14, 2047–2064.CrossRefPubMedGoogle Scholar
  47. Spinks, P. Q., Shaffer, H. B., Iverson, J. B., & McCord, W. P. (2004). Phylogenetic hypotheses for the turtle family Geoemydidae. Molecular Phylogenetics and Evolution, 32, 164–182.CrossRefPubMedGoogle Scholar
  48. Stephens, M., & Donnelly, P. (2003). A comparison of Bayesian methods for haplotype reconstruction. American Journal of Human Genetics, 73, 1162–1169.CrossRefPubMedGoogle Scholar
  49. Stephens, M., Smith, N. J., & Donnelly, P. (2001). A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics, 68, 978–989.CrossRefPubMedGoogle Scholar
  50. Stuart, B. L., & Parham, J. F. (2004). Molecular phylogeny of the critically endangered Indochinese box turtle (Cuora galbinifrons). Molecular Phylogenetics and Evolution, 31, 164–177.CrossRefPubMedGoogle Scholar
  51. Swofford, D. L. (2002). PAUP*. Phylogenetic analysis using parsimony (*and other methods), ver. 4.0b10. Sunderland: Sinauer.Google Scholar
  52. Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.CrossRefPubMedGoogle Scholar
  53. Tang, Y. (1997). Research on a new species of Pelodiscus, Trionychidae in China. Zoological Research / Kunming Institute of Zoology, 18, 13–17 [in Chinese, with English abstract].Google Scholar
  54. van Dijk, P. P., Stuart, B. L., & Rhodin, A. G. J. (Eds.) (2000). Asian turtle trade. Proceedings of a workshop on conservation and trade of freshwater turtles and tortoises in Asia. Phnom Penh, Cambodia, 1–4 December 1999. Chelonian Research Monographs, 2, 1–164.Google Scholar
  55. Vargas-Ramírez, M., Castaño-Mora, O. V., & Fritz, U. (2008). Molecular phylogeny and divergence times of ancient South American and Malagasy river turtles (Testudines: Pleurodira: Podocnemididae). Organisms Diversity and Evolution, 8, 388–398.CrossRefGoogle Scholar
  56. Weisrock, D. W., & Janzen, F. J. (2000). Comparative molecular phylogeography of North American softshell turtles (Apalone): implications for regional and wide-scale historical evolutionary forces. Molecular Phylogenetics and Evolution, 14, 152–164.CrossRefPubMedGoogle Scholar
  57. Wermuth, H., & Mertens, R. (1961). Schildkröten, Krokodile, Brückenechsen. Jena: Fischer.Google Scholar
  58. Wermuth, H., & Mertens, R. (1977). Testudines, Crocodylia, Rhynchocephalia. Das Tierreich, 100, i–xxvii + 1–174.Google Scholar
  59. Zhang, L., Hua, N., & Sun, S. (2008). Wildlife trade, consumption and conservation awareness in southwest China. Biodiversity and Conservation, 17, 1493–1516.CrossRefGoogle Scholar
  60. Zhao, E.-M., & Adler, K. (1993). Herpetology of China. Oxford: Society for the Study of Amphibians and Reptiles.Google Scholar
  61. Zhou, G., Zhang, X., & Fang, Z. (1991). Bulletin of a new species Trionyx. Acta Scientiarum Naturalium Universitatis Normalis Hunanensis, 14, 379–382 [in Chinese, with English abstract].Google Scholar
  62. Zhu, D.-Y., & Sun, X.-Z. (2000). Sex determination in Trionyx sinensis. Chinese Journal of Zoology, 35, 37–38.Google Scholar

Copyright information

© Gesellschaft fuer Biologische Systematik 2010

Authors and Affiliations

  • Uwe Fritz
    • 1
    Email author
  • Shiping Gong
    • 2
  • Markus Auer
    • 1
  • Gerald Kuchling
    • 3
  • Norbert Schneeweiß
    • 4
  • Anna K. Hundsdörfer
    • 1
  1. 1.Museum of Zoology (Museum für Tierkunde)Senckenberg Natural History Collections DresdenDresdenGermany
  2. 2.Guangdong Provincial Public Laboratory for Wild Animal Conservation and ManagementSouth China Institute of Endangered AnimalsGuangzhouPeoples’ Republic of China
  3. 3.School of Animal BiologyThe University of Western AustraliaPerthAustralia
  4. 4.Landesumweltamt BrandenburgNaturschutzstation RhinluchLinumGermany

Personalised recommendations