Abstract
Platt sinuosus Roberts & Bullard n. g., n. sp. (type-species) infects the kidney and mesenteric blood vessels of Mekong snail-eating turtles, Malayemys subtrijuga (Schlegel & Müller), in the Mekong River Basin. Species of Platt Roberts & Bullard n. g. are unique by the combination of having a papillate ventral sucker, vasa efferentia that are dorsal to the gonads, a massive cirrus-sac that is directed anteriad or laterad, and a vitellarium that surrounds the intestinal caeca. The new species resembles Platt ocadiae (Takeuti, 1942) Roberts & Bullard n. comb. but differs from it by having an external seminal vesicle that overlaps with or is immediately posterior to the level of the ventral sucker. Seven species previously of Hapalorhynchus Stunkard, 1922 are reassigned herein to Platt: P. odhnerensis (Mehra, 1933) Roberts & Bullard n. comb.; P. yoshidai (Ozaki, 1939) Roberts & Bullard n. comb.; P. ocadiae; P. oschmarini (Belous, 1963) Roberts & Bullard n. comb.; P. sutlejensis (Mehrotra, 1973) Roberts & Bullard n. comb.; P. synderi (Platt & Sharma, 2012) Roberts & Bullard n. comb.; and P. tkachi (Platt & Sharma, 2012) Roberts & Bullard n. comb. A dichotomous key to Platt spp. is provided. Hapalorhynchus sheilae (Mehrotra, 1973) Bourgat, 1990 and Hapalorhynchus mica (Oshmarin, 1971) Bourgat, 1990 are considered as species inquirendae, and Hapalorhynchus indicus (Thapar, 1933) Price, 1934 and Hapalorhynchus macrotesticularis (Rohde, Lee, & Lim, 1968) Brooks & Sullivan, 1981 are considered as species incertae sedis. Phylogenetic analysis of the large subunit rDNA (28S) showed P. sinuosus and P. snyderi to be sister taxa distinct from a monophyletic Hapalorhynchus and Coeuritrema platti Roberts & Bullard, 2016.
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References
Anderson, G. R., & Barker, S. C. (1998). Inference of phylogeny and taxonomy within the Didymozoidae (Digenea) from the second internal transcribed spacer (ITS2) of ribosomal DNA. Systematic Parasitology, 41, 87–94.
Brant, S. V., & Loker, E. S. (2005). Can specialized pathogens colonize distantly related hosts? Schistosome evolution as a case study. PLoS Pathogens, 1, e38.
Belous, E. V. (1963). Helminth fauna of water turtles, Amyda sinensis, of the Far East. Helminthologia, 4, 79–99 (In Russian).
Chapman, P. A., Cribb, T. H., Blair, D., Traub, R. J., Kyaw-Tanner, M. T., Flint, M., et al. (2015). Molecular analysis of the genera Hapalotrema Looss, 1899 and Learedius Price, 1934 (Digenea: Spirorchiidae) reveals potential cryptic species, with comments on the validity of the genus Learedius. Systematic Parasitology, 90, 67–79.
Cribb, T. H., Anderson, G. R., Adlard, R. D., & Bray, R. A. (1998). A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). International Journal for Parasitology, 28, 1,791–1,795.
Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.
Dwivedi, M. P. (1967). Contribution to the family Spirorchiidae Stunkard, 1921 (Digenea: Trematoda). Indian Journal of Helminthology, 19, 1–14.
ICZN. (2012). International Commission on Zoological Nomenclature: Amendment of articles 8, 9, 10, 21 and 78 of the International Code of Zoological Nomenclature to expand and refine methods of publication. Bulletin of Zoological Nomenclature, 69, 161–169.
Katoh, K., & Standley, D. M. (2013). MAFFT Multiple Sequence Alignment Software Version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.
Lockyer, A. E., Olson, P. D., Ostergaard, P., Rollinson, D., Johnston, D. A., Attwood, S. W., et al. (2003). The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology, 126, 203–224.
Maddison, W. P., & Maddison, D. R. (2017). Mesquite: a modular system for evolutionary analysis. Version 3.2 http://mesquiteproject.org. Accessed on 3 June 2017.
Mehra, H. R. (1933). New blood flukes of the family Spirorchidae Stunkard from Indian fresh-water tortoises with discussion on the synonymy of certain genera and the relationships of the families of blood flukes. Part I. Bulletin of the Academy of Sciences of the United Provinces of Agra and Oudh, India, 2, 203–225.
Mehrotra, V. (1973). Digenea from some reptile hosts in India, Part II (in continuation with Abstract No. 286 in Part III of the Proceedings). Proceedings of the Sixtieth Indian Science Congress, 4, 46–47.
Oshmarin, P. G. (1971). [A new species of trematode from the blood vessels of Chelonia.] In: Parazity Zhivotnykh I Rasternii Dal’nego Vostoka. Vladivostok, USSR: Dal’nevostochnoe Knizhnoe Izdatel’stvo, pp. 142–143 (In Russian).
Ozaki, Y. (1939). [A new blood-fluke Hapalorhynchus yoshidai.] Volumen Jubilare pro Professore Sadao Yoshida, Osaka, 1, 29–37 (In Japanese; English summary pp. 34–35).
Platt, T. R. (1922). Family Spirorchiidae Stunkard, 1921.In: Gibson, D. I., Jones, A. J. & Bray, R. A. (Eds), Keys to the Trematoda, Volume 1. Wallingford: CABI Publishing, pp. 453–468.
Platt, T. R., & Sharma, R. S. K. (2012). Two new species of Hapalorhynchus (Digenea: Spirorchiidae) from freshwater turtles (Testudines: Geoemydidae) in Malaysia. Comparative Parasitology, 79, 202–207.
Roberts, J. R., Halanych, K. M., Arias, C. R., Folt, B., Goessling, J. M., & Bullard, S. A. (2017). Emendation and new species of Hapalorhynchus Stunkard, 1922 (Digenea: Schistosomatoidea) from musk turtles (Kinosternidae: Sternotherus) in Alabama and Florida rivers. Parasitology International, 66, 748–760.
Roberts, J. R., Orélis-Ribeiro, R., Dang, B. T., Halanych, K. M., & Bullard, S. A. (2016a). Blood flukes of Asiatic softshell turtles: revision of Coeuritrema Mehra, 1933 (Digenea: Schistosomatoidea) and a new species infecting Chinese softshell turtles, Pelodiscus sinensis, (Trionychidae) from the Da Rang River, VietnamFolia Parasitologica, 63, 031.
Roberts, J. R., Orélis-Ribeiro, R., Halanych, K. M., Arias, C. R., & Bullard, S. A. (2016b). A new species of Spirorchis MacCallum, 1918 (Digenea: Schistosomatoidea) and Spirorchis cf. scripta from chicken turtle, Deirochelys reticularia, (Emydidae), with an emendation and molecular phylogeny of Spirorchis. Folia Parasitologica, 63, 041.
Roberts, J. R., Platt, T. R., Orélis-Ribeiro, R., & Bullard, S. A. (2016c). New genus of blood fluke (Digenea: Schistosomatoidea) from Malaysian freshwater turtles (Geoemydidae) and its phylogenetic position within Schistosomatoidea. Journal of Parasitology, 102, 451–462.
Rohde, K., Lee, S. K., & Lim, H. W. (1968). Ueber drei malayische Trematoden. Annales de Parasitologie Humaine et Comparée, 43, 33–43.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.
Smith, J. W. (1997a). The blood flukes (Digenea: Sanguinicolidae and Spirorchidae) of cold-blooded vertebrates: Part I. A review of the literature published since 1971, and bibliography. Helminthological Abstracts, 66, 255–294.
Smith, J. W. (1997b). The blood flukes (Digenea: Sanguinicolidae and Spirorchidae) of cold-blooded vertebrates: Part II. Appendix I: Comprehensive parasite-host list; Appendix II: Comprehensive host-parasite list. Helminthological Abstracts, 66, 329–344.
Snyder, S. D. (2004). Phylogeny and paraphyly among tetrapod blood flukes (Digenea: Schistosomatidae and Spirorchiidae). International Journal Parasitology, 34, 1385–1392.
Takeuti, E. (1942). New blood flukes of the family Spirorchidae from Japanese fresh-water tortoise and marine turtles. Japanese Journal of Medical Sciences, VI, Bacteriology and Parasitology, 2, 161–174.
Tandon, V., & Gupta, N. K. (1982). On some blood flukes (Spirorchiidae: Coeuritrematinae) from freshwater chelonians in India. Proceedings of the Indian Academy of Sciences (Animal Science), 91, 275–282.
Tandon, V., & Gupta, N. K. (1985). On the blood fluke, Cardiotrema roparensis Mehrotra, 1973 and validity of C. longivesticulata Dwivedi, 1967 (Spirorchiidae: Coeuritrematinae). Research Bulletin (Science) of the Panjab University, 36, 331–334.
Thapar, G. S. (1933). A new blood fluke from an Indian tortoise, Trionyx gangeticus. Journal of Helminthology, 11, 163–168.
van Dijk, P. P., Iverson, J. B., Rhodin, A. G. J., Shaffer, H. B., & Bour, R. (2014). Turtles of the world, 7th Edition: Annotated checklist of taxonomy, synonymy, distribution with maps, and conservation status. Chelonian Research Monographs, 5, 329–479.
Acknowledgements
We thank Raphael Orélis-Ribeiro (Curitiba, Brazil) for generating the gene sequence data for the new species; Colin Cai and Stacey LaFrentz (Auburn University) for laboratory assistance in generating molecular data; Matthew Womble (National Oceanic and Atmospheric Administration, Washington DC) for helping collect parasites; and Estefania Rodriguez (AMNH), Anna Philips, Chad Walter, and William Moser (all USNM) for loaning museum specimens.
Funding
This study was supported financially by and is a contribution of the Southeastern Cooperative Fish Parasite and Disease Project. Initial funding was provided by several grants from the National Science Foundation’s (NSF) Division of Environmental Biology (NSF-DEB 1112729, 1051106, 1048523) to SAB and KMH as well as by an NSF grant to stimulate research and collaborative work in the Mekong River Basin awarded to Herbert “Bert” H. Covert (University of Colorado, Boulder, Colorado).
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This article was registered in the Official Register of Zoological Nomenclature (ZooBank) as EA5233B0-DCF8-4890-8762-37EBFEB5C14E. This article was published as an Online First article on the online publication date shown on this page. The article should be cited by using the doi number. This is the Version of Record.
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Roberts, J.R., Arias, C.R., Halanych, K.M. et al. A new genus and species of turtle blood fluke (Digenea: Schistosomatoidea) from the Mekong snail-eating turtle, Malayemys subtrijuga (Schlegel & Müller) (Testudines: Geoemydidae) in Vietnam, with a reassessment of related Asiatic turtle blood flukes and molecular phylogeny. Syst Parasitol 95, 133–145 (2018). https://doi.org/10.1007/s11230-017-9772-y
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DOI: https://doi.org/10.1007/s11230-017-9772-y