Cryptic diversity of limestone karst inhabiting land snails (Cyclophorus spp.) in northern Vietnam, their evolutionary history and the description of four new species

English version

Autoři: Katharina C. M. von Oheimb ^aff001; Parm Viktor von Oheimb ^aff001; Takahiro Hirano ^aff003; Tu Van Do ^aff004; Jonathan Ablett ^aff001; Hao Van Luong ^aff006; Sang Van Pham ^aff007; Fred Naggs ^aff001
Působiště autorů: Life Sciences Department, The Natural History Museum, London, England, United Kingdom ^aff001; Museum für Naturkunde – Leibniz Institute for Evolution and Biodiversity Science, Berlin, Germany ^aff002; Department of Biological Sciences, University of Idaho, Moscow, Idaho, United States of America ^aff003; Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, Ha Noi, Vietnam ^aff004; Graduate University of Science and Technology, Vietnam Academy of Science and Technology, Ha Noi, Vietnam ^aff005; Centre for Rescue and Conservation of Organisms, Hoang Lien National Park, Sa Pa, Vietnam ^aff006; Department of Specimen Preparation and Exhibitive Design, Vietnam National Museum of Nature, Vietnam Academy of Science and Technology, Ha Noi, Vietnam ^aff007
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222163

Souhrn

Limestone karsts can form terrestrial habitat islands for calcium-dependent organisms. In Vietnam, many karst habitats are threatened, while their rich biodiversity is still far from being thoroughly explored. Given that conservation of karst biota strongly relies on correct species identification, the presence of undetected cryptic species can pose severe problems. The present study focuses on cryptic diversity among karst-inhabiting land snails of the genus Cyclophorus in northern Vietnam, where specimens with a similar shell morphology have been reported from various regions. In order to examine the diversity and evolutionary history of this “widespread morphotype”, we generated a Bayesian phylogeny based on DNA sequence data. Automatic Barcode Gap Discovery (ABGD) and the Bayesian implementation of the Poisson tree processes model (bPTP) contributed to species delimitation and analyses of shell shape and size aided the morphological characterisation of individual species. We found that the examined specimens of the widespread morphotype did not form a single monophyletic group in the phylogeny but clustered into several different clades. We delimited nine different species that develop the widespread morphotype and described four of them as new. Processes of convergent evolution were probably involved in the origin of the delimited species, while their generally allopatric distribution could result from interspecific competition. Our findings indicate ongoing processes of speciation and a potential case of morphological character displacement. The high degree of morphological overlap found among the species underlines the importance of DNA sequence data for species delimitation and description in the genus Cyclophorus. Given the findings of the present study and the high potential that as yet undiscovered cryptic taxa have also evolved in other groups of karst-inhabiting organisms, we argue for a systematic and efficient detection and description of Vietnam’s karst biodiversity to provide a solid basis for future conservation planning.

Klíčová slova:

Phylogenetic analysis – Ethanol – Species delimitation – New species reports – Vietnam – Limestone – Cryptic speciation – Karst features

Zdroje

1. Tweedie MWF. On certain Mollusca of the Malayan limestone hills. Bull Raffles Mus. 1961;26: 49–65.

2. Clements R, Ng PKL, Lu XX, Ambu S, Schilthuizen M, Bradshaw CJA. Using biogeographical patterns of endemic land snails to improve conservation planning for limestone karsts. Biol Conserv. 2008;141: 2751–2764.

3. Gao Y, Ai B, Kong H, Kang M, Huang H. Geographical pattern of isolation and diversification in karst habitat islands: a case study in the Primulina eburnea complex. J Biogeogr. 2015;42: 2131–2144.

4. Clements R, Sodhi NS, Schilthuizen M, Ng PKL. Limestone karsts of Southeast Asia: imperiled arks of biodiversity. BioScience. 2006;56: 733–742.

5. Tongkerd P, Lee T, Panha S, Burch JB, Ó Foighil D. Molecular phylogeny of certain Thai gastrocoptine micro land snails (Stylommatophora: Pupillidae) inferred from mitochondrial and nuclear ribosomal DNA sequences. J Molluscan Stud. 2004;70: 139–147.

6. von Oheimb PV, von Oheimb KCM, Hirano T, Do TV, Luong HV, Ablett J, et al. Competition matters: Determining the drivers of land snail community assembly among limestone karst areas in northern Vietnam. Ecol Evol. 2018;8: 4136–4149. doi: 10.1002/ece3.3984 29721286

7. Schilthuizen M, Liew T- S, Bin Elahan B, Lackman-Ancrenaz I. Effects of karst forest degradation on pulmonate and prosobranch land snail communities in Sabah, Malaysian Borneo. Conserv Biol. 2005;19: 949–954.

8. Do T. Characteristics of karst ecosystems of Vietnam and their vulnerability to human impact. Acta Geol Sin. 2001;75: 325–329.

9. Fong-Sam Y. The mineral industry of Vietnam. In: U.S. Geological Survey, editor. Minerals yearbook, area reports: international 2009, Asia and the Pacific, volume III. Washington: United States Government Printing Office; 2011. pp. 28.1–28.8.

10. Fong-Sam Y. The mineral industry of Vietnam [advance release]. In: U.S. Geological Survey, editor. Minerals yearbook, area reports: international 2015, Asia and the Pacific, volume III. Washington: United States Government Printing Office; 2018. pp. 30.1–30.13.

11. Vermeulen JJ. Notes on the non-marine molluscs of the island of Borneo 6. The genus Opisthostoma (Gastropoda Prosobranchia: Diplommatinidae), part 2. Basteria. 1994;58: 75–191.

12. Sterling EJ, Hurley MM. Conserving biodiversity in Vietnam: applying biogeography to conservation research. Proc Calif Acad Sci. 2005;56: 98–118.

13. Sterling EJ, Hurley MM, Le MD. Vietnam: a natural history. New Haven, London: Yale University Press; 2006

14. Alström P, Davidson P, Duckworth JW, Eames JC, Le TT, Nguyen C, et al. Description of a new species of Phylloscopus warbler from Vietnam and Laos. Ibis. 2010;152: 145–168.

15. Gueidan C, Do TV, Lu NT. Phylogeny and taxonomy of Staurothele (Verrucariaceae, lichenized ascomycetes) from the karst of northern Vietnam. Lichenologist. 2014;46: 515–533.

16. Nguyen SN, Yang J-X, Le T-NT, Nguyen LT, Orlov NL, Hoang CV, et al. DNA barcoding of Vietnamese bent-toed geckos (Squamata: Gekkonidae: Cyrtodactylus) and the description of a new species. Zootaxa. 2014;3784: 48–66. doi: 10.11646/zootaxa.3784.1.2 24872031

17. Do TV, Le TV, Phan DD. Binhthuanomon vinhtan, a new genus and new species of semi-terrestrial freshwater crab (Crustacea: Decapoda: Brachyura: Potamidae) from south central Vietnam. Zootaxa. 2015;4052: 117–126. doi: 10.11646/zootaxa.4052.1.6 26624780

18. Leong-Škorničková J, Nguyen BQ, Tran DH, Šída O, Rybková R, Truong VB. Nine new Zingiber species (Zingiberaceae) from Vietnam. Phytotaxa. 2015;219: 201–220.

19. Nguyen TT, Pham CT, Nguyen TQ, Ninh HT, Ziegler T. A new species of Rhacophorus (Amphibia: Anura: Rhacophoridae) from Vietnam. Asian Herpetol Res. 2017;8: 221–234.

20. Páll-Gergely B, Szekeres M. New and little-known Clausiliidae (Gastropoda: Pulmonata) from Laos and southern Vietnam. J Conchol. 2017;42: 507–521.

21. Vu DV, Pham GM, Nguyen CN, Do T, Arctander P, MacKinnon J. A new species of living bovid from Vietnam. Nature. 1993;363: 443–445.

22. Giao PM, Tuoc D, Dung VV, Wikramanayake ED, Amato G, Arctander P, et al. Description of Muntiacus truongsonensis, a new species of muntjac (Artiodactyla: Muntiacidae) from central Vietnam, and implications for conservation. Anim Conserv. 1998;1: 61–68.

23. Kuznetsov A, Guigue AM. The forests of Vu Quang Nature Reserve: a description of habitats and plant communities. Ha Noi: Vu Quang Nature Reserve Conservation Project; 2000.

24. Eames JC, Eve R, Tordoff AW. The importance of Vu Quang Nature Reserve, Vietnam, for bird conservation, in the context of the Annamese Lowlands Endemic Bird Area. Bird Conserv Int. 2001;11: 247–285.

25. Vermeulen JJ, Maassen WJM. The non-marine mollusk fauna of the Pu Luong, Cuc Phuong, Phu Ly, and Ha Long regions in northern Vietnam. A survey for the Vietnam Programme of FFI (Flora and Fauna International). 2003.

26. Furey NM, Mackie IJ, Racey PA. Bat diversity in Vietnamese limestone karst areas and the implications of forest degradation. Biodivers Conserv. 2010;19: 1821–1838.

27. Jestrzemski D, Schütz S, Nguyen TQ, Ziegler T. A survey of amphibians and reptiles in Chu Mom Ray National Park, Vietnam, with implications for herpetofaunal conservation. Asian J Conserv Biol. 2013;2: 88–110.

28. Brooks TM, Mittermeier RA, da Fonseca GAB, Gerlach J, Hoffmann M, Lamoreux JF, et al. Global biodiversity conservation priorities. Science. 2006;313: 58–61. doi: 10.1126/science.1127609 16825561

29. Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, et al. Cryptic species as a window on diversity and conservation. Trends Ecol Evol. 2007;22: 148–155. doi: 10.1016/j.tree.2006.11.004 17129636

30. Crawford AJ, Cruz C, Griffith E, Ross H, Ibáñez R, Lips KR, et al. DNA barcoding applied to ex situ tropical amphibian conservation programme reveals cryptic diversity in captive populations. Mol Ecol Resour. 2013;13: 1005–1018. doi: 10.1111/1755-0998.12054 23280343

31. Allendorf FW, Leary RF, Spruell P, Wenburg JK. The problems with hybrids: setting conservation guidelines. Trends Ecol Evol. 2001;16: 613–622.

32. Schönrogge K, Barr B, Wardlaw JC, Napper E, Gardner MG, Breen J, et al. When rare species become endangered: cryptic speciation in myrmecophilous hoverflies. Biol J Linn Soc Lond. 2002;75: 291–300.

33. Juan C, Guzik MT, Jaume D, Cooper SJB. Evolution in caves: Darwin’s ‘wrecks of ancient life’ in the molecular era. Mol Ecol. 2010;19: 3865–3880. doi: 10.1111/j.1365-294X.2010.04759.x 20637049

34. Liu H-P, Hershler R, Lang B, Davies J. Molecular evidence for cryptic species in a narrowly endemic western North American springsnail (Pyrgulopsis gilae). Conserv Genet. 2013;14: 917–923.

35. Sturmbauer C, Meyer A. Genetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes. Nature, 1992;358: 578–581. doi: 10.1038/358578a0 1501712

36. Losos JB, Jackman TR, Larson A, de Queiroz K, Rodríguez-Schettino L. Contingency and determinism in replicated adaptive radiations of island lizards. Science. 1998;279: 2115–2118. doi: 10.1126/science.279.5359.2115 9516114

37. Kocher TD, Conroy JA, McKaye KR, Stauffer JR. Similar morphologies of cichlid fish in lakes Tanganyika and Malawi are due to convergence. Mol Phylogenet Evol. 1993;2: 158–165. doi: 10.1006/mpev.1993.1016 8025722

38. Jörger KM, Schrödl M. How to describe a cryptic species? Practical challenges of molecular taxonomy. Front Zool. 2013;10: 1–27.

39. Webb CO, Slik JWF, Triono T. Biodiversity inventory and informatics in Southeast Asia. Biodivers Conserv. 2010;19: 955–972.

40. Stuart BL, Inger RF, Voris HK. High level of cryptic species diversity revealed by sympatric lineages of Southeast Asian forest frogs. Biol Lett. 2006;2: 470–474. doi: 10.1098/rsbl.2006.0505 17148433

41. Gittenberger A, Gittenberger E. Cryptic, adaptive radiation of endoparasitic snails: sibling species of Leptoconchus (Gastropoda: Coralliophilidae) in corals. Org Divers Evol. 2011;11: 21–41.

42. Riedel A, Sagata K, Surbakti S, Tänzler R, Balke M. One hundred and one new species of Trigonopterus weevils from New Guinea. ZooKeys. 2013;280: 1–150.

43. Mutanen M, Pretorius E. Subjective visual evaluation vs. traditional and geometric morphometrics in species delimitation: a comparison of moth genitalia. Syst Entomol. 2007;32: 371–386.

44. Fontaneto D, Flot J-F, Tang CQ. Guidelines for DNA taxonomy, with a focus on the meiofauna. Mar Biodivers. 2015;45: 433–451.

45. Raheem DC, Backeljau T, Pearce-Kelly P, Taylor H, Fenn J, Sutcharit C, et al. An illustrated guide to the land snails and slugs of Vietnam. London, Brussels: The Natural History Museum, the Royal Belgian Institute of Natural Sciences & the Zoological Society of London; 2017.

46. Schilthuizen M. Community ecology of tropical forest snails: 30 years after Solem. Contrib Zool. 2011;80: 1–15.

47. Nantarat N, Tongkerd P, Sutcharit C, Wade CM, Naggs F, Panha S. Phylogenetic relationships of the operculate land snail genus Cyclophorus Montfort, 1810 in Thailand. Mol Phylogenet Evol. 2014;70: 99–111. doi: 10.1016/j.ympev.2013.09.013 24076249

48. Kobelt W. Die gedeckelten Lungenschnecken (Cyclostomacea). In Abbildungen nach der Natur mit Beschreibungen. Dritte Abteilung. Cyclophoridae I. Systematisches Conchylien-Cabinet von Martini und Chemnitz. 1908;1(19): 401–711, pls 51–103.

49. Do SD, Do NV. Family Cyclophoridae in Vietnam (Gastropoda: Cyclophoroidea): the genus Cyclophorus Montfort, 1810. Ruthenica. 2019;29: 1–53.

50. Pfeiffer L. Descriptions of sixty-six new land shells, from the collection of H. Cuming, Esq. Proc Zool Soc Lond. 1852(published in 1854);20: 56–70.

51. Müller OF. Vermium terrestrium et fluviatilium, seu animalium infusoriorum, helminthicorum, et testaceorum, non marinorum, succincta historia. Volumen alterum. Copenhagen, Leipzig: Heineck et Faber; 1774.

52. Dang TN. Overview on the species composition of the landsnails fauna of Vietnam. Tap chi Sinh hoc. 2008;30: 1–15.

53. Do SD, Nguyen HTT, Do NV. A checklist and classification of terrestrial prosobranch snails from Son La, north-western Vietnam. Ruthenica. 2015;25: 117–132.

54. Nguyen BT, Hoang KN, Hoang NV. Species composition of Cyclophoridae (Gastropoda: Prosobranchia) in Than Sa Phuong Hoang Nature Reserve, Thai Nguyen province. Tap chi Khoa hoc DHQGHN: Khoa hoc Tu nhien va Cong nghe. 2017;33(1S): 34–41.

55. Nantarat N, Wade CM, Jeratthitikul E, Sutcharit C, Panha S. Molecular evidence for cryptic speciation in the Cyclophorus fulguratus (Pfeiffer, 1854) species complex (Caenogastropoda: Cyclophoridae) with description of new species. PLOS ONE. 2014;9: e109785. doi: 10.1371/journal.pone.0109785 25299674

56. Sosa BO III, Batomalaque GA, Fontanilla IKC. An updated survey and biodiversity assessment of the terrestrial snail (Mollusca: Gastropoda) species in Marinduque, Philippines. Philipp J Sci. 2014;143: 199–210.

57. Budha PB, Naggs F, Backeljau T. Annotated checklist of the terrestrial gastropods of Nepal. ZooKeys. 2015;492: 1–48.

58. Inkhavilay K, Sutcharit C, Bantaowong U, Chanabun R, Siriwut W, Srisonchai R, et al. Annotated checklist of the terrestrial molluscs from Laos (Mollusca, Gastropoda). ZooKeys. 2019;834: 1–166. doi: 10.3897/zookeys.834.28800 31105437

59. Nantarat N, Sutcharit C, Tongkerd P, Wade CM, Naggs F, Panha S. Phylogenetics and species delimitations of the operculated land snail Cyclophorus volvulus (Gastropoda: Cyclophoridae) reveal cryptic diversity and new species in Thailand. Sci Rep. 2019;9: 7041. doi: 10.1038/s41598-019-43382-5 31065003

60. Naggs F, Panha S, Raheem D. Developing land snail expertise in South and Southeast Asia, a new Darwin Initiative project. Nat Hist J Chulalongkorn Univ. 2006;6: 43–46.

61. Kerney MP, Cameron RAD. A field guide to the land snails of Britain and north-west Europe. Glasgow: William Collins Sons and Co; 1979.

62. Winnepenninckx B, Backeljau T, De Wachter R. Extraction of high molecular weight DNA from molluscs. Trends Genet. 1993;9: 407. doi: 10.1016/0168-9525(93)90102-n 8122306

63. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3: 294–299. 7881515

64. Fehér Z, Németh L, Nicoarǎ A, Szekeres M. Molecular phylogeny of the land snail genus Alopia (Gastropoda: Clausiliidae) reveals multiple inversions of chirality. Zool J Linn Soc. 2013;167: 259–272.

65. Palumbi SR, Martin AP, Romano S, McMillan WO, Stice L, Grabowski G. The simple fool’s guide to PCR. Honolulu: University of Hawaii; 1991.

66. Morgan JAT, DeJong RJ, Jung Y, Khallaayoune K, Kock S, Mkoji GM, et al. A phylogeny of planorbid snails, with implications for the evolution of Schistosoma parasites. Mol Phylogenet Evol. 2002;25: 477–488. 12450752

67. Wade CM, Mordan PB. Evolution within the gastropod molluscs; using the ribosomal RNA gene-cluster as an indicator of phylogenetic relationships. J Molluscan Stud. 2000;66: 565–570.

68. Chang C-T, Tsai C-N, Tang CY, Chen C-H, Lian J-H, Hu C-Y, et al. Mixed Sequence Reader: a program for analyzing DNA sequences with heterozygous base calling. Sci World J. 2012: 365104.

69. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22: 4673–4680. doi: 10.1093/nar/22.22.4673 7984417

70. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41: 95–98.

71. Katoh K, Toh H. Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. BMC Bioinformatics. 2008;9: 212. doi: 10.1186/1471-2105-9-212 18439255

72. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30: 772–780. doi: 10.1093/molbev/mst010 23329690

73. Xia X, Xie Z, Salemi M, Chen L, Wang Y. An index of substitution saturation and its application. Mol Phylogenet Evol. 2003;26: 1–7. 12470932

74. Xia X, Lemey P. Assessing substitution saturation with DAMBE. In: Lemey P, Salemi M, Vandamme A-M, editors. The phylogenetic handbook: a practical approach to phylogenetic analysis and hypothesis testing. 2nd ed. Cambridge: Cambridge University Press; 2009. pp. 611–626.

75. Xia X. DAMBE7: new and improved tools for data analysis in molecular biology and evolution. Mol Biol Evol, 2018;35: 1550–1552. doi: 10.1093/molbev/msy073 29669107

76. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61: 539–542. doi: 10.1093/sysbio/sys029 22357727

77. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE). 2010: 1–8.

78. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9: 772.

79. Huelsenbeck JP, Rannala B. Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst Biol. 2004;53: 904–913. doi: 10.1080/10635150490522629 15764559

80. Rambaut A, Drummond AJ, Xie D, Baele G., Suchard MA. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol. 2018;67: 901–904. doi: 10.1093/sysbio/syy032 29718447

81. Puillandre N, Lambert A, Brouillet S, Achaz G. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol Ecol. 2012;21: 1864–1877. doi: 10.1111/j.1365-294X.2011.05239.x 21883587

82. Zhang J, Kapli P, Pavlidis P, Stamatakis A. A general species delimitation method with applications to phylogenetic placements. Bioinformatics. 2013;29: 2869–2876. doi: 10.1093/bioinformatics/btt499 23990417

83. Hebert PDN, Cywinska A, Ball SL, deWaard JR. Biological identifications through DNA barcodes. Proc Biol Sci. 2003;270: 313–321. doi: 10.1098/rspb.2002.2218 12614582

84. Tielecke H. Anatomie, Phylogenie und Tiergeographie der Cyclophoriden. Arch Naturg (Neue Folge). 1940;9: 317–371.

85. Dang VH, editor. Vietnam national atlas. Ha Noi: The Ministry of Science, Technology and Environment; 1996.

86. Rohlf FJ. tps Utility program version 1.70. 2016. http://life.bio.sunysb.edu/morph/

87. Van Bocxlaer B, Schultheiß R. Comparison of morphometric techniques for shapes with few homologous landmarks based on machine-learning approaches to biological discrimination. Paleobiology. 2010;36: 497–515.

88. Rohlf FJ. tpsDig 2 version 2.30. 2017. http://life.bio.sunysb.edu/morph/

89. Klingenberg CP. MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour. 2011;11: 353–357. doi: 10.1111/j.1755-0998.2010.02924.x 21429143

90. R Core Team. R: a language and environment for statistical computing. 2018. https://www.R-project.org/

91. Barber CB, Habel K, Grasman R, Gramacy RB, Stahel A, Sterratt DC. Package ‘geometry’: mesh generation and surface tesselation. 2015. http://geometry.r-forge.r-project.org/

92. Ancey CF. Mollusques du Haut-Tonkin. Le Naturaliste (2e série). 1888;10: 92–93.

93. Morlet L. Diagnoses de mollusques terrestres et fluviatiles du Tonkin. Paris: Mane et Noble; 1886.

94. Zhang Y, Li S. Ancient lineage, young troglobites: recent colonization of caves by Nesticella spiders. BMC Evol Biol. 2013;13: 183. doi: 10.1186/1471-2148-13-183 24006950

95. Goodfriend GA. Variation in land-snail shell form and size and its causes: a review. Syst Zool. 1986;35: 204–223.

96. Chiba S. Ecological and morphological patterns in communities of land snails of the genus Mandarina from the Bonin Islands. J Evol Biol. 2004;17: 131–143. 15000656

97. Nguyen TN. Shells of Vietnam. Hackenheim: ConchBooks; 2005.

98. Kobelt W. Cyclophoridae. Das Tierreich. 1902;16: 1–662.

99. Renner SS. A return to Linnaeus’s focus on diagnosis, not description: the use of DNA characters in the formal naming of species. Syst Biol. 2016;65: 1085–1095. doi: 10.1093/sysbio/syw032 27146045

100. Kasinathan R. Some studies of five species of cyclophorid snails from Peninsular India. Proc Malacol Soc Lond, 1975;41: 379–394.

101. Benson WH. Geographical notices, and characters of fourteen new species of Cyclostoma, from the East Indies. Ann Mag Nat Hist (second series). 1851;8: 184–195.

102. Egorov R, Greke K. The genus Cyclophorus Montfort, 1810: systematics and nomenclature. Club Conchylia Inf. 2007;38: 57–64.

103. Bouchet P, Rocroi J-P, Hausdorf B, Kaim A, Kano Y, Nützel A, et al. Revised classification, nomenclator and typification of gastropod and monoplacophoran families. Malacologia. 2017;61: 1–526.

104. Raheem DC, Schneider S, Böhme M, Vasiliyan D, Prieto J. The oldest known cyclophoroidean land snails (Caenogastropoda) from Asia. J Syst Palaeontol. 2018;16: 1301–1317.

105. Gray JE. A list of the genera of recent Mollusca, their synonyma and types. Proc Zool Soc Lond. 1847;15: 129–219.

106. Montfort D. Conchyliologie systématique, et classification méthodique des coquilles, vol. 2. Paris: F. Schoell; 1810.

107. Wood H, Gallichan J. The new molluscan names of César-Marie-Felix Ancey including illustrated type material from the National Museum of Wales. Biotir Rep. 2008;3: 1–162.

108. Zilch A. Die Typen und Typoide des Natur-Museums Senckenberg, 17: Mollusca, Cyclophoridae, Cyclophorinae-Cyclophoreae (3). Arch Molluskenkd. 1956;85: 33–54.

109. Morlet L. Liste des coquilles recueillies, au Tonkin, par M. Jourdy, chef d’escadron d’artillerie, et description d’espèces nouvelles. J Conchyliologie. 1886;34: 257–295.

Cryptic diversity of limestone karst inhabiting land snails (Cyclophorus spp.) in northern Vietnam, their evolutionary history and the description of four new species

Souhrn

Klíčová slova:

Zdroje

PLOS One

Získaná hemofilie - Povědomí o nemoci a její diagnostika

Eozinofilní granulomatóza s polyangiitidou